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Schmid"> <meta name="citation_author_orcid" content="0000-0003-1077-5750"> <meta name="citation_author" content="Graham Simmons"> <meta name="citation_author_orcid" content="0000-0002-9615-7023"> <meta name="citation_author" content="Jing Jin"> <meta name="citation_author_orcid" content="0000-0003-3994-8600"> <meta name="citation_author" content="Wah Chiu"> <meta name="citation_author_orcid" content="0000-0002-8910-3078"> <meta name="citation_publication_date" content="2020/01"> <meta name="citation_online_date" content="2020/11/17"> <meta name="citation_volume" content="1"> <meta name="citation_firstpage" content="e11"> <meta name="citation_issn" content="2633-2892"> <meta name="citation_keywords" content="Cryo-EM; human coronavirus NL63; spike trimer"> <meta name="citation_pdf_url" content="https://www.cambridge.org/core/services/aop-cambridge-core/content/view/6566DF036E29EAE203048C708B48B9EB/S2633289220000162a.pdf/div-class-title-a-3-4-aa-cryo-electron-microscopy-structure-of-the-human-coronavirus-spike-trimer-computationally-derived-from-vitrified-nl63-virus-particles-div.pdf"> <meta name="citation_reference" content="citation_title=Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites; citation_author=Belouzard, S; citation_author=Chu, VC; citation_author=Whittaker, GR; citation_publication_date=2009; citation_journal_title=Proceedings of the National Academy of Sciences; citation_volume=106; citation_firstpage=5871; citation_lastpage=5876; citation_doi=10.1073/pnas.0809524106"> <meta name="citation_reference" content="citation_title=The Coronavirus Spike Protein Is a Class I Virus Fusion Protein: Structural and Functional Characterization of the Fusion Core Complex; citation_author=Bosch, BJ; citation_author=van der Zee, R; citation_author=de Haan, CAM; citation_author=Rottier, PJM; citation_publication_date=2003; citation_journal_title=Journal of Virology; citation_volume=77; citation_firstpage=8801; citation_lastpage=8811; citation_doi=10.1128/JVI.77.16.8801-8811.2003"> <meta name="citation_reference" content="citation_title=Features and development of Coot; citation_author=Emsley, P; citation_author=Lohkamp, B; citation_author=Scott, WG; citation_author=Cowtan, K; citation_publication_date=2010; citation_journal_title=Acta Crystallographica Section D Biological Crystallography; citation_volume=66; citation_firstpage=486; citation_lastpage=501; citation_doi=10.1107/S0907444910007493"> <meta name="citation_reference" content="citation_title=PHENIX: a comprehensive Python-based system for macromolecular structure solution; citation_author=Adams, PD; citation_author=Afonine, PV; citation_author=Bunkóczi, G; citation_author=Chen, VB; citation_author=Davis, IW; citation_author=Echols, N; citation_author=Zwart, PH; citation_publication_date=2010; citation_journal_title=Acta Crystallographica Section D Biological Crystallography; citation_volume=66; citation_firstpage=213; citation_lastpage=221; citation_doi=10.1107/S0907444909052925"> <meta name="citation_reference" content="citation_title=Co-circulation of three camel coronavirus species and recombination of MERS-CoVs in Saudi Arabia; citation_author=Sabir, JSM; citation_author=Lam, TTY; citation_author=Ahmed, MMM; citation_author=Li, L; citation_author=Shen, YEM; citation_author=Abo- Aba, S; citation_author=Guan, Y; citation_publication_date=2015; citation_journal_title=Science; citation_volume=351; citation_firstpage=81; citation_lastpage=84; citation_doi=10.1126/science.aac8608"> <meta name="citation_reference" content="Ke, Z, Oton, J, Qu, K, Cortese, M, Zila, V, McKeane, L and Briggs, JAG (2020). 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citation_author=Watanabe, Y; citation_author=Berndsen, ZT; citation_author=Raghwani, J; citation_author=Seabright, GE; citation_author=Allen, JD; citation_author=Pybus, OG; citation_author=Crispin, M; citation_publication_date=2020; citation_journal_title=Nature Communications; citation_volume=11; citation_doi=10.1038/s41467-020-16567-0"> <meta name="citation_abstract" content="Human coronavirus NL63 (HCoV-NL63) is an enveloped pathogen of the family Coronaviridae that spreads worldwide and causes up to 10% of all annual respiratory diseases. HCoV-NL63 is typically associated with mild upper respiratory symptoms in children, elderly and immunocompromised individuals. It has also been shown to cause severe lower respiratory illness. NL63 shares ACE2 as a receptor for viral entry with SARS-CoV-1 and SARS-CoV-2. Here, we present the in situ structure of HCoV-NL63 spike (S) trimer at 3.4-Å resolution by single-particle cryo-EM imaging of vitrified virions without chemical fixative. It is structurally homologous to that obtained previously from the biochemically purified ectodomain of HCoV-NL63 S trimer, which displays a three-fold symmetric trimer in a single conformation. In addition to previously proposed and observed glycosylation sites, our map shows density at other sites, as well as different glycan structures. The domain arrangement within a protomer is strikingly different from that of the SARS-CoV-2 S and may explain their different requirements for activating binding to the receptor. 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Discovery</span> </a></li><li class="page-breadcrumbs__item" data-v-3692cf84><span aria-hidden="true" class="breadcrumbs-wrapper__arrow" data-v-3692cf84>></span><a href="/core/journals/qrb-discovery/volume/F8B5CF3E0096CC946882DA4D8D779FE9" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-3692cf84><span data-v-63dfaf6e>Volume 1</span> </a></li><li class="page-breadcrumbs__item" data-v-3692cf84><span aria-hidden="true" class="breadcrumbs-wrapper__arrow" data-v-3692cf84>></span><span data-v-3692cf84>A 3.4-Å cryo-electron microscopy structure of the human...</span></li></ul></div></div> <div class="language" data-v-3692cf84><ul class="language-switch" data-v-6b1118dd data-v-3692cf84><li aria-label="English" data-v-6b1118dd><span class="language-option current divider" data-v-6b1118dd>English</span></li><li aria-label="Français" data-v-6b1118dd><span role="button" tabindex="0" href="#" lang="fr" class="language-option" data-v-6b1118dd> Français </span></li></ul></div></div></div></div> <div class="container container__modified" data-v-01274b1d>  <div class="row" data-v-01274b1d><div role="complementary" aria-label="table of content" class="column__left" data-v-01274b1d><div class="col journal-container row" data-v-146270e8 data-v-01274b1d><img src="https://static.cambridge.org/covers/QRD_0_0_0/qrb-discovery.jpg" alt="" class="journal__image" data-v-146270e8> <a href="/core/journals/qrb-discovery" class="app-link journal__title app-link__text app-link--underlined" data-v-63dfaf6e data-v-146270e8><span class="text" data-v-63dfaf6e>QRB Discovery </span> </a> <hr aria-hidden="true" class="separator default" data-v-7036083a data-v-146270e8></div>  <div id="toc" class="table-of-content" data-v-01274b1d><h2>Article contents</h2> <div id="toc-list-wrapper" class="table-of-content__wrapper"><ul id="toc-list" class="list"><li class="list__item"><a href="#sec0" class="list__item__link"><span class="toc-title">Abstract</span></a></li> <li class="list__item"><a href="#sec1" class="list__item__link"> <span><div class="toc-title">Introduction</div></span></a></li><li class="list__item"><a href="#sec2" class="list__item__link"> <span><div class="toc-title">Results and discussion</div></span></a></li><li class="list__item"><a href="#sec3" class="list__item__link"> <span><div class="toc-title">Methods</div></span></a></li><li class="list__item"><a href="#sec8" class="list__item__link"> <span><div class="toc-title">Conflicts of Interests</div></span></a></li><li class="list__item"><a href="#sec9" class="list__item__link"> <span><div class="toc-title">Authorship Contributions</div></span></a></li><li class="list__item"><a href="#sec10" class="list__item__link"> <span><div class="toc-title">Data Deposition</div></span></a></li><li class="list__item"><a href="#sec20" class="list__item__link"> <span><div class="toc-title">Open Peer Review</div></span></a></li><li class="list__item"><a href="#sec11" class="list__item__link"> <span><div class="toc-title">Supplementary Materials</div></span></a></li>  <li class="list__item"><a href="#references-list" class="list__item__link"><span class="toc-title">References</span></a></li></ul></div></div></div> <div class="column__main" data-v-01274b1d><div class="row" data-v-01274b1d><div class="column__main__left" data-v-01274b1d><div id="maincontent" class="col" data-v-862424e6 data-v-01274b1d> <hgroup data-v-862424e6><h1 data-v-862424e6>A 3.4-Å cryo-electron microscopy structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles</h1> </hgroup>     <div class="row published-date" data-v-862424e6><p data-v-862424e6> Published online by Cambridge University Press: <strong data-v-862424e6>17 November 2020</strong></p></div>   <div class="contributors-details" data-v-99f6eb26 data-v-862424e6><div class="row contributors" data-v-99f6eb26><div class="col" data-v-99f6eb26><div class="row contributor-type" data-v-792406ce data-v-99f6eb26> <div class="contributor-type__contributor" data-v-792406ce><a href="/core/search?filters%5BauthorTerms%5D=Kaiming%20Zhang&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-792406ce><span data-v-63dfaf6e>Kaiming Zhang</span> </a> <a target="_blank" href="https://orcid.org/0000-0003-0414-4776" data-test-orcid="Kaiming Zhang" class="app-link contributor-type__contributor__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-792406ce><img src="data:image/svg+xml;base64,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" alt="Open the ORCID record for Kaiming Zhang" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span data-v-792406ce>,</span></div><div class="contributor-type__contributor" data-v-792406ce><a href="/core/search?filters%5BauthorTerms%5D=Shanshan%20Li&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-792406ce><span data-v-63dfaf6e>Shanshan Li</span> </a> <a target="_blank" href="https://orcid.org/0000-0002-7041-5960" data-test-orcid="Shanshan Li" class="app-link contributor-type__contributor__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-792406ce><img src="data:image/svg+xml;base64,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" alt="Open the ORCID record for Shanshan Li" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span data-v-792406ce>,</span></div><div class="contributor-type__contributor" data-v-792406ce><a href="/core/search?filters%5BauthorTerms%5D=Grigore%20Pintilie&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-792406ce><span data-v-63dfaf6e>Grigore Pintilie</span> </a> <a target="_blank" href="https://orcid.org/0000-0002-0848-5335" data-test-orcid="Grigore Pintilie" class="app-link contributor-type__contributor__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-792406ce><img src="data:image/svg+xml;base64,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" alt="Open the ORCID record for Grigore Pintilie" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span data-v-792406ce>,</span></div><div class="contributor-type__contributor" data-v-792406ce><a href="/core/search?filters%5BauthorTerms%5D=David%20Chmielewski&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-792406ce><span data-v-63dfaf6e>David Chmielewski</span> </a> <a target="_blank" href="https://orcid.org/0000-0002-4498-7949" data-test-orcid="David Chmielewski" class="app-link contributor-type__contributor__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-792406ce><img src="data:image/svg+xml;base64,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" alt="Open the ORCID record for David Chmielewski" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span data-v-792406ce>,</span></div><div class="contributor-type__contributor" data-v-792406ce><a href="/core/search?filters%5BauthorTerms%5D=Michael%20F.%20Schmid&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-792406ce><span data-v-63dfaf6e>Michael F. Schmid</span> </a> <a target="_blank" href="https://orcid.org/0000-0003-1077-5750" data-test-orcid="Michael F. Schmid" class="app-link contributor-type__contributor__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-792406ce><img src="data:image/svg+xml;base64,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" alt="Open the ORCID record for Michael F. Schmid" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span data-v-792406ce>,</span></div><div class="contributor-type__contributor" data-v-792406ce><a href="/core/search?filters%5BauthorTerms%5D=Graham%20Simmons&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-792406ce><span data-v-63dfaf6e>Graham Simmons</span> </a> <a target="_blank" href="https://orcid.org/0000-0002-9615-7023" data-test-orcid="Graham Simmons" class="app-link contributor-type__contributor__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-792406ce><img src="data:image/svg+xml;base64,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" alt="Open the ORCID record for Graham Simmons" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span data-v-792406ce>,</span></div><div class="contributor-type__contributor" data-v-792406ce><a href="/core/search?filters%5BauthorTerms%5D=Jing%20Jin&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-792406ce><span data-v-63dfaf6e>Jing Jin</span> </a> <a target="_blank" href="https://orcid.org/0000-0003-3994-8600" data-test-orcid="Jing Jin" class="app-link contributor-type__contributor__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-792406ce><img src="data:image/svg+xml;base64,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" alt="Open the ORCID record for Jing Jin" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span data-v-792406ce> and</span></div><div class="contributor-type__contributor" data-v-792406ce><a href="/core/search?filters%5BauthorTerms%5D=Wah%20Chiu&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-792406ce><span data-v-63dfaf6e>Wah Chiu</span> </a> <a target="_blank" href="https://orcid.org/0000-0002-8910-3078" data-test-orcid="Wah Chiu" class="app-link contributor-type__contributor__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-792406ce><img src="data:image/svg+xml;base64,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" alt="Open the ORCID record for Wah Chiu" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span data-v-792406ce></span></div> </div> </div> <div class="col-2 collapse-link" data-v-99f6eb26><a href="#authors-details" data-toggle="collapse" aria-expanded="false" aria-controls="authors-details" class="app-link collapsed app-link__text-icon app-link--secondary reverse" data-v-63dfaf6e data-v-99f6eb26><img src="data:image/svg+xml;base64,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" alt="" class="app-icon icon arrow-down" data-v-d2c09870 data-v-63dfaf6e><span class="text" data-v-63dfaf6e>Show author details </span> </a></div></div> <hr aria-hidden="true" class="separator default" data-v-7036083a data-v-99f6eb26> <dl id="authors-details" class="authors-details collapse" data-v-2edb8da6 data-v-99f6eb26><div data-test-author="Kaiming Zhang" class="row author" data-v-2edb8da6><dt class="col-12 col-sm-2 title" data-v-2edb8da6>Kaiming Zhang</dt> <dd class="col content d-inline d-sm-flex" data-v-2edb8da6><span class="content__title" data-v-2edb8da6>Affiliation:</span> <div class="d-sm-flex flex-column flex-sm-1 d-inline" data-v-2edb8da6><span data-v-2edb8da6><span data-v-2edb8da6>Department of Bioengineering and James H. Clark Center, Stanford University, Stanford, CA94305, USA</span> </span></div></dd></div><div data-test-author="Shanshan Li" class="row author" data-v-2edb8da6><dt class="col-12 col-sm-2 title" data-v-2edb8da6>Shanshan Li</dt> <dd class="col content d-inline d-sm-flex" data-v-2edb8da6><span class="content__title" data-v-2edb8da6>Affiliation:</span> <div class="d-sm-flex flex-column flex-sm-1 d-inline" data-v-2edb8da6><span data-v-2edb8da6><span data-v-2edb8da6>Department of Bioengineering and James H. Clark Center, Stanford University, Stanford, CA94305, USA</span> </span></div></dd></div><div data-test-author="Grigore Pintilie" class="row author" data-v-2edb8da6><dt class="col-12 col-sm-2 title" data-v-2edb8da6>Grigore Pintilie</dt> <dd class="col content d-inline d-sm-flex" data-v-2edb8da6><span class="content__title" data-v-2edb8da6>Affiliation:</span> <div class="d-sm-flex flex-column flex-sm-1 d-inline" data-v-2edb8da6><span data-v-2edb8da6><span data-v-2edb8da6>Department of Bioengineering and James H. Clark Center, Stanford University, Stanford, CA94305, USA</span> </span></div></dd></div><div data-test-author="David Chmielewski" class="row author" data-v-2edb8da6><dt class="col-12 col-sm-2 title" data-v-2edb8da6>David Chmielewski</dt> <dd class="col content d-inline d-sm-flex" data-v-2edb8da6><span class="content__title" data-v-2edb8da6>Affiliation:</span> <div class="d-sm-flex flex-column flex-sm-1 d-inline" data-v-2edb8da6><span data-v-2edb8da6><span data-v-2edb8da6>Graduate Program in Biophysics, Stanford University, Stanford, CA94305, USA</span> </span></div></dd></div><div data-test-author="Michael F. Schmid" class="row author" data-v-2edb8da6><dt class="col-12 col-sm-2 title" data-v-2edb8da6>Michael F. Schmid</dt> <dd class="col content d-inline d-sm-flex" data-v-2edb8da6><span class="content__title" data-v-2edb8da6>Affiliation:</span> <div class="d-sm-flex flex-column flex-sm-1 d-inline" data-v-2edb8da6><span data-v-2edb8da6><span data-v-2edb8da6>Division of CryoEM and Bioimaging, SSRL, SLAC National Accelerator Laboratory, Menlo Park, CA94025, USA</span> </span></div></dd></div><div data-test-author="Graham Simmons" class="row author" data-v-2edb8da6><dt class="col-12 col-sm-2 title" data-v-2edb8da6>Graham Simmons</dt> <dd class="col content d-inline d-sm-flex" data-v-2edb8da6><span class="content__title" data-v-2edb8da6>Affiliation:</span> <div class="d-sm-flex flex-column flex-sm-1 d-inline" data-v-2edb8da6><span data-v-2edb8da6><span data-v-2edb8da6>Vitalant Research Institute, San Francisco, CA94030, USA</span> </span></div></dd></div><div data-test-author="Jing Jin" class="row author" data-v-2edb8da6><dt class="col-12 col-sm-2 title" data-v-2edb8da6>Jing Jin</dt> <dd class="col content d-inline d-sm-flex" data-v-2edb8da6><span class="content__title" data-v-2edb8da6>Affiliation:</span> <div class="d-sm-flex flex-column flex-sm-1 d-inline" data-v-2edb8da6><span data-v-2edb8da6><span data-v-2edb8da6>Vitalant Research Institute, San Francisco, CA94030, USA</span> </span><span data-v-2edb8da6><span data-v-2edb8da6>Division of CryoEM and Bioimaging, SSRL, SLAC National Accelerator Laboratory, Menlo Park, CA94025, USA</span> </span></div></dd></div><div data-test-author="Wah Chiu" class="row author" data-v-2edb8da6><dt class="col-12 col-sm-2 title" data-v-2edb8da6>Wah Chiu*</dt> <dd class="col content d-inline d-sm-flex" data-v-2edb8da6><span class="content__title" data-v-2edb8da6>Affiliation:</span> <div class="d-sm-flex flex-column flex-sm-1 d-inline" data-v-2edb8da6><span data-v-2edb8da6><span data-v-2edb8da6>Department of Bioengineering and James H. Clark Center, Stanford University, Stanford, CA94305, USA</span> </span><span data-v-2edb8da6><span data-v-2edb8da6>Division of CryoEM and Bioimaging, SSRL, SLAC National Accelerator Laboratory, Menlo Park, CA94025, USA</span> </span></div></dd></div> <div class="row" data-v-2edb8da6><dt class="col-sm-2 col-12 title" data-v-2edb8da6> * </dt> <dd class="col content" data-v-2edb8da6><div class="row" data-v-2edb8da6><div class="d-sm-flex d-inline flex-sm-1 flex-sm-wrap" data-v-2edb8da6><div class="d-inline" data-v-2edb8da6><span data-v-2edb8da6><div class="corresp"><span class="label">*</span><span class="bold">Author for correspondence:</span> Wah Chiu, E-mail: <a href="mailto:wahc@stanford.edu">wahc@stanford.edu</a></div></span></div></div></div></dd></div> <hr aria-hidden="true" class="separator default" data-v-7036083a data-v-2edb8da6></dl></div></div> <div id="app-tabs" class="tabs" data-v-1d90c6ce data-v-01274b1d><div id="app-tabs-wrapper" class="tabs__wrapper" data-v-1d90c6ce><div 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class="list__item__link"><span class="toc-title">Abstract</span></a></li> <li class="list__item"><a href="#sec1" class="list__item__link"> <span>Introduction</span></a></li><li class="list__item"><a href="#sec2" class="list__item__link"> <span>Results and discussion</span></a></li><li class="list__item"><a href="#sec3" class="list__item__link"> <span>Methods</span></a></li><li class="list__item"><a href="#sec8" class="list__item__link"> <span>Conflicts of Interests</span></a></li><li class="list__item"><a href="#sec9" class="list__item__link"> <span>Authorship Contributions</span></a></li><li class="list__item"><a href="#sec10" class="list__item__link"> <span>Data Deposition</span></a></li><li class="list__item"><a href="#sec20" class="list__item__link"> <span>Open Peer Review</span></a></li><li class="list__item"><a href="#sec11" class="list__item__link"> <span>Supplementary Materials</span></a></li>  <li class="list__item"><a href="#references-list" class="list__item__link"><span 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style="display:none;" data-v-fab090b8><div aria-labelledby="dropdown-share-button" data-v-fab090b8 data-v-beffd87c> <div class="social-share-container" data-v-fab090b8 data-v-beffd87c></div></div> <button aria-label="Close Share dropdown" aria-expanded="false" class="app-button close-icon app-button__icon app-button--" data-v-2a038744 data-v-fab090b8><img src="/core/page-component/img/close-icon.194b28a.svg" alt="" class="app-icon icon close" data-v-d2c09870 data-v-2a038744> </button></div></div> <button aria-expanded="false" data-test-id="buttonCiteOptions" data-prod-id="6566DF036E29EAE203048C708B48B9EB" data-toggle="modal" href="#cite-modal" class="app-button cite-button d-print-none app-button__text-icon app-button--secondary export-citation-product" data-v-2a038744 data-v-2ce5f61d data-v-43a4d572><img src="/core/page-component/img/cite-icon.44eaaa4.svg" alt="" class="app-icon icon cite" data-v-d2c09870 data-v-2a038744> <span class="text" data-v-2a038744>Cite</span></button>  <a target="_blank" href="https://s100.copyright.com/AppDispatchServlet?publisherName=CUP&publication=QRD&title=A%203.4-%C3%85%20cryo-electron%20microscopy%20structure%20of%20the%20human%20coronavirus%20spike%20trimer%20computationally%20derived%20from%20vitrified%20NL63%20virus%20particles&publicationDate=17%20November%202020&author=Kaiming%20Zhang%2C%20Shanshan%20Li%2C%20Grigore%20Pintilie%2C%20David%20Chmielewski%2C%20Michael%20F.%20Schmid%2C%20Graham%20Simmons%2C%20Jing%20Jin%2C%20Wah%20Chiu©right=%C2%A9%20The%20Author(s)%202020.%20Published%20by%20Cambridge%20University%20Press&contentID=10.1017%2Fqrd.2020.16&startPage=&endPage=&orderBeanReset=True&volumeNum=1&issueNum=&oa=CC-BY" data-test-id="buttonRightLink" class="app-link rights-link d-print-none app-link__text-icon app-link--accent" data-v-63dfaf6e data-v-92ee52a2 data-v-43a4d572><img src="/core/page-component/img/rights-icon.d4a677c.svg" alt="" class="app-icon icon rights" data-v-d2c09870 data-v-63dfaf6e><span class="text" data-v-63dfaf6e>Rights & Permissions </span> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a></div> <hr aria-hidden="true" class="separator default" data-v-7036083a></div> <div class="share-modal-overlay" style="display:none;" data-v-43a4d572></div> <div data-spy="scroll" data-target="#toc" class="scrollspy-content" data-v-43a4d572> <div id="sec0" class="col article-abstract sec" data-v-2fa8b348 data-v-43a4d572><div class="abstract-text-container" data-v-2fa8b348><div lang="en"><h2>Abstract</h2>  <div class="abstract-content"><div class="abstract" data-abstract-type="normal"><p>Human coronavirus NL63 (HCoV-NL63) is an enveloped pathogen of the family <span class="italic">Coronaviridae</span> that spreads worldwide and causes up to 10% of all annual respiratory diseases. HCoV-NL63 is typically associated with mild upper respiratory symptoms in children, elderly and immunocompromised individuals. It has also been shown to cause severe lower respiratory illness. NL63 shares ACE2 as a receptor for viral entry with SARS-CoV-1 and SARS-CoV-2. Here, we present the <span class="italic">in situ</span> structure of HCoV-NL63 spike (S) trimer at 3.4-Å resolution by single-particle cryo-EM imaging of vitrified virions without chemical fixative. It is structurally homologous to that obtained previously from the biochemically purified ectodomain of HCoV-NL63 S trimer, which displays a three-fold symmetric trimer in a single conformation. In addition to previously proposed and observed glycosylation sites, our map shows density at other sites, as well as different glycan structures. The domain arrangement within a protomer is strikingly different from that of the SARS-CoV-2 S and may explain their different requirements for activating binding to the receptor. This structure provides the basis for future studies of spike proteins with receptors, antibodies or drugs, in the native state of the coronavirus particles.</p></div></div> <hr aria-hidden="true" class="abstract-divider separator default" data-v-7036083a></div></div>   </div>  <div class="keywords" data-v-86c27100 data-v-43a4d572><h2 data-v-86c27100>Keywords</h2> <div class="row keywords__pills" data-v-86c27100><a href="/core/search?filters[keywords]=Cryo-EM" data-v-f0b31360 data-v-86c27100><span data-v-f0b31360 data-v-86c27100>Cryo-EM</span></a><a href="/core/search?filters[keywords]=human coronavirus NL63" data-v-f0b31360 data-v-86c27100><span data-v-f0b31360 data-v-86c27100>human coronavirus NL63</span></a><a href="/core/search?filters[keywords]=spike trimer" data-v-f0b31360 data-v-86c27100><span data-v-f0b31360 data-v-86c27100>spike trimer</span></a></div> <hr aria-hidden="true" class="separator default" data-v-7036083a data-v-86c27100></div>  <dl class="article-details" data-v-6e32a161 data-v-43a4d572><div class="row" data-v-6e32a161><dt class="col-12 col-sm-3 col-md-2_5 title" data-v-6e32a161> Type </dt> <dd class="col content" data-v-6e32a161>Research Article</dd></div> <div class="row" data-v-6e32a161><dt class="col-12 col-sm-3 col-md-2_5 title" data-v-6e32a161> Information </dt> <dd class="col content" data-v-6e32a161><div class="content__journal" data-v-6e32a161><a href="/core/journals/qrb-discovery" class="app-link app-link__text app-link--underlined" data-v-63dfaf6e data-v-6e32a161><span class="text" data-v-63dfaf6e>QRB Discovery </span> </a> <span data-v-6e32a161> , <a href="/core/journals/qrb-discovery/volume/F8B5CF3E0096CC946882DA4D8D779FE9" class="app-link app-link__text app-link--underlined" data-v-63dfaf6e data-v-6e32a161><span class="text" data-v-63dfaf6e>Volume 1 </span> </a></span>  <span data-v-6e32a161>, 2020</span>   <span data-v-6e32a161>, e11</span></div> <div class="doi-data" data-v-6e32a161><div data-v-6e32a161>DOI: <a target="_blank" href="https://doi.org/10.1017/qrd.2020.16" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-6e32a161><span class="text" data-v-63dfaf6e>https://doi.org/10.1017/qrd.2020.16 </span> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a></div> </div>  </dd></div> <div class="row creative-commons" data-v-6e32a161><dt class="col-12 col-sm-3 col-md-2_5 creative-commons__title"> Creative Commons </dt> <dd class="col"><div class="creative-commons__content"><div class="creative-commons__icons"><img src="/core/page-component/img/license-cc-icon.e3a74ed.svg" alt="Creative Common License - CC" class="app-icon creative-commons__icon license-cc" data-v-d2c09870><img src="/core/page-component/img/license-by-icon.33e212c.svg" alt="Creative Common License - BY" class="app-icon creative-commons__icon license-by" data-v-d2c09870></div> <div class="creative-commons__description">This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (<a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a>), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.</div></div></dd></div>  <div class="row" data-v-6e32a161><dt class="col-12 col-sm-3 col-md-2_5 title" data-v-6e32a161> Copyright </dt> <dd class="col content" data-v-6e32a161><div data-v-6e32a161> © The Author(s) 2020. Published by Cambridge University Press </div></dd></div></dl>  <div id="content-container" class="content-container" data-v-43a4d572><div class="content-box"><div class="article research-article NLM"> <div class="body"> <div class="sec intro" data-magellan-destination="sec1" id="sec1"> <h2 class="A"> Introduction</h2> <p class="p"> <em class="italic">Coronaviridae</em> constitute a large family of enveloped, positive-sense single-stranded RNA (+ssRNA) viruses capable of causing severe and widespread human respiratory disease. The coronaviruses are zoonotic pathogens, often circulating among natural reservoirs, such as bats or camels prior to crossing the species barrier into humans (Wang <em class="italic">et al.,</em> <a class="xref bibr" href="#ref30"><span class="show-for-sr">Reference Wang, Shi, Zhang, Field, Daszak and Eaton</span>2006</a>; Sabir <em class="italic">et al.,</em> <a class="xref bibr" href="#ref21"><span class="show-for-sr">Reference Sabir, Lam, Ahmed, Li, Shen, Abo- Aba and Guan</span>2015</a>). Coronaviruses are classified into four genera (alpha-CoV, beta-CoV, gamma-CoV and delta-CoV), with human coronaviruses found in two: alpha-CoVs (HCoV-229E and HCoV-NL63) and beta-CoVs [middle-east respiratory syndrome (MERS) and severe acute respiratory syndrome coronavirus 1 and 2 (SARS-CoV-1 and SARS-CoV-2)] (Cui <em class="italic">et al.,</em> <a class="xref bibr" href="#ref7"><span class="show-for-sr">Reference Cui, Li and Shi</span>2018</a>). SARS-CoV-2, responsible for the COVID-19 pandemic, has infected over 47 million people and claimed over 1.2 million lives worldwide as of early November 2020, underscoring the urgency of studying all circulating human coronaviruses (<a class="uri" href="https://covid19.who.int/">https://covid19.who.int/</a>) (Cui <em class="italic">et al.,</em> <a class="xref bibr" href="#ref7"><span class="show-for-sr">Reference Cui, Li and Shi</span>2018</a>; Zhou <em class="italic">et al.,</em> <a class="xref bibr" href="#ref41"><span class="show-for-sr">Reference Zhou, Yang, Wang, Hu, Zhang, Zhang and Shi</span>2020</a>). While beta-CoVs are more commonly associated with high pathogenicity and severe respiratory disease, alpha-CoVs are widely circulating viruses associated with cold-like symptoms, and in rare cases, more serious respiratory failure (Wang <em class="italic">et al.,</em> <a class="xref bibr" href="#ref31"><span class="show-for-sr">Reference Wang, Li, Liu, Gan, Zhang, Wang and Zhao</span>2020</a>). HCoV-NL63 is estimated to be the causative agent of up to 10% of annual respiratory disease and is a major cause of bronchiolitis and pneumonia in newborns (van der Hoek <em class="italic">et al.,</em> <a class="xref bibr" href="#ref10"><span class="show-for-sr">Reference Van der Hoek, Pyrc, Jebbink, Vermeulen- Oost, Berkhout, Wolthers and Berkhout</span>2004</a>; Chiu <em class="italic">et al.,</em> <a class="xref bibr" href="#ref6"><span class="show-for-sr">Reference Chiu, Hung Chan, Wing Chu, Kwan, Guan, Man Poon and Peiris</span>2005</a>).</p> <p class="p"> Coronaviruses utilize large spike (S) homotrimers (500-600 kDa) protruding from the viral membrane to engage cellular receptors and mediate fusion with host membranes (Thorp <em class="italic">et al.,</em> <a class="xref bibr" href="#ref24"><span class="show-for-sr">Reference Thorp, Boscarino, Logan, Goletz and Gallagher</span>2006</a>; Pallesen <em class="italic">et al.,</em> <a class="xref bibr" href="#ref16"><span class="show-for-sr">Reference Pallesen, Wang, Corbett, Wrapp, Kirchdoerfer, Turner and McLellan</span>2017</a>). These spikes, numerous on the virus surface, constitute the primary target of neutralizing antibodies (NAbs) and are central to vaccine design and structural studies for drug optimization. Each S protomer contains two large regions: N-terminal S1 responsible for receptor-binding and C-terminal S2 responsible for type-I fusion, as well as an additional single-pass transmembrane helix that anchors the spike to the viral envelope (Bosch <em class="italic">et al.,</em> <a class="xref bibr" href="#ref3"><span class="show-for-sr">Reference Bosch, van der Zee, de Haan and Rottier</span>2003</a>; Zheng <em class="italic">et al.,</em> <a class="xref bibr" href="#ref39"><span class="show-for-sr">Reference Zheng, Deng, Liu, van der Hoek, Berkhout and Lu</span>2006</a>). Spikes are activated by protease cleavage, near the putative fusion peptide, allowing the transition from pre- to post-fusion conformation during virus entry (Belouzard <em class="italic">et al.,</em> <a class="xref bibr" href="#ref2"><span class="show-for-sr">Reference Belouzard, Chu and Whittaker</span>2009</a>).</p> <p class="p"> Several single-particle cryo-electron microscopy (cryo-EM) structures of purified ectodomains of pre-fusion S trimers from alpha-CoV and beta-CoV genera have been determined, illustrating conformational heterogeneity of S1, multiple glycosylation sites, and the interactions with soluble receptors and NAbs (Walls <em class="italic">et al.,</em> <a class="xref bibr" href="#ref27"><span class="show-for-sr">Reference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler</span>2016</a>, <a class="xref bibr" href="#ref28"><span class="show-for-sr">Reference Walls, Park, Tortorici, Wall, McGuire and Veesler</span>2020</a>; Song <em class="italic">et al.,</em> <a class="xref bibr" href="#ref23"><span class="show-for-sr">Reference Song, Gui, Wang and Xiang</span>2018</a>; Wrapp <em class="italic">et al.,</em> <a class="xref bibr" href="#ref36"><span class="show-for-sr">Reference Wrapp, Wang, Corbett, Goldsmith, Hsieh, Abiona and McLellan</span>2020</a>). These S complexes lack the helical C-terminal stem that connects S2 to the viral envelope, and require residues mutated to proline at the loop between the first heptad repeat and the central helix to stabilize the construct (Pallesen <em class="italic">et al.,</em> <a class="xref bibr" href="#ref16"><span class="show-for-sr">Reference Pallesen, Wang, Corbett, Wrapp, Kirchdoerfer, Turner and McLellan</span>2017</a>; Kirchdoerfer <em class="italic">et al.,</em> <a class="xref bibr" href="#ref12"><span class="show-for-sr">Reference Kirchdoerfer, Wang, Pallesen, Wrapp, Turner, Cottrell and Ward</span>2018</a>; Park <em class="italic">et al.,</em> <a class="xref bibr" href="#ref17"><span class="show-for-sr">Reference Park, Walls, Wang, Sauer, Li, Tortorici and Veesler</span>2019</a>). High-resolution structure determinations of molecular components in pleomorphic virions are typically obtained by single-particle cryo-EM or X-ray crystallography of exogenously expressed and purified components. Conversely, cryo-electron tomography (cryo-ET) has been used to reconstruct tomograms of the whole virus particles, from which sub-volume density, corresponding to the feature of interest, would be further processed by classification and averaging (Schmid <em class="italic">et al.,</em> <a class="xref bibr" href="#ref22"><span class="show-for-sr">Reference Schmid, Hecksel, Rochat, Bhella, Chiu and Rixon</span>2012</a>; Wan and Briggs, <a class="xref bibr" href="#ref32"><span class="show-for-sr">Reference Wan and Briggs</span>2016</a>). Here, we take the approach of utilizing single-particle cryo-EM imaging of purified and vitrified HCoV-NL63 virus particles, and then using computational methods to extract the S trimer density for its high-resolution structure determination. Our approach is similar to a recent preprint report for chemically fixed SARS-CoV-2 particles (Ke <em class="italic">et al.,</em> <a class="xref bibr" href="#ref11"><span class="show-for-sr">Reference Ke, Oton, Qu, Cortese, Zila, McKeane and Briggs</span>2020</a>). We report the 3.4-Å structure of the S trimer in its native, pre-fusion state, and expect our data will be of value in future drug and vaccine design for various strains of coronaviruses without the need to genetically construct and biochemically purify spike proteins.</p> </div> <div class="sec" data-magellan-destination="sec2" id="sec2"> <h2 class="A"> Results and discussion</h2> <p class="p"> Since the S trimers protrude from the membrane surface of the virion, many of the crown-shaped S trimers can be easily identified, computationally extracted from the raw images, and treated as single-particle images with a distinct particle orientation without the need of tilting the specimens (<a class="xref fig" href="#fig1">Fig. 1</a> <em class="italic">a</em>). Based on the fact that single-particle cryo-EM is a more routine procedure for computing high-resolution structures compared to cryo-ET, we decided not to collect tilt series, and used single-particle cryo-EM analysis of the native S trimer on purified and vitrified virions. The two-dimensional (2D) class averages showed a clear triangular shape for the S trimer and other distinct views (<a class="xref fig" href="#fig1">Fig. 1</a> <em class="italic">b</em>). D<em class="italic">e novo</em> building of the initial map, using the ‘Ab-initio reconstruction’ option in cryoSPARC without any symmetry applied, resulted in a three-dimensional (3D) structure with well-defined features. Further 3D refinement was performed with and without C3 symmetry to obtain 3.4 and 3.7 Å maps, respectively (<a class="xref fig" href="#fig1">Fig. 1</a> <em class="italic">c–e</em> and Fig. S1). The reconstructed map without imposed symmetry also displayed three-fold symmetry, showing a high cross-correlation coefficient (CC = 0.98) with the symmetric map (Fig. S1<em class="italic">d</em>). Hereafter, we will present our structural analysis of the 3.4-Å map with C3 imposed symmetry after refinement from a subset of ~82,000 S trimer particles showing adequate orientation sampling (Fig. S1). The local resolution varies in our map (<a class="xref fig" href="#fig1">Fig. 1</a> <em class="italic">e</em>); the densities at the outer surface of the protein have a much lower resolution than the central region (<a class="xref fig" href="#fig1">Fig. 1</a> <em class="italic">e</em>), which could be attributed to the inherent flexibility of the distal ends of glycans. Compared to the map of the purified S ectodomain (EMD-8331), our map has a more extended density without recognizable secondary structure element features that points towards the viral membrane (<a class="xref fig" href="#fig1">Fig. 1</a> <em class="italic">e</em>). The detection of this feature likely results from the direct picking of S trimer anchored in the lipid envelope of native virions, which stabilizes the stem region that otherwise disassembles in the purified S ectodomains.</p><section><div class="fig" data-magellan-destination="fig1" id="fig1"> <div class="figure-thumb"><img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig1.png?pub-status=live" class="aop-lazy-load-image" width="1750" height="1617" data-original-image="/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig1.png" data-zoomable="true"></div> <div class="caption"><p class="p"> </p><p class="p"><span class="label">Fig. 1.</span> Single-particle cryo-EM analysis of <em class="italic">in-situ</em> structure of the HCoV-NL63 coronavirus spike glycoprotein. (<em class="italic">a</em>) Representative motion-corrected cryo-EM micrograph. (<em class="italic">b</em>) Reference-free 2D class averages of computationally extracted spikes. (<em class="italic">c-d</em>) Reconstructed 3-fold symmetry-imposed cryo-EM map of the spike in the top and side views without (c) and with (<em class="italic">d</em>) glycans shown. (<em class="italic">e</em>) Resolution variation maps for 3D reconstruction. Left, whole map view; middle, slice view; right, whole map view at a lower threshold.</p> </div></div></section> <p class="p"> Because of the high feature similarity of our map to that determined from the biochemically purified S ectodomain (Walls <em class="italic">et al.,</em> <a class="xref bibr" href="#ref27"><span class="show-for-sr">Reference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler</span>2016</a>), we fitted the published model (PDB ID: 5SZS) including the glycans to our 3.4-Å map and refined it. Residues 883–889 and 993–1000 that were previously unresolved were also modeled (see Methods section). The quality of the final model was validated by MolProbity (Chen <em class="italic">et al.,</em> <a class="xref bibr" href="#ref5"><span class="show-for-sr">Reference Chen, Arendall, Headd, Keedy, Immormino, Kapral and Richardson</span>2009</a>) (Table S1), the cross correlation between the map and model (<a class="xref fig" href="#fig2">Fig. 2</a> <em class="italic">a</em>), and Q-score analysis per residue (Pintilie <em class="italic">et al.,</em> <a class="xref bibr" href="#ref19"><span class="show-for-sr">Reference Pintilie, Zhang, Su, Li, Schmid and Chiu</span>2020</a>) (<a class="xref fig" href="#fig2">Fig. 2</a> <em class="italic">b–e</em>). The density map of our structure is better resolved in many regions, relative to the previous structure (PDB ID: 5SZS), including glycans (<a class="xref fig" href="#fig3">Fig. 3</a>), which were previously interpreted with accompanied mass spectrometry measurements (Walls <em class="italic">et al.,</em> <a class="xref bibr" href="#ref27"><span class="show-for-sr">Reference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler</span>2016</a>). Superimposition of our model and 5SZS yields 804 pruned atom pairs matched with 1.28-Å root mean square deviation (RMSD), indicating their high structural similarity. Structural comparisons based on individual domains also show similar results. These domains include domain 0, domain A, domain B (also known as RBD), domain C, and domain D, with the RMSD ranging from 0.29 Å to 0.90 Å. As shown in <a class="xref fig" href="#fig1">Fig. 1</a>, each of the three receptor-binding domains (RBDs) within the S trimer is pointed downwards. Notably, heterogeneous refinement and 3D variability did not reveal alternative RBD conformations, implying that the native S trimer proteins on the virion are predominantly in a fully closed state, consistent with the previous report of purified HCoV-NL63 S ectodomain (Walls <em class="italic">et al.,</em> <a class="xref bibr" href="#ref27"><span class="show-for-sr">Reference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler</span>2016</a>).</p><section><div class="fig" data-magellan-destination="fig2" id="fig2"> <div class="figure-thumb"><img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig2.png?pub-status=live" class="aop-lazy-load-image" width="1692" height="2450" data-original-image="/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig2.png" data-zoomable="true"></div> <div class="caption"><p class="p"> </p><p class="p"><span class="label">Fig. 2.</span> Model validation of the HCoV-NL63 coronavirus spike glycoprotein protomer. (<em class="italic">a</em>) Per-residue cross-correlation coefficient between the model and 3.4-Å map. (<em class="italic">b</em>) Q-score for each amino acid residue in the model and 3.4-Å map; the orange line represents the expected Q-score of 0.52 at 3.4-Å resolution based on the correlation between Q-scores and map resolutions (Pintilie <em class="italic">et al.,</em> <a class="xref bibr" href="#ref19"><span class="show-for-sr">Reference Pintilie, Zhang, Su, Li, Schmid and Chiu</span>2020</a>). (<em class="italic">c–e</em>) Examples of different regions of the map with different resolvability: (<em class="italic">c</em>) well-resolved, (<em class="italic">d</em>) poorly-resolved; (<em class="italic">e</em>) residues not resolved in the previous biochemically purified HCoV-NL63 spike protein structure (PDB ID: 5SZS) and thus their model built <em class="italic">de novo</em> here. The model is shown as ribbon, with residue Q-scores annotated in colors. The higher Q-score indicates better resolvability.</p> </div></div></section> <section><div class="fig" data-magellan-destination="fig3" id="fig3"> <div class="figure-thumb"><img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig3.png?pub-status=live" class="aop-lazy-load-image" width="1501" height="1904" data-original-image="/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig3.png" data-zoomable="true"></div> <div class="caption"><p class="p"> </p><p class="p"><span class="label">Fig. 3.</span> Resolvability of glycans. (<em class="italic">a</em>) Q-scores analysis for each glycan residue (# starting from 1401) in model and map; the orange line represents the expected Q-score of 0.52 at 3.4-Å resolution based on the correlation between Q-scores and map resolutions of amino acid residues (Pintilie <em class="italic">et al.,</em> <a class="xref bibr" href="#ref19"><span class="show-for-sr">Reference Pintilie, Zhang, Su, Li, Schmid and Chiu</span>2020</a>). (<em class="italic">b</em>) Highlights on several glycans. Green: Positive difference density between our and previous map (EMD-8331) suggesting extra glycan densities; Yellow: glycan densities found both in our map and in the previous study. The glycan models were derived from (PDB ID: 5SZS).</p> </div></div></section> <p class="p"> Glycosylation of S plays an important role in the viral life cycle and immune-evasion (Vigerust and Shepherd, <a class="xref bibr" href="#ref26"><span class="show-for-sr">Reference Vigerust and Shepherd</span>2007</a>; Watanabe <em class="italic">et al.,</em> <a class="xref bibr" href="#ref33"><span class="show-for-sr">Reference Watanabe, Bowden, Wilson and Crispin</span>2019</a>, <a class="xref bibr" href="#ref34"><span class="show-for-sr">Reference Watanabe, Berndsen, Raghwani, Seabright, Allen, Pybus and Crispin</span>2020</a>; Casalino <em class="italic">et al.,</em> <a class="xref bibr" href="#ref4"><span class="show-for-sr">Reference Casalino, Gaieb, Goldsmith, Hjorth, Dommer, Harbison and Amaro</span>2020</a>). We observed densities protruding from the amino acid residues corresponding to all the glycan sites that were previously observed in the cryo-EM map of the ectodomain of biochemically purified S (EMD-8331). All these glycosylation sites had been identified by a combination of cryo-EM densities protruding from the expected amino acid side chains and mass spectrometry (<a class="xref table" href="#tab1">Table 1</a> and Table S2) (Walls <em class="italic">et al.,</em> <a class="xref bibr" href="#ref27"><span class="show-for-sr">Reference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler</span>2016</a>). The models for these glycans were fitted into our map and their Q scores are shown in <a class="xref fig" href="#fig3">Fig. 3</a> <em class="italic">a</em>. Some examples are displayed as NAG residues in <a class="xref fig" href="#fig3">Fig. 3</a> <em class="italic">b</em>. To further investigate the possible presence of other glycan moieties, we calculated a difference map between our map and the EMD-8331 (see Methods). We observed positive difference density in five sites shown in green in <a class="xref fig" href="#fig3">Fig. 3</a> <em class="italic">b</em>. Two N-linked glycosylation sites (Asn24 and Asn203 in domain 0), predicted to exist from their sequence, as well as one O-linked glycosylation site (Ser496 in domain B), were newly identified in our difference density map (<a class="xref fig" href="#fig3">Fig. 3</a> <em class="italic">b</em> and <a class="xref table" href="#tab1">Table 1</a>). None of these was found by mass spectrometry or shown clearly in the previous map. These differences between our structure and the previously published one are possibly due to the differences in glycosylation patterns across species (Walls <em class="italic">et al.,</em> <a class="xref bibr" href="#ref27"><span class="show-for-sr">Reference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler</span>2016</a>). In our study, the virus was grown in mammalian cells, while the previous study used S ectodomain expressed in insect cells. N-linked glycosylation in mammalian cells typically results in complex-type glycans with two to four branches extended from the tri-mannosyl core. In contrast, glycosylation in insect cells typically yields truncated, paucimannosidic or oligomannosidic glycans with few if any complex-type glycans (Tomiya <em class="italic">et al.,</em> <a class="xref bibr" href="#ref25"><span class="show-for-sr">Reference Tomiya, Narang, Lee and Betenbaugh</span>2004</a>). Overall, there is significant agreement between <em class="italic">in situ</em> and biochemically purified S protein structure with these notable differences in glycan densities. Our structure cross-validates the conformation of the spike protein of HCoV-NL63 determined from either the biochemically purified specimen or the intact virions by cryo-EM.</p><div class="table-wrap" data-magellan-destination="tab1" id="tab1"> <div class="caption"> <p class="p"><span class="label">Table 1.</span> Newly identified glycosylation sites in this study.</p> </div> <span> <div class="figure-thumb"><img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_tab1.png?pub-status=live" class="aop-lazy-load-image" width="2142" height="276" data-original-image="/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_tab1.png" data-zoomable="true"></div> </span> <div class="table-wrap-foot"> <p class="p"> Abbreviation: MS, mass spectrometry; ND, not detected; cryo-EM, cryo-electron microscopy.</p> </div> </div> <p class="p"> Compared to the S1 protein of betacoronavirus (i.e. SARS-CoV-2), HCoV-NL63 S1 has an additional N-terminal domain (domain 0) that is assumed to be a gene duplication of domain A and is a canonical feature of alphacoronaviruses. Domain B (RBD) of beta-coronaviruses transitions between upward (open) and downward (closed) conformations due to its inherent flexibility; the viral receptor ACE2 is able to sample the RBD’s up conformation to initiate virus-receptor binding. In contrast, domain B of HCoV-NL63 interacts with domain A, therefore being stabilized in a closed ‘circle’ of HCoV-NL63 S1 (<a class="xref fig" href="#fig4">Fig. 4</a> <em class="italic">a</em>). The interface area between domains A and B of HCoV-NL63 is ~500 Å<sup class="sup">2</sup> and involves 22 hydrophobic interactions (<a class="xref fig" href="#fig4">Fig. 4</a> <em class="italic">b</em>) according to PDBsum structure bioinformatics analysis (Laskowski <em class="italic">et al.,</em> <a class="xref bibr" href="#ref13"><span class="show-for-sr">Reference Laskowski, Jabłońska, Pravda, Vařeková and Thornton</span>2017</a>). The three receptor binding motifs (RBMs) on HCoV-NL63 RBD are consequently buried in the interface between domain A and domain B, and prevented from binding to the viral receptor ACE2 (Wu <em class="italic">et al.,</em> <a class="xref bibr" href="#ref37"><span class="show-for-sr">Reference Wu, Li, Peng and Li</span>2009</a>). There must exist a mechanism to induce a conformational change to release the RBMs from domain A to allow receptor binding. It was reported that HCoV-NL63 utilizes heparan sulfate proteoglycans as the attachment factor before binding to ACE2 for virus entry (Milewska <em class="italic">et al.,</em> <a class="xref bibr" href="#ref14"><span class="show-for-sr">Reference Milewska, Zarebski, Nowak, Stozek, Potempa and Pyrc</span>2014</a>, <a class="xref bibr" href="#ref15"><span class="show-for-sr">Reference Milewska, Nowak, Owczarek, Szczepanski, Zarebski, Hoang and Pyrc</span>2017</a>). Whether heparan sulfate binding to HCoV-NL63 S1 or other factors induce conformational changes to release RBMs for ACE2 binding warrants further studies.</p><section><div class="fig" data-magellan-destination="fig4" id="fig4"> <div class="figure-thumb"><img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig4.png?pub-status=live" class="aop-lazy-load-image" width="1751" height="2062" data-original-image="/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig4.png" data-zoomable="true"></div> <div class="caption"><p class="p"> </p><p class="p"><span class="label">Fig. 4.</span> Structure comparison between HCoV-NL63 and SARS-CoV-2 spike. (<em class="italic">a</em>) Comparison of our structure with SARS-CoV-2 spike in closed state (PDB ID: 6VXX) in two different views. Different domains and the linker (Lk) between domains A and B are indicated in different colors. (<em class="italic">b</em>) Zoom-in view to show the interactions between domain A and domain B in the HCoV-NL63 spike protein. (<em class="italic">c</em>) Extracted densities of the S2 fusion machinery region with models fitted.</p> </div></div></section> <p class="p"> S proteins of coronaviruses require protease cleavage to release the fusion peptide that inserts into the target membrane to initiate membrane fusion for virus entry. We compared HCoV-NL63 and SARS-CoV-2 S2 fusion machineries by superimposing their structures together and an excellent agreement was observed (<a class="xref fig" href="#fig4">Fig. 4</a> <em class="italic">c</em>). In both structures, the <sub> </sub> loop where the host protease cleavage site is located in the S2 region is almost perpendicular to the central helix, protruding at the periphery of the S trimer and readily accessible to host proteases. The fusion machineries of HCoV-NL63 and SARS-CoV-2 are almost identical except that the <sub> </sub> trigger loop of HCoV-NL63 forms a short alpha helix before looping back to connect to the fusion peptide while the corresponding loop of SARS-CoV-2 is long and flexible. The fusion machinery of coronaviruses provides a potential target for broad anti-coronavirus therapeutics development.</p> <p class="p"> Further similarities between HCoV-NL63 and SARS-CoV-2 domains are illustrated in <a class="xref fig" href="#fig5">Fig. 5</a> and Fig. S2. Structure-based alignments using TM-align (Zhang and Skolnick, <a class="xref bibr" href="#ref38"><span class="show-for-sr">Reference Zhang and Skolnick</span>2005</a>) show that structurally, domains A and 0 from HCoV-NL63, and domain A′ from SARS-CoV-2 are very similar, with RMSDs of ~3.5 Å between ~75% aligned residues. These aligned residues however have quite low sequence identities (7.5–10.2%). Regardless, due to such high structure similarity, it is very likely that they evolved from a common ancestor, consistent with the previous hypothesis that domains 0 and A resulted from a gene duplication event of a single domain. Domains B and B′ also have a similar core fold, with RMSD of 4.13 Å, though the receptor-binding motifs look significantly different between the two, even though both bind the receptor ACE2. Domains D and D′ are also structurally similar, though still having a low sequence identity of 6.3%. Domains C/C′ and S2/S2′ are the most similar, with relatively high sequence identities of 25.4% and 37.0%; this high conservation shows that these domains, in particular, may be less prone to mutate and may be targeted by cross-reactive antibodies as reported very recently (Wang <em class="italic">et al.,</em> <a class="xref bibr" href="#ref29"><span class="show-for-sr">Reference Wang, van Haperen, Gutiérrez-Álvarez, Li, Okba, Albulescu and Bosch</span>2020</a>).</p><section><div class="fig" data-magellan-destination="fig5" id="fig5"> <div class="figure-thumb"><img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig5.png?pub-status=live" class="aop-lazy-load-image" width="1254" height="954" data-original-image="/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig5.png" data-zoomable="true"></div> <div class="caption"><p class="p"> </p><p class="p"><span class="label">Fig. 5.</span> Structural comparison of domains in HCoV-NL63 and SARS-CoV-2 spikes. (<em class="italic">a</em>) Ribbon diagram of the spikes. Each domain is shown in different colors. (<em class="italic">b</em>) Structure-based alignment of corresponding domains (PDB ID: 6VXX for A′, C′, D′ and S2′), analysed by TM-align (Zhang and Skolnick, <a class="xref bibr" href="#ref38"><span class="show-for-sr">Reference Zhang and Skolnick</span>2005</a>). For domain B–B′ comparison, PDB ID: 6VW1 was used for domain B′ because it has receptor-binding motif (outlined in dotted ellipse).</p> </div></div></section> <p class="p"> The feasibility of solving the near-atomic resolution structure of membrane-anchored S trimer on the purified viral particle opens a straightforward path for follow-up structural studies of coronaviruses with external reagents like receptors, antibodies or drugs. In addition, the single-particle cryo-EM derived structures can be used together with sub-tomogram averages of the S trimer in the virion to understand complex and heterogeneous modes of interactions between S and various external reagents in different biochemical conditions, and the orientation in 3D of S with respect to the viral membrane, and, ultimately, the cell surface. Such a hybrid approach across different imaging protocols will be very useful for the discovery of authentic structural states of molecular components in a pleomorphic virus particle in the context of pathogenicity relevant to human health.</p> </div> <div class="sec methods" data-magellan-destination="sec3" id="sec3"> <h2 class="A"> Methods</h2> <div class="sec" data-magellan-destination="sec4" id="sec4"> <h3 class="B"> Cell culture and virus</h3> <p class="p"> Vero E6 (ATCC CRL-1586) and MA104 (ATCC CRL-2378.1) cells were maintained at 37°C in a fully humidified atmosphere with 5% CO<sub>2</sub> in Dulbecco's Modified Eagle's medium (Invitrogen) and M199 (Gibco) medium respectively. All culture media were supplemented with penicillin and streptomycin and 10% foetal bovine serum (Hyclone). HCoV-NL63 was obtained from BEI Resources, NIAID, NIH: Human Coronavirus, NL63, NR-470.</p> </div> <div class="sec" data-magellan-destination="sec5" id="sec5"> <h3 class="B"> Virus production and purification</h3> <p class="p"> Monolayers of Vero E6 or MA-104 cells were infected with HCoV-NL63 at MOI 0.5. Culture supernatants were harvested when clear cytopathic effect developed. After clarification of the supernatants through a 0.45 μm filter, the virus was pelleted down through a 20% sucrose cushion. Virus was then resuspended in virus resuspension buffer (20 mM Tris, pH 8.0, 120 mM NaCl, 1 mM EDTA) before layered onto 2 ml of 60% OptiPrep (Sigma-Aldrich) and spun at 50,000<em class="italic">g</em> for 1.5 h using a SW28 rotor. After ultracentrifugation, the supernatants were removed to leave 4 ml above the virus band. The remaining 4 ml supernatant, the virus band and the underlay of 2 ml of 60% OptiPrep were mixed to reach a final concentration of 20% OptiPrep. The mixture was spun at 360,000<em class="italic">g</em> for 3.5 h with a NVT65.2 rotor. The virus band was extracted and buffer exchanged to the virus resuspension buffer using an Amicon Ultra-2 Centrifugal Filter Unit with Ultracel-100 membrane (Millipore).</p> </div> <div class="sec" data-magellan-destination="sec6" id="sec6"> <h3 class="B"> Cryo-EM vitrification, data acquisition, image processing and 3D reconstruction</h3> <p class="p"> Three microliters of purified HCoV-NL63 virions (4.5 mg ml<sup class="sup">−1</sup>) were first applied to 300-mesh R2/1 + 2 nm C-film grids (Quantifoil) that had been glow-discharged for 15 s PELCO easiGlow (TED PELLA, INC.). Grids were then front-blotted for 2 s in a 90% humidified chamber and vitrified using the LEICA EM GP automated plunge freezing device. Frozen grids were then stored in liquid nitrogen until imaging. The samples were imaged in a Titan Krios cryo-electron microscope (Thermo Fisher Scientific) operated at 300 kV with GIF energy filter (BioQuantum, Ametek) at a magnification of 64,000× (corresponding to a calibrated sampling of 1.4 Å per pixel). Micrographs were recorded by EPU software (Thermo Fisher Scientific) with a Ametek K3 Summit direct electron detector, where each image was composed of 30 individual frames with an exposure time of 3 s and an exposure rate of 16 electrons per second per Å<sup class="sup">2</sup>. A total of 4,138 movie stacks were collected. All movie stacks were motion-corrected by MotionCor2 (Zheng <em class="italic">et al.,</em> <a class="xref bibr" href="#ref40"><span class="show-for-sr">Reference Zheng, Palovcak, Armache, Verba, Cheng and Agard</span>2017</a>). Motion-corrected micrographs were imported into cryoSPARC for image processing. The contrast transfer function (CTF) was determined using the ‘Patch CTF Estimation’ option, and the micrographs with ‘CTF fit <5 Å’ were selected using the ‘Manually Curate Exposures’. Then 157 particles were manually picked and subjected to 2D classification into 10 classes, 3 of which were selected as the template for the auto-particle picking, yielding 944,822 particles. Several rounds of 2D classification were then performed to remove the poor 2D class averages, and 300,236 particles were obtained. The initial map was built using ab-initio reconstruction without any symmetry applied. Next, three rounds of heterogeneous refinement were performed to further remove bad particles. The final 3D non-uniform refinement was performed using the selected 82,030 particles with or without C3 symmetry applied, and a 3.4-Å map and a 3.7-Å map were obtained, respectively. Resolution for the final maps was estimated with the 0.143 criterion of the Fourier shell correlation curve. Resolution map was calculated in cryoSPARC using the ‘Local Resolution Estimation’ option. The figures were prepared using UCSF Chimera (Pettersen <em class="italic">et al.,</em> <a class="xref bibr" href="#ref18"><span class="show-for-sr">Reference Pettersen, Goddard, Huang, Couch, Greenblatt, Meng and Ferrin</span>2004</a>) or UCSF Chimera X (Goddard <em class="italic">et al.,</em> <a class="xref bibr" href="#ref9"><span class="show-for-sr">Reference Goddard, Huang, Meng, Pettersen, Couch, Morris and Ferrin</span>2017</a>).</p> </div> <div class="sec" data-magellan-destination="sec7" id="sec7"> <h3 class="B"> Model building</h3> <p class="p"> One protomer was first computationally extracted (Pintilie <em class="italic">et al.,</em> <a class="xref bibr" href="#ref20"><span class="show-for-sr">Reference Pintilie, Zhang, Goddard, Chiu and Gossard</span>2010</a>) from the 3.4-Å cryo-EM map of the spike protein expressed on HCoV-NL63 coronavirus. The PDB coordinates of biochemically purified HCoV-NL63 spike protein (PDB ID: 5SZS) were then fitted into the computationally extracted S protomer map. Residues 883–889 and 993–1,000 that were previously unresolved were also modeled using SWISS-MODEL (Waterhouse <em class="italic">et al.,</em> <a class="xref bibr" href="#ref35"><span class="show-for-sr">Reference Waterhouse, Bertoni, Bienert, Studer, Tauriello, Gumienny and Schwede</span>2018</a>). The resultant model was refined using phenix.real_space_refine (Adams <em class="italic">et al.,</em> <a class="xref bibr" href="#ref1"><span class="show-for-sr">Reference Adams, Afonine, Bunkóczi, Chen, Davis, Echols and Zwart</span>2010</a>) and manually optimized with Coot (Emsley <em class="italic">et al.,</em> <a class="xref bibr" href="#ref8"><span class="show-for-sr">Reference Emsley, Lohkamp, Scott and Cowtan</span>2010</a>). The atomic model of protomer was then fitted into the cryo-EM density of the other two protomers in the HCoV-NL63 spike trimer using Chimera (Pettersen <em class="italic">et al.,</em> <a class="xref bibr" href="#ref18"><span class="show-for-sr">Reference Pettersen, Goddard, Huang, Couch, Greenblatt, Meng and Ferrin</span>2004</a>), followed by the optimization of the whole model with phenix.real_space_refine. The glycans in the PDB ID: 5SZS model were also used in our model for refinement. The final model was evaluated by MolProbity (Chen <em class="italic">et al.,</em> <a class="xref bibr" href="#ref5"><span class="show-for-sr">Reference Chen, Arendall, Headd, Keedy, Immormino, Kapral and Richardson</span>2009</a>) and Q-scores (Pintilie <em class="italic">et al.,</em> <a class="xref bibr" href="#ref19"><span class="show-for-sr">Reference Pintilie, Zhang, Su, Li, Schmid and Chiu</span>2020</a>). The match between the map and the model was evaluated by the correlation for each residue (<a class="xref fig" href="#fig2">Fig. 2</a> <em class="italic">a</em>). For assessing the resolvability of the map density, the Q score was calculated for each residue with the final model (<a class="xref fig" href="#fig2">Fig. 2</a> <em class="italic">b</em>). The Q-scores were also computed for glycan residues (<a class="xref fig" href="#fig3">Fig. 3</a> <em class="italic">a</em>). Statistics of map reconstruction and model optimization are shown in Table S1. To identify extra glycosylation sites beyond what was previously known from the S ectodomain map (EMD-8331), we computed the difference map between our map and the previous map of the S ectodomain. When we fitted our map to this previous map using Chimera Fit in Map, it was apparent that the maps have different scales. Thus, the step size in our map was adjusted until the maximum cross-correlation between the two maps was obtained, at which point the maps also visually overlapped better. Density values in the two maps were then normalized to an average of 0 and standard deviation of 1. The difference map was then computed at each voxel with the rescaled maps. Extra glycan densities seen in this difference map were extracted using Segger (Pintilie <em class="italic">et</em> <em class="italic">al</em>., <a class="xref bibr" href="#ref20"><span class="show-for-sr">Reference Pintilie, Zhang, Goddard, Chiu and Gossard</span>2010</a>) for further visualization. All figures were prepared using Chimera (Pettersen <em class="italic">et al.,</em> <a class="xref bibr" href="#ref18"><span class="show-for-sr">Reference Pettersen, Goddard, Huang, Couch, Greenblatt, Meng and Ferrin</span>2004</a>) or Chimera X (Goddard <em class="italic">et al.,</em> <a class="xref bibr" href="#ref9"><span class="show-for-sr">Reference Goddard, Huang, Meng, Pettersen, Couch, Morris and Ferrin</span>2017</a>).</p> </div> </div> </div> <div class="back"> <div class="ack"> <h2 class="A"> Acknowledgements</h2> <p class="p"> We thank Drs. Corey Hecksel and Patrick Mitchell for expert maintenance of Stanford-SLAC Cryo-EM Centre and the SLAC National Accelerator Laboratory for supporting conduct of these studies during a university-wide pandemic shutdown. We also thank Dr. Andriy Kryshtafovych for help with structure-based alignment analysis. This work was supported by the National Institutes of Health grants (P41GM103832, R01AI148382, P01AI120943, R01GM079429, U24GM129564 to W.C.); DOE Office of Science through the National Virtual Biotechnology Laboratory, a consortium of DOE national laboratories focused on response to COVID-19, with funding provided by the Coronavirus CARES Act.</p> </div> <div class="sec" data-magellan-destination="sec8" id="sec8"> <h2 class="A"> Conflicts of Interests</h2> <p class="p"> All authors declare no competing interest.</p> </div> <div class="sec" data-magellan-destination="sec9" id="sec9"> <h2 class="A"> Authorship Contributions</h2> <p class="p"> W.C. and G.S. supervised the study. J.J. prepared the sample. D.C. performed cryo-EM sample preparation. K.Z. and D.C. collected cryo-EM data. K.Z. performed cryo-EM image processing and structure determination; S.L. and K.Z. built and refined the model; K.Z., S.L., G.P., D.C., M.F.S, J.J., and W.C. analysed data. K.Z., S.L., and G.P prepared the figures. K.Z., S.L., D.C., J.J, and W.C. wrote the manuscript with input from all other authors.</p> </div> <div class="sec" data-magellan-destination="sec10" id="sec10"> <h2 class="A"> Data Deposition</h2> <p class="p"> Cryo-EM maps of the HCoV-NL63 Spike protein with its associated atomic model have been deposited in the wwPDB OneDep System under EMD accession code EMD-22889 and PDB ID code 7KIP.</p> </div> <div class="sec" data-magellan-destination="sec20" id="sec20"> <h2 class="A"> Open Peer Review</h2> <p class="p"> To view the open peer review materials for this article, please visit <a class="uri" href="https://doi.org/10.1017/qrd.2020.16">http://doi.org/10.1017/qrd.2020.16</a>.</p> </div> <div class="sec" data-magellan-destination="sec11" id="sec11"> <h2 class="A"> Supplementary Materials</h2> <p class="p"> To view supplementary material for this article, please visit <a class="uri" href="https://dx.doi.org/10.1017/qrd.2020.16">http://dx.doi.org/10.1017/qrd.2020.16</a>.</p> </div> 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data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary-alt:20201206180614-42244-mediumThumb-S2633289220000162_fig1.jpg" data-enlarged-image="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary-alt:20201206180614-52417-optimisedImage-S2633289220000162_fig1.jpg" class="graphic" data-v-241a4b23></div> <div data-v-241a4b23><div class="caption" data-v-241a4b23><p data-v-241a4b23><span class="label" data-v-241a4b23>Fig. 1.</span> <span data-v-241a4b23><span class="p">Single-particle cryo-EM analysis of <span class="italic">in-situ</span> structure of the HCoV-NL63 coronavirus spike glycoprotein. (<span class="italic">a</span>) Representative motion-corrected cryo-EM micrograph. (<span class="italic">b</span>) Reference-free 2D class averages of computationally extracted spikes. (<span class="italic">c-d</span>) Reconstructed 3-fold symmetry-imposed cryo-EM map of the spike in the top and side views without (c) and with (<span class="italic">d</span>) glycans shown. (<span class="italic">e</span>) Resolution variation maps for 3D reconstruction. Left, whole map view; middle, slice view; right, whole map view at a lower threshold.</span></span></p></div> </div></div> <hr aria-hidden="true" class="separator dashed" data-v-7036083a data-v-241a4b23></div><div data-v-241a4b23><div class="figures__item" data-v-241a4b23><div class="figures__item__image-box" data-v-241a4b23><button class="figures__ref" data-v-241a4b23> View in content </button> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" alt="Figure 1" data-zoomable="true" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig2.png" data-enlarged-image="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig2.png" class="graphic" data-v-241a4b23></div> <div data-v-241a4b23><div class="caption" data-v-241a4b23><p data-v-241a4b23><span class="label" data-v-241a4b23>Fig. 2.</span> <span data-v-241a4b23><span class="p">Model validation of the HCoV-NL63 coronavirus spike glycoprotein protomer. (<span class="italic">a</span>) Per-residue cross-correlation coefficient between the model and 3.4-Å map. (<span class="italic">b</span>) Q-score for each amino acid residue in the model and 3.4-Å map; the orange line represents the expected Q-score of 0.52 at 3.4-Å resolution based on the correlation between Q-scores and map resolutions (Pintilie <span class="italic">et al.,</span>2020). (<span class="italic">c–e</span>) Examples of different regions of the map with different resolvability: (<span class="italic">c</span>) well-resolved, (<span class="italic">d</span>) poorly-resolved; (<span class="italic">e</span>) residues not resolved in the previous biochemically purified HCoV-NL63 spike protein structure (PDB ID: 5SZS) and thus their model built <span class="italic">de novo</span> here. The model is shown as ribbon, with residue Q-scores annotated in colors. The higher Q-score indicates better resolvability.</span></span></p></div> </div></div> <hr aria-hidden="true" class="separator dashed" data-v-7036083a data-v-241a4b23></div><div data-v-241a4b23><div class="figures__item" data-v-241a4b23><div class="figures__item__image-box" data-v-241a4b23><button class="figures__ref" data-v-241a4b23> View in content </button> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" alt="Figure 2" data-zoomable="true" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary-alt:20201206180614-68956-mediumThumb-S2633289220000162_fig3.jpg" data-enlarged-image="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary-alt:20201206180614-85383-optimisedImage-S2633289220000162_fig3.jpg" class="graphic" data-v-241a4b23></div> <div data-v-241a4b23><div class="caption" data-v-241a4b23><p data-v-241a4b23><span class="label" data-v-241a4b23>Fig. 3.</span> <span data-v-241a4b23><span class="p">Resolvability of glycans. (<span class="italic">a</span>) Q-scores analysis for each glycan residue (# starting from 1401) in model and map; the orange line represents the expected Q-score of 0.52 at 3.4-Å resolution based on the correlation between Q-scores and map resolutions of amino acid residues (Pintilie <span class="italic">et al.,</span>2020). (<span class="italic">b</span>) Highlights on several glycans. Green: Positive difference density between our and previous map (EMD-8331) suggesting extra glycan densities; Yellow: glycan densities found both in our map and in the previous study. The glycan models were derived from (PDB ID: 5SZS).</span></span></p></div> </div></div> <hr aria-hidden="true" class="separator dashed" data-v-7036083a data-v-241a4b23></div><div data-v-241a4b23><div class="figures__item" data-v-241a4b23><div class="figures__item__image-box" data-v-241a4b23><button class="figures__ref" data-v-241a4b23> View in content </button> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" alt="Figure 3" data-zoomable="true" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_tab1.png" data-enlarged-image="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_tab1.png" class="graphic" data-v-241a4b23></div> <div data-v-241a4b23><div class="caption" data-v-241a4b23><p data-v-241a4b23><span class="label" data-v-241a4b23>Table 1.</span> <span data-v-241a4b23><span class="p">Newly identified glycosylation sites in this study.</span></span></p></div> </div></div> <hr aria-hidden="true" class="separator dashed" data-v-7036083a data-v-241a4b23></div><div data-v-241a4b23><div class="figures__item" data-v-241a4b23><div class="figures__item__image-box" data-v-241a4b23><button class="figures__ref" data-v-241a4b23> View in content </button> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" alt="Figure 4" data-zoomable="true" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary-alt:20201206180614-98554-mediumThumb-S2633289220000162_fig4.jpg" data-enlarged-image="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary-alt:20201206180614-64037-optimisedImage-S2633289220000162_fig4.jpg" class="graphic" data-v-241a4b23></div> <div data-v-241a4b23><div class="caption" data-v-241a4b23><p data-v-241a4b23><span class="label" data-v-241a4b23>Fig. 4.</span> <span data-v-241a4b23><span class="p">Structure comparison between HCoV-NL63 and SARS-CoV-2 spike. (<span class="italic">a</span>) Comparison of our structure with SARS-CoV-2 spike in closed state (PDB ID: 6VXX) in two different views. Different domains and the linker (Lk) between domains A and B are indicated in different colors. (<span class="italic">b</span>) Zoom-in view to show the interactions between domain A and domain B in the HCoV-NL63 spike protein. (<span class="italic">c</span>) Extracted densities of the S2 fusion machinery region with models fitted.</span></span></p></div> </div></div> <hr aria-hidden="true" class="separator dashed" data-v-7036083a data-v-241a4b23></div><div data-v-241a4b23><div class="figures__item" data-v-241a4b23><div class="figures__item__image-box" data-v-241a4b23><button class="figures__ref" data-v-241a4b23> View in content </button> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==" alt="Figure 5" data-zoomable="true" data-src="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig5.png" data-enlarged-image="https://static.cambridge.org/binary/version/id/urn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig5.png" class="graphic" data-v-241a4b23></div> <div data-v-241a4b23><div class="caption" data-v-241a4b23><p data-v-241a4b23><span class="label" data-v-241a4b23>Fig. 5.</span> <span data-v-241a4b23><span class="p">Structural comparison of domains in HCoV-NL63 and SARS-CoV-2 spikes. (<span class="italic">a</span>) Ribbon diagram of the spikes. Each domain is shown in different colors. (<span class="italic">b</span>) Structure-based alignment of corresponding domains (PDB ID: 6VXX for A′, C′, D′ and S2′), analysed by TM-align (Zhang and Skolnick, 2005). For domain B–B′ comparison, PDB ID: 6VW1 was used for domain B′ because it has receptor-binding motif (outlined in dotted ellipse).</span></span></p></div> </div></div> </div></div> <div id="supplementary-materials-tab" class="supplementary-materials tab-pane"><div class="materials-table"><div class="materials-table__item"><div class="materials-table__row"><img src="/core/page-component/img/pdf-icon.6d46a59.svg" alt="Supplementary material: PDF" class="app-icon materials-table__row__left-elem pdf" data-v-d2c09870> <div class="materials-table__row__main-elem"><h3 class="materials-table__row__title">Zhang et al. supplementary material</h3> <div class="materials-table__row__description"><p>Zhang et al. supplementary material</p></div></div> <a href="https://static.cambridge.org/content/id/urn:cambridge.org:id:article:S2633289220000162/resource/name/S2633289220000162sup001.pdf" download="" class="app-link clickable-button materials-table__row__right-elem materials-table__row__download-button app-link__icon app-link--" data-v-63dfaf6e><img src="data:image/svg+xml;base64,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" alt="Download Zhang et al. supplementary material(PDF)" class="app-icon icon download" data-v-d2c09870 data-v-63dfaf6e> </a></div> <div class="materials-table__row"><div class="left-offset"></div>  <div class="right-offset"></div></div>  <div class="materials-table__row border-bottom"><div class="left-offset"></div> <div class="materials-table__row__size-type"> PDF 1.5 MB </div></div></div></div></div>       <div id="peer-review-tab" class="peer-review tab-pane" data-v-4d0e8700>  <div id="full-review-1" class="review" data-v-4d0e8700><div class="review__headings" data-v-4d0e8700><h2 data-v-4d0e8700><div class="article-title">Review: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R0/PR1</div></h2> <button aria-expanded="false" data-test-id="buttonCiteOptions" data-prod-id="DAA24F6BB10FBD32F37B29967E845BC2" data-toggle="modal" href="#cite-modal" class="app-button cite-button d-print-none app-button__text-icon app-button--secondary export-citation-product" data-v-2a038744 data-v-2ce5f61d data-v-4d0e8700><img src="/core/page-component/img/cite-icon.44eaaa4.svg" alt="" class="app-icon icon cite" data-v-d2c09870 data-v-2a038744> <span class="text" data-v-2a038744>Cite</span></button></div> <div class="review__metadata" data-v-4d0e8700><div data-v-4d0e8700> Published online by Cambridge University Press: <strong data-v-4d0e8700><span class="app-date" data-v-d415a782 data-v-4d0e8700> 17 November 2020 </span></strong></div> DOI: <a target="_blank" href="https://doi.org/10.1017/qrd.2020.16.pr1" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>https://doi.org/10.1017/qrd.2020.16.pr1 </span> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <div class="review__reviewer" data-v-4d0e8700><div data-v-4d0e8700><div class="review__author" data-v-4d0e8700><a href="/core/search?filters%5BauthorTerms%5D=Elena%20Orlova&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>Elena Orlova </span> </a> <a target="_blank" href="https://orcid.org/0000-0003-3371-415X" aria-label="Open the ORCID record for Elena Orlova in new tab/window" class="app-link review__author__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-4d0e8700><img src="data:image/svg+xml;base64,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" alt="" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span class="review__author__affiliation" data-v-4d0e8700><span data-v-4d0e8700> Biological sciences, Birkbeck University of London, United Kingdom </span></span></div></div></div> <div data-v-4d0e8700> Date of review: <strong data-v-4d0e8700><span class="app-date" data-v-d415a782 data-v-4d0e8700> 28 September 2020 </span></strong></div> <div data-v-4d0e8700>Revision round: 0</div> <div data-v-4d0e8700>Role: reviewer</div> <div data-v-4d0e8700>Recommendation/decision: minor-revision</div></div> <div class="review__statement" data-v-4d0e8700><h3 data-v-4d0e8700>Conflict of interest statement</h3> <div data-v-4d0e8700>Reviewer declares none.</div></div> <div class="review__comments" data-v-4d0e8700><h3 data-v-4d0e8700>Comments</h3> <div data-v-4d0e8700><p><span class="italic">Comments to Author</span>: The manuscript "A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles" by Zhang and co-authors reports a structure of the human coronavirus NL63 (HCoV-NL63) spike. This impactful study provides analysis of domain localisations within the HCoV-NL63 S (spike) trimer without chemical fixative in its prefusion conformation. Cryo-EM has been used in this structural study. The results of the research reported in the MS have several major outcomes. Firstly, the authors have proved the faithfulness of structural organisation of the NL63 spike obtained.Two structures (one from vitrified complete virus and another obtained using an expression system forHCoV-NL63 S ectodomain) demonstrate high level of consistency. Secondly, such consistency allowed analysing differences between the NL63 spike and the SARS-CoV-2 S structures, revealing and evaluation sites related to the receptor bindings. Thirdly, the structure of the NL63 spike from the vitrified viruses provides more complete information on glycosylation sites. This study will help to explain discrepancy in the pathogenicity between alpha and beta families of coronaviruses.</p><p>The methodologies used for the imaging and reconstruction processing followed by building the atomic modelare on the level of the state-of-the-art. The MS is well written and concise.Overall this is an important study at the current pandemic and linked to pathogenicity of the virus. It is related to the findingmedical means for suppressing infections.</p><p>It would be good if the comments listed below will be addressed:</p><p>Comparison of structures NL63 (HCoV-NL63) and SARS-CoV-2spikes indicated large rearrangements between domainsA and B. What is known about similarity (homology) of these domains and linkers between them?While a simplified schematic representation was given inWalls et all (NSMB,2016, Fig4) it does not provide sufficient information for explanation of biological relevance of this conformational differences.It would be useful to see the sequence alignment at least for domains ABCD (as a supplementary figure). Possibly, it will help to explain such big shift of the B domain in the SARS-CoV-2 S and the open conformation of the RBDs. It seems that the linker between A and B is shorter in NL63 so a different mechanism should be used for triggering the receptor binding.</p><p>It is rather difficult to find both the upstream helix and locations of the triggers loops within the entire spike structures.Therefore, it would be useful to highlight locations of the S2' trigger-loop region on side views of spikes (Figure 4a). Here may be hidden a very interesting mechanism of the spike activation.</p><p>The Fourier-Shell correlation graph should be deposited to the EMDB. Page 18 of the report: the table "Experimental information" 4 is practically empty, although these information is present in methods.</p><p>The authors have done good fitting and geometry of the model is rather good, but they did not read the report of evaluation of the fit quality:</p><p>"A red diamond above a residue indicates a poor fit to the EM map for this residue (all atom inclusion < 40%)." That effect takes place if the authors have used a too high threshold for the presentation and fitting of the model into the map. So it would make sense to try a lower threshold and the number of red diamonds will be possibly reduced and hopefully will be more consistent with other graphs in the evaluation report.</p><p>It would be good to explain why locations of ligands were poorly defined, since too many of them have high percentage of misplacements (both in bonds length and angles). While this fact does not diminish the value of the MS some verbal explanation will be helpful.</p></div></div> <hr aria-hidden="true" class="review__separator separator default" data-v-7036083a data-v-4d0e8700></div><div id="full-review-2" class="review" data-v-4d0e8700><div class="review__headings" data-v-4d0e8700><h2 data-v-4d0e8700><div class="article-title">Review: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R0/PR2</div></h2> <button aria-expanded="false" data-test-id="buttonCiteOptions" data-prod-id="2274E00CD9D4DCAE8FC69C89A1CF4932" data-toggle="modal" href="#cite-modal" class="app-button cite-button d-print-none app-button__text-icon app-button--secondary export-citation-product" data-v-2a038744 data-v-2ce5f61d data-v-4d0e8700><img src="/core/page-component/img/cite-icon.44eaaa4.svg" alt="" class="app-icon icon cite" data-v-d2c09870 data-v-2a038744> <span class="text" data-v-2a038744>Cite</span></button></div> <div class="review__metadata" data-v-4d0e8700><div data-v-4d0e8700> Published online by Cambridge University Press: <strong data-v-4d0e8700><span class="app-date" data-v-d415a782 data-v-4d0e8700> 17 November 2020 </span></strong></div> DOI: <a target="_blank" href="https://doi.org/10.1017/qrd.2020.16.pr2" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>https://doi.org/10.1017/qrd.2020.16.pr2 </span> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <div class="review__reviewer" data-v-4d0e8700><div data-v-4d0e8700><div class="review__author" data-v-4d0e8700><a href="/core/search?filters%5BauthorTerms%5D=Sheemei%20Lok&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>Sheemei Lok </span> </a> <a target="_blank" href="https://orcid.org/0000-0003-4631-8041" aria-label="Open the ORCID record for Sheemei Lok in new tab/window" class="app-link review__author__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-4d0e8700><img src="data:image/svg+xml;base64,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" alt="" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span class="review__author__affiliation" data-v-4d0e8700><span data-v-4d0e8700> Emerging Infectious Diseases, Duke-NUS Medical School, Singapore </span></span></div></div></div> <div data-v-4d0e8700> Date of review: <strong data-v-4d0e8700><span class="app-date" data-v-d415a782 data-v-4d0e8700> 14 September 2020 </span></strong></div> <div data-v-4d0e8700>Revision round: 0</div> <div data-v-4d0e8700>Role: reviewer</div> <div data-v-4d0e8700>Recommendation/decision: minor-revision</div></div> <div class="review__statement" data-v-4d0e8700><h3 data-v-4d0e8700>Conflict of interest statement</h3> <div data-v-4d0e8700>Reviewer declares none.</div></div> <div class="review__comments" data-v-4d0e8700><h3 data-v-4d0e8700>Comments</h3> <div data-v-4d0e8700><p> <span class="italic">Comments to Author</span>: "A 3.4Å cryoEM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles" by Zhang et al</p><p>The authors reported a 3.4Å resolution cryoEM structure of the S protein on the NL63 virus. Previously another cryoEM structure of the recombinantly expressed ectodomain of the NL63 S protein was determined to similar resolution (Walls et al., 2016). Structural comparison shows they are highly similar except that the current structure on the virus surface shows more glycosylation sites likely because the virus was grown in mammalian cells compared to the ectodomain S protein that was expressed in insect cells. Their map also showed extended density pointing towards the viral membrane although they are unable to recognize secondary structure elements. Also they showed that the RBD domain of the S proteins on the virus surface are in a "down" or "closed" state.</p><p>Glycosylation can shield the protein structures from antibody binding, therefore the level of glycosylation will affect the antigenic property of the S proteins. The results here showed that in mammalian cells, the protein are highly glycosylated. This offer important information perhaps to why antibody response is poor towards coronaviruses. The structural studies here is technically well done.</p><p>This reviewer only have minor comments:</p><p>(1)Page 4 line 113, the authors should put the reference to the map of the purified S ectodomain or its EMDB code.</p><p>(2)Page 5 line 130 "As shown in Fig. 1 and 2", I don't not see any figures regarding the RBD in a downwards conformation in Figure 2. Is that a mistake?</p><p>(3)There is no title for Table 1 and Supplementary Table S2</p><p>(4)Figure S1: It is hard to see the overlap of the two maps with and without C3 imposed.</p><p>(5)Caption of Figure 1: (c-d) should mention the cryoEM map is that of the C3 averaged map or not.</p></div></div> <hr aria-hidden="true" class="review__separator separator default" data-v-7036083a data-v-4d0e8700></div><div id="full-review-3" class="review" data-v-4d0e8700><div class="review__headings" data-v-4d0e8700><h2 data-v-4d0e8700><div class="article-title">Decision: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R0/PR3</div></h2> <button aria-expanded="false" data-test-id="buttonCiteOptions" data-prod-id="2C758F9BBF34CB087A51DE54730BF3D0" data-toggle="modal" href="#cite-modal" class="app-button cite-button d-print-none app-button__text-icon app-button--secondary export-citation-product" data-v-2a038744 data-v-2ce5f61d data-v-4d0e8700><img src="/core/page-component/img/cite-icon.44eaaa4.svg" alt="" class="app-icon icon cite" data-v-d2c09870 data-v-2a038744> <span class="text" data-v-2a038744>Cite</span></button></div> <div class="review__metadata" data-v-4d0e8700><div data-v-4d0e8700> Published online by Cambridge University Press: <strong data-v-4d0e8700><span class="app-date" data-v-d415a782 data-v-4d0e8700> 17 November 2020 </span></strong></div> DOI: <a target="_blank" href="https://doi.org/10.1017/qrd.2020.16.pr3" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>https://doi.org/10.1017/qrd.2020.16.pr3 </span> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <div class="review__reviewer" data-v-4d0e8700><div data-v-4d0e8700><div class="review__author" data-v-4d0e8700><a href="/core/search?filters%5BauthorTerms%5D=Bengt%20J.%20F.%20Nord%C3%A9n&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>Bengt J. F. Nordén </span> </a> <a target="_blank" href="https://orcid.org/0000-0002-7946-200X" aria-label="Open the ORCID record for Bengt J. F. Nordén in new tab/window" class="app-link review__author__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-4d0e8700><img src="data:image/svg+xml;base64,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" alt="" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span class="review__author__affiliation" data-v-4d0e8700><span data-v-4d0e8700> Chemistry and Chemical Engineering, Chalmers University of Technology, Sweden </span></span></div></div></div>  <div data-v-4d0e8700>Revision round: 0</div> <div data-v-4d0e8700>Role: Chair of the Board of Editors</div> <div data-v-4d0e8700>Recommendation/decision: minor-revision</div></div>  <div class="review__comments" data-v-4d0e8700><h3 data-v-4d0e8700>Comments</h3> <div data-v-4d0e8700><p> <span class="italic">Comments to Author</span>: Reviewer #1: "A 3.4Å cryoEM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles" by Zhang et al</p><p>The authors reported a 3.4Å resolution cryoEM structure of the S protein on the NL63 virus. Previously another cryoEM structure of the recombinantly expressed ectodomain of the NL63 S protein was determined to similar resolution (Walls et al., 2016). Structural comparison shows they are highly similar except that the current structure on the virus surface shows more glycosylation sites likely because the virus was grown in mammalian cells compared to the ectodomain S protein that was expressed in insect cells. Their map also showed extended density pointing towards the viral membrane although they are unable to recognize secondary structure elements. Also they showed that the RBD domain of the S proteins on the virus surface are in a "down" or "closed" state.</p><p>Glycosylation can shield the protein structures from antibody binding, therefore the level of glycosylation will affect the antigenic property of the S proteins. The results here showed that in mammalian cells, the protein are highly glycosylated. This offer important information perhaps to why antibody response is poor towards coronaviruses. The structural studies here is technically well done.</p><p>This reviewer only have minor comments:</p><p>(1)Page 4 line 113, the authors should put the reference to the map of the purified S ectodomain or its EMDB code.</p><p>(2)Page 5 line 130 "As shown in Fig. 1 and 2", I don't not see any figures regarding the RBD in a downwards conformation in Figure 2. Is that a mistake?</p><p>(3)There is no title for Table 1 and Supplementary Table S2</p><p>(4)Figure S1: It is hard to see the overlap of the two maps with and without C3 imposed.</p><p>(5)Caption of Figure 1: (c-d) should mention the cryoEM map is that of the C3 averaged map or not.</p><p>Reviewer #2: The manuscript "A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles" by Zhang and co-authors reports a structure of the human coronavirus NL63 (HCoV-NL63) spike. This impactful study provides analysis of domain localisations within the HCoV-NL63 S (spike) trimer without chemical fixative in its prefusion conformation. Cryo-EM has been used in this structural study. The results of the research reported in the MS have several major outcomes. Firstly, the authors have proved the faithfulness of structural organisation of the NL63 spike obtained.Two structures (one from vitrified complete virus and another obtained using an expression system forHCoV-NL63 S ectodomain) demonstrate high level of consistency. Secondly, such consistency allowed analysing differences between the NL63 spike and the SARS-CoV-2 S structures, revealing and evaluation sites related to the receptor bindings. Thirdly, the structure of the NL63 spike from the vitrified viruses provides more complete information on glycosylation sites. This study will help to explain discrepancy in the pathogenicity between alpha and beta families of coronaviruses.</p><p>The methodologies used for the imaging and reconstruction processing followed by building the atomic modelare on the level of the state-of-the-art. The MS is well written and concise.Overall this is an important study at the current pandemic and linked to pathogenicity of the virus. It is related to the findingmedical means for suppressing infections.</p><p>It would be good if the comments listed below will be addressed:</p><p>Comparison of structures NL63 (HCoV-NL63) and SARS-CoV-2spikes indicated large rearrangements between domainsA and B. What is known about similarity (homology) of these domains and linkers between them?While a simplified schematic representation was given inWalls et all (NSMB,2016, Fig4) it does not provide sufficient information for explanation of biological relevance of this conformational differences.It would be useful to see the sequence alignment at least for domains ABCD (as a supplementary figure). Possibly, it will help to explain such big shift of the B domain in the SARS-CoV-2 S and the open conformation of the RBDs. It seems that the linker between A and B is shorter in NL63 so a different mechanism should be used for triggering the receptor binding.</p><p>It is rather difficult to find both the upstream helix and locations of the triggers loops within the entire spike structures.Therefore, it would be useful to highlight locations of the S2' trigger-loop region on side views of spikes (Figure 4a). Here may be hidden a very interesting mechanism of the spike activation.</p><p>The Fourier-Shell correlation graph should be deposited to the EMDB. Page 18 of the report: the table "Experimental information" 4 is practically empty, although these information is present in methods.</p><p>The authors have done good fitting and geometry of the model is rather good, but they did not read the report of evaluation of the fit quality:</p><p>"A red diamond above a residue indicates a poor fit to the EM map for this residue (all atom inclusion < 40%)." That effect takes place if the authors have used a too high threshold for the presentation and fitting of the model into the map. So it would make sense to try a lower threshold and the number of red diamonds will be possibly reduced and hopefully will be more consistent with other graphs in the evaluation report.</p><p>It would be good to explain why locations of ligands were poorly defined, since too many of them have high percentage of misplacements (both in bonds length and angles). While this fact does not diminish the value of the MS some verbal explanation will be helpful.</p></div></div> <hr aria-hidden="true" class="review__separator separator default" data-v-7036083a data-v-4d0e8700></div><div id="full-review-4" class="review" data-v-4d0e8700><div class="review__headings" data-v-4d0e8700><h2 data-v-4d0e8700><div class="article-title">Decision: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R1/PR4</div></h2> <button aria-expanded="false" data-test-id="buttonCiteOptions" data-prod-id="E2C45115C6ACA2E9DAEF737AF7C24EAE" data-toggle="modal" href="#cite-modal" class="app-button cite-button d-print-none app-button__text-icon app-button--secondary export-citation-product" data-v-2a038744 data-v-2ce5f61d data-v-4d0e8700><img src="/core/page-component/img/cite-icon.44eaaa4.svg" alt="" class="app-icon icon cite" data-v-d2c09870 data-v-2a038744> <span class="text" data-v-2a038744>Cite</span></button></div> <div class="review__metadata" data-v-4d0e8700><div data-v-4d0e8700> Published online by Cambridge University Press: <strong data-v-4d0e8700><span class="app-date" data-v-d415a782 data-v-4d0e8700> 17 November 2020 </span></strong></div> DOI: <a target="_blank" href="https://doi.org/10.1017/qrd.2020.16.pr4" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>https://doi.org/10.1017/qrd.2020.16.pr4 </span> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <div class="review__reviewer" data-v-4d0e8700><div data-v-4d0e8700><div class="review__author" data-v-4d0e8700><a href="/core/search?filters%5BauthorTerms%5D=Bengt%20J.%20F.%20Nord%C3%A9n&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>Bengt J. F. Nordén </span> </a> <a target="_blank" href="https://orcid.org/0000-0002-7946-200X" aria-label="Open the ORCID record for Bengt J. F. Nordén in new tab/window" class="app-link review__author__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-4d0e8700><img src="data:image/svg+xml;base64,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" alt="" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span class="review__author__affiliation" data-v-4d0e8700><span data-v-4d0e8700> Chemistry and Chemical Engineering, Chalmers University of Technology, Sweden </span></span></div></div></div>  <div data-v-4d0e8700>Revision round: 1</div> <div data-v-4d0e8700>Role: Chair of the Board of Editors</div> <div data-v-4d0e8700>Recommendation/decision: minor-revision</div></div>  <div class="review__comments" data-v-4d0e8700><h3 data-v-4d0e8700>Comments</h3> <div data-v-4d0e8700><p>No accompanying comment.</p></div></div> <hr aria-hidden="true" class="review__separator separator default" data-v-7036083a data-v-4d0e8700></div><div id="full-review-5" class="review" data-v-4d0e8700><div class="review__headings" data-v-4d0e8700><h2 data-v-4d0e8700><div class="article-title">Decision: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R2/PR5</div></h2> <button aria-expanded="false" data-test-id="buttonCiteOptions" data-prod-id="94B30B4EB5804534CE6F3A9CA311BB69" data-toggle="modal" href="#cite-modal" class="app-button cite-button d-print-none app-button__text-icon app-button--secondary export-citation-product" data-v-2a038744 data-v-2ce5f61d data-v-4d0e8700><img src="/core/page-component/img/cite-icon.44eaaa4.svg" alt="" class="app-icon icon cite" data-v-d2c09870 data-v-2a038744> <span class="text" data-v-2a038744>Cite</span></button></div> <div class="review__metadata" data-v-4d0e8700><div data-v-4d0e8700> Published online by Cambridge University Press: <strong data-v-4d0e8700><span class="app-date" data-v-d415a782 data-v-4d0e8700> 17 November 2020 </span></strong></div> DOI: <a target="_blank" href="https://doi.org/10.1017/qrd.2020.16.pr5" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>https://doi.org/10.1017/qrd.2020.16.pr5 </span> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <div class="review__reviewer" data-v-4d0e8700><div data-v-4d0e8700><div class="review__author" data-v-4d0e8700><a href="/core/search?filters%5BauthorTerms%5D=Bengt%20J.%20F.%20Nord%C3%A9n&eventCode=SE-AU" class="app-link app-link__text app-link--accent" data-v-63dfaf6e data-v-4d0e8700><span class="text" data-v-63dfaf6e>Bengt J. F. Nordén </span> </a> <a target="_blank" href="https://orcid.org/0000-0002-7946-200X" aria-label="Open the ORCID record for Bengt J. F. Nordén in new tab/window" class="app-link review__author__orcid app-link__icon app-link--" data-v-63dfaf6e data-v-4d0e8700><img src="data:image/svg+xml;base64,PD94bWwgdmVyc2lvbj0iMS4wIiBlbmNvZGluZz0idXRmLTgiPz4KPHN2ZyB3aWR0aD0iMjIiIGhlaWdodD0iMjIiIHZlcnNpb249IjEuMSIgaWQ9IkxheWVyXzEiIHhtbG5zPSJodHRwOi8vd3d3LnczLm9yZy8yMDAwL3N2ZyIgeG1sbnM6eGxpbms9Imh0dHA6Ly93d3cudzMub3JnLzE5OTkveGxpbmsiIHg9IjBweCIgeT0iMHB4IgoJIHZpZXdCb3g9IjAgMCAyNTYgMjU2IiBzdHlsZT0iZW5hYmxlLWJhY2tncm91bmQ6bmV3IDAgMCAyNTYgMjU2OyIgeG1sOnNwYWNlPSJwcmVzZXJ2ZSI+CjxzdHlsZSB0eXBlPSJ0ZXh0L2NzcyI+Cgkuc3Qwe2ZpbGw6I0E2Q0UzOTt9Cgkuc3Qxe2ZpbGw6I0ZGRkZGRjt9Cjwvc3R5bGU+CjxwYXRoIGNsYXNzPSJzdDAiIGQ9Ik0yNTYsMTI4YzAsNzAuNy01Ny4zLDEyOC0xMjgsMTI4QzU3LjMsMjU2LDAsMTk4LjcsMCwxMjhDMCw1Ny4zLDU3LjMsMCwxMjgsMEMxOTguNywwLDI1Niw1Ny4zLDI1NiwxMjh6Ii8+CjxnPgoJPHBhdGggY2xhc3M9InN0MSIgZD0iTTg2LjMsMTg2LjJINzAuOVY3OS4xaDE1LjR2NDguNFYxODYuMnoiLz4KCTxwYXRoIGNsYXNzPSJzdDEiIGQ9Ik0xMDguOSw3OS4xaDQxLjZjMzkuNiwwLDU3LDI4LjMsNTcsNTMuNmMwLDI3LjUtMjEuNSw1My42LTU2LjgsNTMuNmgtNDEuOFY3OS4xeiBNMTI0LjMsMTcyLjRoMjQuNQoJCWMzNC45LDAsNDIuOS0yNi41LDQyLjktMzkuN2MwLTIxLjUtMTMuNy0zOS43LTQzLjctMzkuN2gtMjMuN1YxNzIuNHoiLz4KCTxwYXRoIGNsYXNzPSJzdDEiIGQ9Ik04OC43LDU2LjhjMCw1LjUtNC41LDEwLjEtMTAuMSwxMC4xYy01LjYsMC0xMC4xLTQuNi0xMC4xLTEwLjFjMC01LjYsNC41LTEwLjEsMTAuMS0xMC4xCgkJQzg0LjIsNDYuNyw4OC43LDUxLjMsODguNyw1Ni44eiIvPgo8L2c+Cjwvc3ZnPgo=" alt="" class="app-icon icon orcid" data-v-d2c09870 data-v-63dfaf6e> <span class="sr-only" data-v-63dfaf6e>[Opens in a new window]</span></a> <span class="review__author__affiliation" data-v-4d0e8700><span data-v-4d0e8700> Chemistry and Chemical Engineering, Chalmers University of Technology, Sweden </span></span></div></div></div>  <div data-v-4d0e8700>Revision round: 2</div> <div data-v-4d0e8700>Role: Chair of the Board of Editors</div> <div data-v-4d0e8700>Recommendation/decision: accept</div></div>  <div class="review__comments" data-v-4d0e8700><h3 data-v-4d0e8700>Comments</h3> <div data-v-4d0e8700><p>No accompanying comment.</p></div></div> </div></div> <div id="metrics-tab" publication-date="17 November 2020" class="metrics tab-pane" data-v-c41a0c86><div class="app-loader" data-v-c41a0c86></div></div></div></div> </div> <div role="complementary" aria-label="related contents" class="column__main__right" data-v-01274b1d><div class="access-block row access-status" data-v-5fad35b8 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Zhang",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Kaiming%20Zhang&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0003-0414-4776"},{givenNames:"Shanshan",surname:"Li",nameStyle:j,affiliations:[{text:p}],isCorresponding:a,notes:b,isAnonymous:a,fullName:"Shanshan Li",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Shanshan%20Li&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0002-7041-5960"},{givenNames:"Grigore",surname:"Pintilie",nameStyle:j,affiliations:[{text:p}],isCorresponding:a,notes:b,isAnonymous:a,fullName:"Grigore Pintilie",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Grigore%20Pintilie&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0002-0848-5335"},{givenNames:"David",surname:"Chmielewski",nameStyle:j,affiliations:[{text:"Graduate Program in Biophysics, Stanford University, Stanford, CA94305, USA"}],isCorresponding:a,notes:b,isAnonymous:a,fullName:"David Chmielewski",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=David%20Chmielewski&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0002-4498-7949"},{givenNames:"Michael F.",surname:"Schmid",nameStyle:j,affiliations:[{text:z}],isCorresponding:a,notes:b,isAnonymous:a,fullName:"Michael F. Schmid",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Michael%20F.%20Schmid&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0003-1077-5750"},{givenNames:"Graham",surname:"Simmons",nameStyle:j,affiliations:[{text:P}],isCorresponding:a,notes:b,isAnonymous:a,fullName:"Graham Simmons",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Graham%20Simmons&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0002-9615-7023"},{givenNames:"Jing",surname:"Jin",nameStyle:j,affiliations:[{text:P},{text:z}],isCorresponding:a,notes:b,isAnonymous:a,fullName:"Jing Jin",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Jing%20Jin&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0003-3994-8600"},{givenNames:"Wah",surname:"Chiu",nameStyle:j,affiliations:[{text:p},{text:z}],isCorresponding:c,notes:"\u003Cdiv class=\"corresp\"\u003E\u003Cspan class=\"label\"\u003E*\u003C\u002Fspan\u003E\u003Cspan class=\"bold\"\u003EAuthor for correspondence:\u003C\u002Fspan\u003E Wah Chiu, E-mail: \u003Ca href=\"mailto:wahc@stanford.edu\"\u003Ewahc@stanford.edu\u003C\u002Fa\u003E\u003C\u002Fdiv\u003E",isAnonymous:a,fullName:"Wah Chiu",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Wah%20Chiu&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0002-8910-3078"}]},translators:{contributors:[],label:"Translated by"}},collections:[],publishedDate:"17 November 2020",keywords:[{url:"\u002Fcore\u002Fsearch?filters[keywords]=Cryo-EM",name:"Cryo-EM"},{url:"\u002Fcore\u002Fsearch?filters[keywords]=human coronavirus NL63",name:"human coronavirus NL63"},{url:"\u002Fcore\u002Fsearch?filters[keywords]=spike trimer",name:"spike trimer"}],openPracticeBadges:[],doi:{url:Q,value:R},copyright:{statement:["© The Author(s) 2020. Published by Cambridge University Press"],holder:["The Author(s) 2020. Published by Cambridge University Press"],year:[2020]},creativeCommons:{descriptions:["This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (\u003Ca href=\"http:\u002F\u002Fcreativecommons.org\u002Flicenses\u002Fby\u002F4.0\u002F\" target=\"_blank\"\u003Ehttp:\u002F\u002Fcreativecommons.org\u002Flicenses\u002Fby\u002F4.0\u002F\u003C\u002Fa\u003E), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited."],oaLicenseType:"CC-BY",licenses:["CC","BY"]},acceptedManuscript:a,type:"research-article",typeDescription:"Research Article",eNumber:"e11",commentsCount:S,topicsAndSubtopics:g},journal:{id:T,title:q,titleSlug:U,mnemonic:"QRD",titleHistory:[],isFirstView:a,journalSlug:U,isCompanion:a,parentCompanionJournalName:q,associatedParentCollection:g,url:V,firstViewUrl:"\u002Fcore\u002Fjournals\u002Fqrb-discovery\u002Ffirstview",coverUrl:"https:\u002F\u002Fstatic.cambridge.org\u002Fcovers\u002FQRD_0_0_0\u002Fqrb-discovery.jpg",submitMaterialsUrl:"\u002Fcore\u002Fjournals\u002Fqrb-discovery\u002Finformation\u002Fauthor-instructions\u002Fsubmitting-your-materials",hasHistory:a,latestTitle:q,latestId:T,hasPastTitle:a,volume:{id:"F8B5CF3E0096CC946882DA4D8D779FE9",number:W,title:X,publishedDate:h,printPublishTimestamp:1577836800000,url:Y}},abstract:{textAbstracts:[{title:"Abstract",content:"\u003Cdiv class=\"abstract\" data-abstract-type=\"normal\"\u003E\u003Cp\u003EHuman coronavirus NL63 (HCoV-NL63) is an enveloped pathogen of the family \u003Cspan class=\"italic\"\u003ECoronaviridae\u003C\u002Fspan\u003E that spreads worldwide and causes up to 10% of all annual respiratory diseases. HCoV-NL63 is typically associated with mild upper respiratory symptoms in children, elderly and immunocompromised individuals. It has also been shown to cause severe lower respiratory illness. NL63 shares ACE2 as a receptor for viral entry with SARS-CoV-1 and SARS-CoV-2. Here, we present the \u003Cspan class=\"italic\"\u003Ein situ\u003C\u002Fspan\u003E structure of HCoV-NL63 spike (S) trimer at 3.4-Å resolution by single-particle cryo-EM imaging of vitrified virions without chemical fixative. It is structurally homologous to that obtained previously from the biochemically purified ectodomain of HCoV-NL63 S trimer, which displays a three-fold symmetric trimer in a single conformation. In addition to previously proposed and observed glycosylation sites, our map shows density at other sites, as well as different glycan structures. The domain arrangement within a protomer is strikingly different from that of the SARS-CoV-2 S and may explain their different requirements for activating binding to the receptor. This structure provides the basis for future studies of spike proteins with receptors, antibodies or drugs, in the native state of the coronavirus particles.\u003C\u002Fp\u003E\u003C\u002Fdiv\u003E",lang:Z}]},content:{html:"\u003Cdiv class=\"article research-article NLM\"\u003E\n\n\u003Cdiv class=\"body\"\u003E\n\u003Cdiv class=\"sec intro\" data-magellan-destination=\"sec1\" id=\"sec1\"\u003E\n\u003Ch2 class=\"A\"\u003E Introduction\u003C\u002Fh2\u003E\n\u003Cp class=\"p\"\u003E \u003Cem class=\"italic\"\u003ECoronaviridae\u003C\u002Fem\u003E constitute a large family of enveloped, positive-sense single-stranded RNA (+ssRNA) viruses capable of causing severe and widespread human respiratory disease. The coronaviruses are zoonotic pathogens, often circulating among natural reservoirs, such as bats or camels prior to crossing the species barrier into humans (Wang \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref30\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Wang, Shi, Zhang, Field, Daszak and Eaton\u003C\u002Fspan\u003E2006\u003C\u002Fa\u003E; Sabir \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref21\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Sabir, Lam, Ahmed, Li, Shen, Abo- Aba and Guan\u003C\u002Fspan\u003E2015\u003C\u002Fa\u003E). Coronaviruses are classified into four genera (alpha-CoV, beta-CoV, gamma-CoV and delta-CoV), with human coronaviruses found in two: alpha-CoVs (HCoV-229E and HCoV-NL63) and beta-CoVs [middle-east respiratory syndrome (MERS) and severe acute respiratory syndrome coronavirus 1 and 2 (SARS-CoV-1 and SARS-CoV-2)] (Cui \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref7\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Cui, Li and Shi\u003C\u002Fspan\u003E2018\u003C\u002Fa\u003E). SARS-CoV-2, responsible for the COVID-19 pandemic, has infected over 47 million people and claimed over 1.2 million lives worldwide as of early November 2020, underscoring the urgency of studying all circulating human coronaviruses (\u003Ca class=\"uri\" href=\"https:\u002F\u002Fcovid19.who.int\u002F\"\u003Ehttps:\u002F\u002Fcovid19.who.int\u002F\u003C\u002Fa\u003E) (Cui \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref7\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Cui, Li and Shi\u003C\u002Fspan\u003E2018\u003C\u002Fa\u003E; Zhou \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref41\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Zhou, Yang, Wang, Hu, Zhang, Zhang and Shi\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E). While beta-CoVs are more commonly associated with high pathogenicity and severe respiratory disease, alpha-CoVs are widely circulating viruses associated with cold-like symptoms, and in rare cases, more serious respiratory failure (Wang \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref31\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Wang, Li, Liu, Gan, Zhang, Wang and Zhao\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E). HCoV-NL63 is estimated to be the causative agent of up to 10% of annual respiratory disease and is a major cause of bronchiolitis and pneumonia in newborns (van der Hoek \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref10\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Van der Hoek, Pyrc, Jebbink, Vermeulen- Oost, Berkhout, Wolthers and Berkhout\u003C\u002Fspan\u003E2004\u003C\u002Fa\u003E; Chiu \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref6\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Chiu, Hung Chan, Wing Chu, Kwan, Guan, Man Poon and Peiris\u003C\u002Fspan\u003E2005\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\n\u003Cp class=\"p\"\u003E Coronaviruses utilize large spike (S) homotrimers (500-600 kDa) protruding from the viral membrane to engage cellular receptors and mediate fusion with host membranes (Thorp \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref24\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Thorp, Boscarino, Logan, Goletz and Gallagher\u003C\u002Fspan\u003E2006\u003C\u002Fa\u003E; Pallesen \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref16\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pallesen, Wang, Corbett, Wrapp, Kirchdoerfer, Turner and McLellan\u003C\u002Fspan\u003E2017\u003C\u002Fa\u003E). These spikes, numerous on the virus surface, constitute the primary target of neutralizing antibodies (NAbs) and are central to vaccine design and structural studies for drug optimization. Each S protomer contains two large regions: N-terminal S1 responsible for receptor-binding and C-terminal S2 responsible for type-I fusion, as well as an additional single-pass transmembrane helix that anchors the spike to the viral envelope (Bosch \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref3\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Bosch, van der Zee, de Haan and Rottier\u003C\u002Fspan\u003E2003\u003C\u002Fa\u003E; Zheng \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref39\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Zheng, Deng, Liu, van der Hoek, Berkhout and Lu\u003C\u002Fspan\u003E2006\u003C\u002Fa\u003E). Spikes are activated by protease cleavage, near the putative fusion peptide, allowing the transition from pre- to post-fusion conformation during virus entry (Belouzard \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref2\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Belouzard, Chu and Whittaker\u003C\u002Fspan\u003E2009\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\n\u003Cp class=\"p\"\u003E Several single-particle cryo-electron microscopy (cryo-EM) structures of purified ectodomains of pre-fusion S trimers from alpha-CoV and beta-CoV genera have been determined, illustrating conformational heterogeneity of S1, multiple glycosylation sites, and the interactions with soluble receptors and NAbs (Walls \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref27\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler\u003C\u002Fspan\u003E2016\u003C\u002Fa\u003E, \u003Ca class=\"xref bibr\" href=\"#ref28\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Walls, Park, Tortorici, Wall, McGuire and Veesler\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E; Song \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref23\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Song, Gui, Wang and Xiang\u003C\u002Fspan\u003E2018\u003C\u002Fa\u003E; Wrapp \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref36\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Wrapp, Wang, Corbett, Goldsmith, Hsieh, Abiona and McLellan\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E). These S complexes lack the helical C-terminal stem that connects S2 to the viral envelope, and require residues mutated to proline at the loop between the first heptad repeat and the central helix to stabilize the construct (Pallesen \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref16\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pallesen, Wang, Corbett, Wrapp, Kirchdoerfer, Turner and McLellan\u003C\u002Fspan\u003E2017\u003C\u002Fa\u003E; Kirchdoerfer \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref12\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Kirchdoerfer, Wang, Pallesen, Wrapp, Turner, Cottrell and Ward\u003C\u002Fspan\u003E2018\u003C\u002Fa\u003E; Park \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref17\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Park, Walls, Wang, Sauer, Li, Tortorici and Veesler\u003C\u002Fspan\u003E2019\u003C\u002Fa\u003E). High-resolution structure determinations of molecular components in pleomorphic virions are typically obtained by single-particle cryo-EM or X-ray crystallography of exogenously expressed and purified components. Conversely, cryo-electron tomography (cryo-ET) has been used to reconstruct tomograms of the whole virus particles, from which sub-volume density, corresponding to the feature of interest, would be further processed by classification and averaging (Schmid \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref22\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Schmid, Hecksel, Rochat, Bhella, Chiu and Rixon\u003C\u002Fspan\u003E2012\u003C\u002Fa\u003E; Wan and Briggs, \u003Ca class=\"xref bibr\" href=\"#ref32\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Wan and Briggs\u003C\u002Fspan\u003E2016\u003C\u002Fa\u003E). Here, we take the approach of utilizing single-particle cryo-EM imaging of purified and vitrified HCoV-NL63 virus particles, and then using computational methods to extract the S trimer density for its high-resolution structure determination. Our approach is similar to a recent preprint report for chemically fixed SARS-CoV-2 particles (Ke \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref11\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Ke, Oton, Qu, Cortese, Zila, McKeane and Briggs\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E). We report the 3.4-Å structure of the S trimer in its native, pre-fusion state, and expect our data will be of value in future drug and vaccine design for various strains of coronaviruses without the need to genetically construct and biochemically purify spike proteins.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec2\" id=\"sec2\"\u003E\n\u003Ch2 class=\"A\"\u003E Results and discussion\u003C\u002Fh2\u003E\n\u003Cp class=\"p\"\u003E Since the S trimers protrude from the membrane surface of the virion, many of the crown-shaped S trimers can be easily identified, computationally extracted from the raw images, and treated as single-particle images with a distinct particle orientation without the need of tilting the specimens (\u003Ca class=\"xref fig\" href=\"#fig1\"\u003EFig. 1\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E). Based on the fact that single-particle cryo-EM is a more routine procedure for computing high-resolution structures compared to cryo-ET, we decided not to collect tilt series, and used single-particle cryo-EM analysis of the native S trimer on purified and vitrified virions. The two-dimensional (2D) class averages showed a clear triangular shape for the S trimer and other distinct views (\u003Ca class=\"xref fig\" href=\"#fig1\"\u003EFig. 1\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E). D\u003Cem class=\"italic\"\u003Ee novo\u003C\u002Fem\u003E building of the initial map, using the ‘Ab-initio reconstruction’ option in cryoSPARC without any symmetry applied, resulted in a three-dimensional (3D) structure with well-defined features. Further 3D refinement was performed with and without C3 symmetry to obtain 3.4 and 3.7 Å maps, respectively (\u003Ca class=\"xref fig\" href=\"#fig1\"\u003EFig. 1\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ec–e\u003C\u002Fem\u003E and Fig. S1). The reconstructed map without imposed symmetry also displayed three-fold symmetry, showing a high cross-correlation coefficient (CC = 0.98) with the symmetric map (Fig. S1\u003Cem class=\"italic\"\u003Ed\u003C\u002Fem\u003E). Hereafter, we will present our structural analysis of the 3.4-Å map with C3 imposed symmetry after refinement from a subset of ~82,000 S trimer particles showing adequate orientation sampling (Fig. S1). The local resolution varies in our map (\u003Ca class=\"xref fig\" href=\"#fig1\"\u003EFig. 1\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ee\u003C\u002Fem\u003E); the densities at the outer surface of the protein have a much lower resolution than the central region (\u003Ca class=\"xref fig\" href=\"#fig1\"\u003EFig. 1\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ee\u003C\u002Fem\u003E), which could be attributed to the inherent flexibility of the distal ends of glycans. Compared to the map of the purified S ectodomain (EMD-8331), our map has a more extended density without recognizable secondary structure element features that points towards the viral membrane (\u003Ca class=\"xref fig\" href=\"#fig1\"\u003EFig. 1\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ee\u003C\u002Fem\u003E). The detection of this feature likely results from the direct picking of S trimer anchored in the lipid envelope of native virions, which stabilizes the stem region that otherwise disassembles in the purified S ectodomains.\u003C\u002Fp\u003E\u003Csection\u003E\u003Cdiv class=\"fig\" data-magellan-destination=\"fig1\" id=\"fig1\"\u003E\n\n\n\u003Cdiv class=\"figure-thumb\"\u003E\u003Cimg src=\"data:image\u002Fgif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==\" data-src=\"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig1.png?pub-status=live\" class=\"aop-lazy-load-image\" width=\"1750\" height=\"1617\" data-original-image=\"\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig1.png\" data-zoomable=\"true\"\u003E\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"caption\"\u003E\u003Cp class=\"p\"\u003E \n\u003C\u002Fp\u003E\u003Cp class=\"p\"\u003E\u003Cspan class=\"label\"\u003EFig. 1.\u003C\u002Fspan\u003E Single-particle cryo-EM analysis of \u003Cem class=\"italic\"\u003Ein-situ\u003C\u002Fem\u003E structure of the HCoV-NL63 coronavirus spike glycoprotein. (\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E) Representative motion-corrected cryo-EM micrograph. (\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E) Reference-free 2D class averages of computationally extracted spikes. (\u003Cem class=\"italic\"\u003Ec-d\u003C\u002Fem\u003E) Reconstructed 3-fold symmetry-imposed cryo-EM map of the spike in the top and side views without (c) and with (\u003Cem class=\"italic\"\u003Ed\u003C\u002Fem\u003E) glycans shown. (\u003Cem class=\"italic\"\u003Ee\u003C\u002Fem\u003E) Resolution variation maps for 3D reconstruction. Left, whole map view; middle, slice view; right, whole map view at a lower threshold.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\u003C\u002Fdiv\u003E\u003C\u002Fsection\u003E\n\u003Cp class=\"p\"\u003E Because of the high feature similarity of our map to that determined from the biochemically purified S ectodomain (Walls \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref27\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler\u003C\u002Fspan\u003E2016\u003C\u002Fa\u003E), we fitted the published model (PDB ID: 5SZS) including the glycans to our 3.4-Å map and refined it. Residues 883–889 and 993–1000 that were previously unresolved were also modeled (see Methods section). The quality of the final model was validated by MolProbity (Chen \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref5\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Chen, Arendall, Headd, Keedy, Immormino, Kapral and Richardson\u003C\u002Fspan\u003E2009\u003C\u002Fa\u003E) (Table S1), the cross correlation between the map and model (\u003Ca class=\"xref fig\" href=\"#fig2\"\u003EFig. 2\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E), and Q-score analysis per residue (Pintilie \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref19\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pintilie, Zhang, Su, Li, Schmid and Chiu\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E) (\u003Ca class=\"xref fig\" href=\"#fig2\"\u003EFig. 2\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Eb–e\u003C\u002Fem\u003E). The density map of our structure is better resolved in many regions, relative to the previous structure (PDB ID: 5SZS), including glycans (\u003Ca class=\"xref fig\" href=\"#fig3\"\u003EFig. 3\u003C\u002Fa\u003E), which were previously interpreted with accompanied mass spectrometry measurements (Walls \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref27\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler\u003C\u002Fspan\u003E2016\u003C\u002Fa\u003E). Superimposition of our model and 5SZS yields 804 pruned atom pairs matched with 1.28-Å root mean square deviation (RMSD), indicating their high structural similarity. Structural comparisons based on individual domains also show similar results. These domains include domain 0, domain A, domain B (also known as RBD), domain C, and domain D, with the RMSD ranging from 0.29 Å to 0.90 Å. As shown in \u003Ca class=\"xref fig\" href=\"#fig1\"\u003EFig. 1\u003C\u002Fa\u003E, each of the three receptor-binding domains (RBDs) within the S trimer is pointed downwards. Notably, heterogeneous refinement and 3D variability did not reveal alternative RBD conformations, implying that the native S trimer proteins on the virion are predominantly in a fully closed state, consistent with the previous report of purified HCoV-NL63 S ectodomain (Walls \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref27\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler\u003C\u002Fspan\u003E2016\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\u003Csection\u003E\u003Cdiv class=\"fig\" data-magellan-destination=\"fig2\" id=\"fig2\"\u003E\n\n\n\u003Cdiv class=\"figure-thumb\"\u003E\u003Cimg src=\"data:image\u002Fgif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==\" data-src=\"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig2.png?pub-status=live\" class=\"aop-lazy-load-image\" width=\"1692\" height=\"2450\" data-original-image=\"\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig2.png\" data-zoomable=\"true\"\u003E\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"caption\"\u003E\u003Cp class=\"p\"\u003E \n\u003C\u002Fp\u003E\u003Cp class=\"p\"\u003E\u003Cspan class=\"label\"\u003EFig. 2.\u003C\u002Fspan\u003E Model validation of the HCoV-NL63 coronavirus spike glycoprotein protomer. (\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E) Per-residue cross-correlation coefficient between the model and 3.4-Å map. (\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E) Q-score for each amino acid residue in the model and 3.4-Å map; the orange line represents the expected Q-score of 0.52 at 3.4-Å resolution based on the correlation between Q-scores and map resolutions (Pintilie \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref19\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pintilie, Zhang, Su, Li, Schmid and Chiu\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E). (\u003Cem class=\"italic\"\u003Ec–e\u003C\u002Fem\u003E) Examples of different regions of the map with different resolvability: (\u003Cem class=\"italic\"\u003Ec\u003C\u002Fem\u003E) well-resolved, (\u003Cem class=\"italic\"\u003Ed\u003C\u002Fem\u003E) poorly-resolved; (\u003Cem class=\"italic\"\u003Ee\u003C\u002Fem\u003E) residues not resolved in the previous biochemically purified HCoV-NL63 spike protein structure (PDB ID: 5SZS) and thus their model built \u003Cem class=\"italic\"\u003Ede novo\u003C\u002Fem\u003E here. The model is shown as ribbon, with residue Q-scores annotated in colors. The higher Q-score indicates better resolvability.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\u003C\u002Fdiv\u003E\u003C\u002Fsection\u003E\n\u003Csection\u003E\u003Cdiv class=\"fig\" data-magellan-destination=\"fig3\" id=\"fig3\"\u003E\n\n\n\u003Cdiv class=\"figure-thumb\"\u003E\u003Cimg src=\"data:image\u002Fgif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==\" data-src=\"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig3.png?pub-status=live\" class=\"aop-lazy-load-image\" width=\"1501\" height=\"1904\" data-original-image=\"\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig3.png\" data-zoomable=\"true\"\u003E\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"caption\"\u003E\u003Cp class=\"p\"\u003E \n\u003C\u002Fp\u003E\u003Cp class=\"p\"\u003E\u003Cspan class=\"label\"\u003EFig. 3.\u003C\u002Fspan\u003E Resolvability of glycans. (\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E) Q-scores analysis for each glycan residue (# starting from 1401) in model and map; the orange line represents the expected Q-score of 0.52 at 3.4-Å resolution based on the correlation between Q-scores and map resolutions of amino acid residues (Pintilie \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref19\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pintilie, Zhang, Su, Li, Schmid and Chiu\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E). (\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E) Highlights on several glycans. Green: Positive difference density between our and previous map (EMD-8331) suggesting extra glycan densities; Yellow: glycan densities found both in our map and in the previous study. The glycan models were derived from (PDB ID: 5SZS).\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\u003C\u002Fdiv\u003E\u003C\u002Fsection\u003E\n\u003Cp class=\"p\"\u003E Glycosylation of S plays an important role in the viral life cycle and immune-evasion (Vigerust and Shepherd, \u003Ca class=\"xref bibr\" href=\"#ref26\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Vigerust and Shepherd\u003C\u002Fspan\u003E2007\u003C\u002Fa\u003E; Watanabe \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref33\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Watanabe, Bowden, Wilson and Crispin\u003C\u002Fspan\u003E2019\u003C\u002Fa\u003E, \u003Ca class=\"xref bibr\" href=\"#ref34\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Watanabe, Berndsen, Raghwani, Seabright, Allen, Pybus and Crispin\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E; Casalino \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref4\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Casalino, Gaieb, Goldsmith, Hjorth, Dommer, Harbison and Amaro\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E). We observed densities protruding from the amino acid residues corresponding to all the glycan sites that were previously observed in the cryo-EM map of the ectodomain of biochemically purified S (EMD-8331). All these glycosylation sites had been identified by a combination of cryo-EM densities protruding from the expected amino acid side chains and mass spectrometry (\u003Ca class=\"xref table\" href=\"#tab1\"\u003ETable 1\u003C\u002Fa\u003E and Table S2) (Walls \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref27\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler\u003C\u002Fspan\u003E2016\u003C\u002Fa\u003E). The models for these glycans were fitted into our map and their Q scores are shown in \u003Ca class=\"xref fig\" href=\"#fig3\"\u003EFig. 3\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E. Some examples are displayed as NAG residues in \u003Ca class=\"xref fig\" href=\"#fig3\"\u003EFig. 3\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E. To further investigate the possible presence of other glycan moieties, we calculated a difference map between our map and the EMD-8331 (see Methods). We observed positive difference density in five sites shown in green in \u003Ca class=\"xref fig\" href=\"#fig3\"\u003EFig. 3\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E. Two N-linked glycosylation sites (Asn24 and Asn203 in domain 0), predicted to exist from their sequence, as well as one O-linked glycosylation site (Ser496 in domain B), were newly identified in our difference density map (\u003Ca class=\"xref fig\" href=\"#fig3\"\u003EFig. 3\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E and \u003Ca class=\"xref table\" href=\"#tab1\"\u003ETable 1\u003C\u002Fa\u003E). None of these was found by mass spectrometry or shown clearly in the previous map. These differences between our structure and the previously published one are possibly due to the differences in glycosylation patterns across species (Walls \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref27\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Walls, Tortorici, Frenz, Snijder, Li, Rey and Veesler\u003C\u002Fspan\u003E2016\u003C\u002Fa\u003E). In our study, the virus was grown in mammalian cells, while the previous study used S ectodomain expressed in insect cells. N-linked glycosylation in mammalian cells typically results in complex-type glycans with two to four branches extended from the tri-mannosyl core. In contrast, glycosylation in insect cells typically yields truncated, paucimannosidic or oligomannosidic glycans with few if any complex-type glycans (Tomiya \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref25\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Tomiya, Narang, Lee and Betenbaugh\u003C\u002Fspan\u003E2004\u003C\u002Fa\u003E). Overall, there is significant agreement between \u003Cem class=\"italic\"\u003Ein situ\u003C\u002Fem\u003E and biochemically purified S protein structure with these notable differences in glycan densities. Our structure cross-validates the conformation of the spike protein of HCoV-NL63 determined from either the biochemically purified specimen or the intact virions by cryo-EM.\u003C\u002Fp\u003E\u003Cdiv class=\"table-wrap\" data-magellan-destination=\"tab1\" id=\"tab1\"\u003E\n\n\u003Cdiv class=\"caption\"\u003E\n\u003Cp class=\"p\"\u003E\u003Cspan class=\"label\"\u003ETable 1.\u003C\u002Fspan\u003E Newly identified glycosylation sites in this study.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cspan\u003E\n\n\u003Cdiv class=\"figure-thumb\"\u003E\u003Cimg src=\"data:image\u002Fgif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==\" data-src=\"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_tab1.png?pub-status=live\" class=\"aop-lazy-load-image\" width=\"2142\" height=\"276\" data-original-image=\"\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_tab1.png\" data-zoomable=\"true\"\u003E\u003C\u002Fdiv\u003E\n\u003C\u002Fspan\u003E\n\u003Cdiv class=\"table-wrap-foot\"\u003E\n\u003Cp class=\"p\"\u003E Abbreviation: MS, mass spectrometry; ND, not detected; cryo-EM, cryo-electron microscopy.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003C\u002Fdiv\u003E\n\u003Cp class=\"p\"\u003E Compared to the S1 protein of betacoronavirus (i.e. SARS-CoV-2), HCoV-NL63 S1 has an additional N-terminal domain (domain 0) that is assumed to be a gene duplication of domain A and is a canonical feature of alphacoronaviruses. Domain B (RBD) of beta-coronaviruses transitions between upward (open) and downward (closed) conformations due to its inherent flexibility; the viral receptor ACE2 is able to sample the RBD’s up conformation to initiate virus-receptor binding. In contrast, domain B of HCoV-NL63 interacts with domain A, therefore being stabilized in a closed ‘circle’ of HCoV-NL63 S1 (\u003Ca class=\"xref fig\" href=\"#fig4\"\u003EFig. 4\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E). The interface area between domains A and B of HCoV-NL63 is ~500 Å\u003Csup class=\"sup\"\u003E2\u003C\u002Fsup\u003E and involves 22 hydrophobic interactions (\u003Ca class=\"xref fig\" href=\"#fig4\"\u003EFig. 4\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E) according to PDBsum structure bioinformatics analysis (Laskowski \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref13\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Laskowski, Jabłońska, Pravda, Vařeková and Thornton\u003C\u002Fspan\u003E2017\u003C\u002Fa\u003E). The three receptor binding motifs (RBMs) on HCoV-NL63 RBD are consequently buried in the interface between domain A and domain B, and prevented from binding to the viral receptor ACE2 (Wu \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref37\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Wu, Li, Peng and Li\u003C\u002Fspan\u003E2009\u003C\u002Fa\u003E). There must exist a mechanism to induce a conformational change to release the RBMs from domain A to allow receptor binding. It was reported that HCoV-NL63 utilizes heparan sulfate proteoglycans as the attachment factor before binding to ACE2 for virus entry (Milewska \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref14\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Milewska, Zarebski, Nowak, Stozek, Potempa and Pyrc\u003C\u002Fspan\u003E2014\u003C\u002Fa\u003E, \u003Ca class=\"xref bibr\" href=\"#ref15\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Milewska, Nowak, Owczarek, Szczepanski, Zarebski, Hoang and Pyrc\u003C\u002Fspan\u003E2017\u003C\u002Fa\u003E). Whether heparan sulfate binding to HCoV-NL63 S1 or other factors induce conformational changes to release RBMs for ACE2 binding warrants further studies.\u003C\u002Fp\u003E\u003Csection\u003E\u003Cdiv class=\"fig\" data-magellan-destination=\"fig4\" id=\"fig4\"\u003E\n\n\n\u003Cdiv class=\"figure-thumb\"\u003E\u003Cimg src=\"data:image\u002Fgif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==\" data-src=\"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig4.png?pub-status=live\" class=\"aop-lazy-load-image\" width=\"1751\" height=\"2062\" data-original-image=\"\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig4.png\" data-zoomable=\"true\"\u003E\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"caption\"\u003E\u003Cp class=\"p\"\u003E \n\u003C\u002Fp\u003E\u003Cp class=\"p\"\u003E\u003Cspan class=\"label\"\u003EFig. 4.\u003C\u002Fspan\u003E Structure comparison between HCoV-NL63 and SARS-CoV-2 spike. (\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E) Comparison of our structure with SARS-CoV-2 spike in closed state (PDB ID: 6VXX) in two different views. Different domains and the linker (Lk) between domains A and B are indicated in different colors. (\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E) Zoom-in view to show the interactions between domain A and domain B in the HCoV-NL63 spike protein. (\u003Cem class=\"italic\"\u003Ec\u003C\u002Fem\u003E) Extracted densities of the S2 fusion machinery region with models fitted.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\u003C\u002Fdiv\u003E\u003C\u002Fsection\u003E\n\u003Cp class=\"p\"\u003E S proteins of coronaviruses require protease cleavage to release the fusion peptide that inserts into the target membrane to initiate membrane fusion for virus entry. We compared HCoV-NL63 and SARS-CoV-2 S2 fusion machineries by superimposing their structures together and an excellent agreement was observed (\u003Ca class=\"xref fig\" href=\"#fig4\"\u003EFig. 4\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ec\u003C\u002Fem\u003E). In both structures, the \u003Csub\u003E\n\u003C\u002Fsub\u003E loop where the host protease cleavage site is located in the S2 region is almost perpendicular to the central helix, protruding at the periphery of the S trimer and readily accessible to host proteases. The fusion machineries of HCoV-NL63 and SARS-CoV-2 are almost identical except that the \u003Csub\u003E\n\u003C\u002Fsub\u003E trigger loop of HCoV-NL63 forms a short alpha helix before looping back to connect to the fusion peptide while the corresponding loop of SARS-CoV-2 is long and flexible. The fusion machinery of coronaviruses provides a potential target for broad anti-coronavirus therapeutics development.\u003C\u002Fp\u003E\n\u003Cp class=\"p\"\u003E Further similarities between HCoV-NL63 and SARS-CoV-2 domains are illustrated in \u003Ca class=\"xref fig\" href=\"#fig5\"\u003EFig. 5\u003C\u002Fa\u003E and Fig. S2. Structure-based alignments using TM-align (Zhang and Skolnick, \u003Ca class=\"xref bibr\" href=\"#ref38\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Zhang and Skolnick\u003C\u002Fspan\u003E2005\u003C\u002Fa\u003E) show that structurally, domains A and 0 from HCoV-NL63, and domain A′ from SARS-CoV-2 are very similar, with RMSDs of ~3.5 Å between ~75% aligned residues. These aligned residues however have quite low sequence identities (7.5–10.2%). Regardless, due to such high structure similarity, it is very likely that they evolved from a common ancestor, consistent with the previous hypothesis that domains 0 and A resulted from a gene duplication event of a single domain. Domains B and B′ also have a similar core fold, with RMSD of 4.13 Å, though the receptor-binding motifs look significantly different between the two, even though both bind the receptor ACE2. Domains D and D′ are also structurally similar, though still having a low sequence identity of 6.3%. Domains C\u002FC′ and S2\u002FS2′ are the most similar, with relatively high sequence identities of 25.4% and 37.0%; this high conservation shows that these domains, in particular, may be less prone to mutate and may be targeted by cross-reactive antibodies as reported very recently (Wang \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref29\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Wang, van Haperen, Gutiérrez-Álvarez, Li, Okba, Albulescu and Bosch\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\u003Csection\u003E\u003Cdiv class=\"fig\" data-magellan-destination=\"fig5\" id=\"fig5\"\u003E\n\n\n\u003Cdiv class=\"figure-thumb\"\u003E\u003Cimg src=\"data:image\u002Fgif;base64,R0lGODlhAQABAIAAAMLCwgAAACH5BAAAAAAALAAAAAABAAEAAAICRAEAOw==\" data-src=\"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig5.png?pub-status=live\" class=\"aop-lazy-load-image\" width=\"1254\" height=\"954\" data-original-image=\"\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary:20201206180532142-0446:S2633289220000162:S2633289220000162_fig5.png\" data-zoomable=\"true\"\u003E\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"caption\"\u003E\u003Cp class=\"p\"\u003E \n\u003C\u002Fp\u003E\u003Cp class=\"p\"\u003E\u003Cspan class=\"label\"\u003EFig. 5.\u003C\u002Fspan\u003E Structural comparison of domains in HCoV-NL63 and SARS-CoV-2 spikes. (\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E) Ribbon diagram of the spikes. Each domain is shown in different colors. (\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E) Structure-based alignment of corresponding domains (PDB ID: 6VXX for A′, C′, D′ and S2′), analysed by TM-align (Zhang and Skolnick, \u003Ca class=\"xref bibr\" href=\"#ref38\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Zhang and Skolnick\u003C\u002Fspan\u003E2005\u003C\u002Fa\u003E). For domain B–B′ comparison, PDB ID: 6VW1 was used for domain B′ because it has receptor-binding motif (outlined in dotted ellipse).\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\u003C\u002Fdiv\u003E\u003C\u002Fsection\u003E\n\u003Cp class=\"p\"\u003E The feasibility of solving the near-atomic resolution structure of membrane-anchored S trimer on the purified viral particle opens a straightforward path for follow-up structural studies of coronaviruses with external reagents like receptors, antibodies or drugs. In addition, the single-particle cryo-EM derived structures can be used together with sub-tomogram averages of the S trimer in the virion to understand complex and heterogeneous modes of interactions between S and various external reagents in different biochemical conditions, and the orientation in 3D of S with respect to the viral membrane, and, ultimately, the cell surface. Such a hybrid approach across different imaging protocols will be very useful for the discovery of authentic structural states of molecular components in a pleomorphic virus particle in the context of pathogenicity relevant to human health.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec methods\" data-magellan-destination=\"sec3\" id=\"sec3\"\u003E\n\u003Ch2 class=\"A\"\u003E Methods\u003C\u002Fh2\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec4\" id=\"sec4\"\u003E\n\u003Ch3 class=\"B\"\u003E Cell culture and virus\u003C\u002Fh3\u003E\n\u003Cp class=\"p\"\u003E Vero E6 (ATCC CRL-1586) and MA104 (ATCC CRL-2378.1) cells were maintained at 37°C in a fully humidified atmosphere with 5% CO\u003Csub\u003E2\u003C\u002Fsub\u003E in Dulbecco's Modified Eagle's medium (Invitrogen) and M199 (Gibco) medium respectively. All culture media were supplemented with penicillin and streptomycin and 10% foetal bovine serum (Hyclone). HCoV-NL63 was obtained from BEI Resources, NIAID, NIH: Human Coronavirus, NL63, NR-470.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec5\" id=\"sec5\"\u003E\n\u003Ch3 class=\"B\"\u003E Virus production and purification\u003C\u002Fh3\u003E\n\u003Cp class=\"p\"\u003E Monolayers of Vero E6 or MA-104 cells were infected with HCoV-NL63 at MOI 0.5. Culture supernatants were harvested when clear cytopathic effect developed. After clarification of the supernatants through a 0.45 μm filter, the virus was pelleted down through a 20% sucrose cushion. Virus was then resuspended in virus resuspension buffer (20 mM Tris, pH 8.0, 120 mM NaCl, 1 mM EDTA) before layered onto 2 ml of 60% OptiPrep (Sigma-Aldrich) and spun at 50,000\u003Cem class=\"italic\"\u003Eg\u003C\u002Fem\u003E for 1.5 h using a SW28 rotor. After ultracentrifugation, the supernatants were removed to leave 4 ml above the virus band. The remaining 4 ml supernatant, the virus band and the underlay of 2 ml of 60% OptiPrep were mixed to reach a final concentration of 20% OptiPrep. The mixture was spun at 360,000\u003Cem class=\"italic\"\u003Eg\u003C\u002Fem\u003E for 3.5 h with a NVT65.2 rotor. The virus band was extracted and buffer exchanged to the virus resuspension buffer using an Amicon Ultra-2 Centrifugal Filter Unit with Ultracel-100 membrane (Millipore).\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec6\" id=\"sec6\"\u003E\n\u003Ch3 class=\"B\"\u003E Cryo-EM vitrification, data acquisition, image processing and 3D reconstruction\u003C\u002Fh3\u003E\n\u003Cp class=\"p\"\u003E Three microliters of purified HCoV-NL63 virions (4.5 mg ml\u003Csup class=\"sup\"\u003E−1\u003C\u002Fsup\u003E) were first applied to 300-mesh R2\u002F1 + 2 nm C-film grids (Quantifoil) that had been glow-discharged for 15 s PELCO easiGlow (TED PELLA, INC.). Grids were then front-blotted for 2 s in a 90% humidified chamber and vitrified using the LEICA EM GP automated plunge freezing device. Frozen grids were then stored in liquid nitrogen until imaging. The samples were imaged in a Titan Krios cryo-electron microscope (Thermo Fisher Scientific) operated at 300 kV with GIF energy filter (BioQuantum, Ametek) at a magnification of 64,000× (corresponding to a calibrated sampling of 1.4 Å per pixel). Micrographs were recorded by EPU software (Thermo Fisher Scientific) with a Ametek K3 Summit direct electron detector, where each image was composed of 30 individual frames with an exposure time of 3 s and an exposure rate of 16 electrons per second per Å\u003Csup class=\"sup\"\u003E2\u003C\u002Fsup\u003E. A total of 4,138 movie stacks were collected. All movie stacks were motion-corrected by MotionCor2 (Zheng \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref40\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Zheng, Palovcak, Armache, Verba, Cheng and Agard\u003C\u002Fspan\u003E2017\u003C\u002Fa\u003E). Motion-corrected micrographs were imported into cryoSPARC for image processing. The contrast transfer function (CTF) was determined using the ‘Patch CTF Estimation’ option, and the micrographs with ‘CTF fit <5 Å’ were selected using the ‘Manually Curate Exposures’. Then 157 particles were manually picked and subjected to 2D classification into 10 classes, 3 of which were selected as the template for the auto-particle picking, yielding 944,822 particles. Several rounds of 2D classification were then performed to remove the poor 2D class averages, and 300,236 particles were obtained. The initial map was built using ab-initio reconstruction without any symmetry applied. Next, three rounds of heterogeneous refinement were performed to further remove bad particles. The final 3D non-uniform refinement was performed using the selected 82,030 particles with or without C3 symmetry applied, and a 3.4-Å map and a 3.7-Å map were obtained, respectively. Resolution for the final maps was estimated with the 0.143 criterion of the Fourier shell correlation curve. Resolution map was calculated in cryoSPARC using the ‘Local Resolution Estimation’ option. The figures were prepared using UCSF Chimera (Pettersen \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref18\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pettersen, Goddard, Huang, Couch, Greenblatt, Meng and Ferrin\u003C\u002Fspan\u003E2004\u003C\u002Fa\u003E) or UCSF Chimera X (Goddard \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref9\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Goddard, Huang, Meng, Pettersen, Couch, Morris and Ferrin\u003C\u002Fspan\u003E2017\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec7\" id=\"sec7\"\u003E\n\u003Ch3 class=\"B\"\u003E Model building\u003C\u002Fh3\u003E\n\u003Cp class=\"p\"\u003E One protomer was first computationally extracted (Pintilie \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref20\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pintilie, Zhang, Goddard, Chiu and Gossard\u003C\u002Fspan\u003E2010\u003C\u002Fa\u003E) from the 3.4-Å cryo-EM map of the spike protein expressed on HCoV-NL63 coronavirus. The PDB coordinates of biochemically purified HCoV-NL63 spike protein (PDB ID: 5SZS) were then fitted into the computationally extracted S protomer map. Residues 883–889 and 993–1,000 that were previously unresolved were also modeled using SWISS-MODEL (Waterhouse \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref35\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Waterhouse, Bertoni, Bienert, Studer, Tauriello, Gumienny and Schwede\u003C\u002Fspan\u003E2018\u003C\u002Fa\u003E). The resultant model was refined using phenix.real_space_refine (Adams \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref1\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Adams, Afonine, Bunkóczi, Chen, Davis, Echols and Zwart\u003C\u002Fspan\u003E2010\u003C\u002Fa\u003E) and manually optimized with Coot (Emsley \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref8\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Emsley, Lohkamp, Scott and Cowtan\u003C\u002Fspan\u003E2010\u003C\u002Fa\u003E). The atomic model of protomer was then fitted into the cryo-EM density of the other two protomers in the HCoV-NL63 spike trimer using Chimera (Pettersen \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref18\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pettersen, Goddard, Huang, Couch, Greenblatt, Meng and Ferrin\u003C\u002Fspan\u003E2004\u003C\u002Fa\u003E), followed by the optimization of the whole model with phenix.real_space_refine. The glycans in the PDB ID: 5SZS model were also used in our model for refinement. The final model was evaluated by MolProbity (Chen \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref5\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Chen, Arendall, Headd, Keedy, Immormino, Kapral and Richardson\u003C\u002Fspan\u003E2009\u003C\u002Fa\u003E) and Q-scores (Pintilie \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref19\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pintilie, Zhang, Su, Li, Schmid and Chiu\u003C\u002Fspan\u003E2020\u003C\u002Fa\u003E). The match between the map and the model was evaluated by the correlation for each residue (\u003Ca class=\"xref fig\" href=\"#fig2\"\u003EFig. 2\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E). For assessing the resolvability of the map density, the Q score was calculated for each residue with the final model (\u003Ca class=\"xref fig\" href=\"#fig2\"\u003EFig. 2\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Eb\u003C\u002Fem\u003E). The Q-scores were also computed for glycan residues (\u003Ca class=\"xref fig\" href=\"#fig3\"\u003EFig. 3\u003C\u002Fa\u003E\n\u003Cem class=\"italic\"\u003Ea\u003C\u002Fem\u003E). Statistics of map reconstruction and model optimization are shown in Table S1. To identify extra glycosylation sites beyond what was previously known from the S ectodomain map (EMD-8331), we computed the difference map between our map and the previous map of the S ectodomain. When we fitted our map to this previous map using Chimera Fit in Map, it was apparent that the maps have different scales. Thus, the step size in our map was adjusted until the maximum cross-correlation between the two maps was obtained, at which point the maps also visually overlapped better. Density values in the two maps were then normalized to an average of 0 and standard deviation of 1. The difference map was then computed at each voxel with the rescaled maps. Extra glycan densities seen in this difference map were extracted using Segger (Pintilie \u003Cem class=\"italic\"\u003Eet\u003C\u002Fem\u003E \u003Cem class=\"italic\"\u003Eal\u003C\u002Fem\u003E., \u003Ca class=\"xref bibr\" href=\"#ref20\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pintilie, Zhang, Goddard, Chiu and Gossard\u003C\u002Fspan\u003E2010\u003C\u002Fa\u003E) for further visualization. All figures were prepared using Chimera (Pettersen \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref18\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Pettersen, Goddard, Huang, Couch, Greenblatt, Meng and Ferrin\u003C\u002Fspan\u003E2004\u003C\u002Fa\u003E) or Chimera X (Goddard \u003Cem class=\"italic\"\u003Eet al.,\u003C\u002Fem\u003E \u003Ca class=\"xref bibr\" href=\"#ref9\"\u003E\u003Cspan class=\"show-for-sr\"\u003EReference Goddard, Huang, Meng, Pettersen, Couch, Morris and Ferrin\u003C\u002Fspan\u003E2017\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003C\u002Fdiv\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"back\"\u003E\n\u003Cdiv class=\"ack\"\u003E\n\u003Ch2 class=\"A\"\u003E Acknowledgements\u003C\u002Fh2\u003E\n\u003Cp class=\"p\"\u003E We thank Drs. Corey Hecksel and Patrick Mitchell for expert maintenance of Stanford-SLAC Cryo-EM Centre and the SLAC National Accelerator Laboratory for supporting conduct of these studies during a university-wide pandemic shutdown. We also thank Dr. Andriy Kryshtafovych for help with structure-based alignment analysis. This work was supported by the National Institutes of Health grants (P41GM103832, R01AI148382, P01AI120943, R01GM079429, U24GM129564 to W.C.); DOE Office of Science through the National Virtual Biotechnology Laboratory, a consortium of DOE national laboratories focused on response to COVID-19, with funding provided by the Coronavirus CARES Act.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec8\" id=\"sec8\"\u003E\n\u003Ch2 class=\"A\"\u003E Conflicts of Interests\u003C\u002Fh2\u003E\n\u003Cp class=\"p\"\u003E All authors declare no competing interest.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec9\" id=\"sec9\"\u003E\n\u003Ch2 class=\"A\"\u003E Authorship Contributions\u003C\u002Fh2\u003E\n\u003Cp class=\"p\"\u003E W.C. and G.S. supervised the study. J.J. prepared the sample. D.C. performed cryo-EM sample preparation. K.Z. and D.C. collected cryo-EM data. K.Z. performed cryo-EM image processing and structure determination; S.L. and K.Z. built and refined the model; K.Z., S.L., G.P., D.C., M.F.S, J.J., and W.C. analysed data. K.Z., S.L., and G.P prepared the figures. K.Z., S.L., D.C., J.J, and W.C. wrote the manuscript with input from all other authors.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec10\" id=\"sec10\"\u003E\n\u003Ch2 class=\"A\"\u003E Data Deposition\u003C\u002Fh2\u003E\n\u003Cp class=\"p\"\u003E Cryo-EM maps of the HCoV-NL63 Spike protein with its associated atomic model have been deposited in the wwPDB OneDep System under EMD accession code EMD-22889 and PDB ID code 7KIP.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec20\" id=\"sec20\"\u003E\n\u003Ch2 class=\"A\"\u003E Open Peer Review\u003C\u002Fh2\u003E\n\u003Cp class=\"p\"\u003E To view the open peer review materials for this article, please visit \u003Ca class=\"uri\" href=\"http:\u002F\u002Fdoi.org\u002F10.1017\u002Fqrd.2020.16\"\u003Ehttp:\u002F\u002Fdoi.org\u002F10.1017\u002Fqrd.2020.16\u003C\u002Fa\u003E.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\u003Cdiv class=\"sec\" data-magellan-destination=\"sec11\" id=\"sec11\"\u003E\n\u003Ch2 class=\"A\"\u003E Supplementary Materials\u003C\u002Fh2\u003E\n\u003Cp class=\"p\"\u003E To view supplementary material for this article, please visit \u003Ca class=\"uri\" href=\"http:\u002F\u002Fdx.doi.org\u002F10.1017\u002Fqrd.2020.16\"\u003Ehttp:\u002F\u002Fdx.doi.org\u002F10.1017\u002Fqrd.2020.16\u003C\u002Fa\u003E.\u003C\u002Fp\u003E\n\u003C\u002Fdiv\u003E\n\n\u003C\u002Fdiv\u003E\n\n\n\n\n\n\u003C\u002Fdiv\u003E",tableOfContent:[{level:i,current:a,title:"\u003Cdiv class=\"toc-title\"\u003EIntroduction\u003C\u002Fdiv\u003E",url:"sec1"},{level:i,current:a,title:"\u003Cdiv class=\"toc-title\"\u003EResults and discussion\u003C\u002Fdiv\u003E",url:"sec2"},{level:i,current:a,title:"\u003Cdiv class=\"toc-title\"\u003EMethods\u003C\u002Fdiv\u003E",url:"sec3"},{level:i,current:a,title:"\u003Cdiv class=\"toc-title\"\u003EConflicts of Interests\u003C\u002Fdiv\u003E",url:"sec8"},{level:i,current:a,title:"\u003Cdiv class=\"toc-title\"\u003EAuthorship Contributions\u003C\u002Fdiv\u003E",url:"sec9"},{level:i,current:a,title:"\u003Cdiv class=\"toc-title\"\u003EData Deposition\u003C\u002Fdiv\u003E",url:"sec10"},{level:i,current:a,title:"\u003Cdiv class=\"toc-title\"\u003EOpen Peer Review\u003C\u002Fdiv\u003E",url:"sec20"},{level:i,current:a,title:"\u003Cdiv class=\"toc-title\"\u003ESupplementary Materials\u003C\u002Fdiv\u003E",url:"sec11"}],footnotes:[],fulltextNotes:[],references:[{id:"r1",displayNumber:b,existInContent:a,content:"\u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EAdams\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EPD\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EAfonine\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EPV\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EBunkóczi\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EG\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EChen\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EVB\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EDavis\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EIW\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EEchols\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EN\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E … \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EZwart\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EPH\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E (\u003Cspan class=\"year\"\u003E2010\u003C\u002Fspan\u003E) \u003Cspan class=\"article-title\"\u003EPHENIX: a 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class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EBelouzard\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ES\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EChu\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EVC\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EWhittaker\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EGR\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E (\u003Cspan class=\"year\"\u003E2009\u003C\u002Fspan\u003E) \u003Cspan class=\"article-title\"\u003EActivation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites\u003C\u002Fspan\u003E. \u003Cspan class=\"source\"\u003EProceedings of the National Academy of Sciences\u003C\u002Fspan\u003E \u003Cspan class=\"volume\"\u003E106\u003C\u002Fspan\u003E(\u003Cspan 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class=\"surname\"\u003EBosch\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EBJ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003Evan der Zee\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ER\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003Ede Haan\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ECAM\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ERottier\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EPJM\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E (\u003Cspan class=\"year\"\u003E2003\u003C\u002Fspan\u003E) \u003Cspan class=\"article-title\"\u003EThe Coronavirus Spike Protein Is a Class I Virus Fusion Protein: Structural and Functional Characterization of the Fusion Core Complex\u003C\u002Fspan\u003E. \u003Cspan 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Scholar\u003C\u002Fa\u003E",item:[{googleScholarLink:"https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=The+Coronavirus+Spike+Protein+Is+a+Class+I+Virus+Fusion+Protein%3A+Structural+and+Functional+Characterization+of+the+Fusion+Core+Complex&author=Bosch+BJ&author=van+der+Zee+R&author=de+Haan+CAM&author=Rottier+PJM&publication+year=2003&journal=Journal+of+Virology&volume=77&doi=10.1128%2FJVI.77.16.8801-8811.2003&pages=8801-8811",openUrlParams:{genre:f,atitle:ad,jtitle:k,title:k,volume:"77",artnum:"5fcd1d7006eec50001661f14",spage:"8801",epage:"8811",date:"2003",sid:e,aulast:b,aufirst:b,doi:ae,au:b},innerRefId:"ref3",title:ad,doi:ae,crossRefLink:"https:\u002F\u002Fdx.doi.org\u002F10.1128\u002FJVI.77.16.8801-8811.2003",pubMedLink:b}]},{id:"r4",displayNumber:b,existInContent:a,content:"\u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ECasalino\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EL\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, 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class=\"surname\"\u003ESchmid\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EMF\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EHecksel\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ECW\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ERochat\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ERH\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EBhella\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ED\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EChiu\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EW\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ERixon\u003C\u002Fspan\u003E, 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href=https:\u002F\u002Fwww.ncbi.nlm.nih.gov\u002Fpubmed\u002F23055933\u003EPubMed\u003C\u002Fa\u003E",item:[{googleScholarLink:"https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=A+Tail-like+Assembly+at+the+Portal+Vertex+in+Intact+Herpes+Simplex+Type-1+Virions&author=Schmid+MF&author=Hecksel+CW&author=Rochat+RH&author=Bhella+D&author=Chiu+W&author=Rixon+FJ&publication+year=2012&journal=PLoS+Pathogens&volume=8&doi=10.1371%2Fjournal.ppat.1002961",openUrlParams:{genre:f,atitle:aZ,jtitle:a_,title:a_,volume:aD,artnum:"5fcd1d7006eec50001661f27",spage:g,epage:g,date:"2012",sid:e,aulast:b,aufirst:b,doi:a$,au:b},innerRefId:"ref22",title:aZ,pubMedId:"23055933",doi:a$,crossRefLink:"https:\u002F\u002Fdx.doi.org\u002F10.1371\u002Fjournal.ppat.1002961",pubMedLink:"https:\u002F\u002Fwww.ncbi.nlm.nih.gov\u002Fpubmed\u002F23055933"}]},{id:"r23",displayNumber:b,existInContent:a,content:"\u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ESong\u003C\u002Fspan\u003E, 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class=\"surname\"\u003EVigerust\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EDJ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EShepherd\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EVL\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E (\u003Cspan class=\"year\"\u003E2007\u003C\u002Fspan\u003E) \u003Cspan class=\"article-title\"\u003EVirus glycosylation: role in virulence and immune interactions\u003C\u002Fspan\u003E. \u003Cspan class=\"source\"\u003ETrends in Microbiology\u003C\u002Fspan\u003E \u003Cspan class=\"volume\"\u003E15\u003C\u002Fspan\u003E(\u003Cspan class=\"issue\"\u003E5\u003C\u002Fspan\u003E), \u003Cspan class=\"fpage\"\u003E211\u003C\u002Fspan\u003E–\u003Cspan class=\"lpage\"\u003E218\u003C\u002Fspan\u003E. doi:\u003Cspan class=\"pub-id doi\"\u003E10.1016\u002Fj.tim.2007.03.003\u003C\u002Fspan\u003E\u003Ca class='ref-link' target='_blank' aria-label='CrossRef link for Virus 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class=\"given-names\"\u003EAC\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ETortorici\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EMA\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EFrenz\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EB\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ESnijder\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EJ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ELi\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EW\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ERey\u003C\u002Fspan\u003E, \u003Cspan 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class=\"surname\"\u003EWalls\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EAC\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EPark\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EYJ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ETortorici\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EMA\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EWall\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EA\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EMcGuire\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EAT\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EVeesler\u003C\u002Fspan\u003E, 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Isolation of cross-reactive monoclonal antibodies against divergent human coronaviruses that delineate a conserved and vulnerable site on the spike protein. doi:10.1101\u002F2020.10.20.346916",doi:"10.1101\u002F2020.10.20.346916",crossRefLink:"https:\u002F\u002Fdx.doi.org\u002F10.1101\u002F2020.10.20.346916",pubMedLink:b}]},{id:"r30",displayNumber:b,existInContent:a,content:"\u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EWang\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ELF\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EShi\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EZ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EZhang\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ES\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan 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class=\"surname\"\u003EZhang\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EY\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ESkolnick\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EJ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E (\u003Cspan class=\"year\"\u003E2005\u003C\u002Fspan\u003E) \u003Cspan class=\"article-title\"\u003ETM-align: a protein structure alignment algorithm based on the TM-score\u003C\u002Fspan\u003E. \u003Cspan class=\"source\"\u003ENucleic Acids Research\u003C\u002Fspan\u003E \u003Cspan class=\"volume\"\u003E33\u003C\u002Fspan\u003E(\u003Cspan class=\"issue\"\u003E7\u003C\u002Fspan\u003E), \u003Cspan class=\"fpage\"\u003E2302\u003C\u002Fspan\u003E–\u003Cspan class=\"lpage\"\u003E2309\u003C\u002Fspan\u003E. doi:\u003Cspan class=\"pub-id doi\"\u003E10.1093\u002Fnar\u002Fgki524\u003C\u002Fspan\u003E\u003Ca class='ref-link' target='_blank' aria-label='CrossRef link for TM-align: a protein structure alignment algorithm based on the TM-score' href=https:\u002F\u002Fdx.doi.org\u002F10.1093\u002Fnar\u002Fgki524\u003ECrossRef\u003C\u002Fa\u003E\u003Ca class='ref-link' target='_blank' aria-label='Google Scholar link for TM-align: a protein structure alignment algorithm based on the TM-score' href=https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=TM-align%3A+a+protein+structure+alignment+algorithm+based+on+the+TM-score&author=Zhang+Y&author=Skolnick+J&publication+year=2005&journal=Nucleic+Acids+Research&volume=33&doi=10.1093%2Fnar%2Fgki524&pages=2302-2309\u003EGoogle Scholar\u003C\u002Fa\u003E\u003Ca class='ref-link' target='_blank' aria-label='PubMed link for TM-align: a protein structure alignment algorithm based on the TM-score' href=https:\u002F\u002Fwww.ncbi.nlm.nih.gov\u002Fpubmed\u002F15849316\u003EPubMed\u003C\u002Fa\u003E",item:[{googleScholarLink:"https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=TM-align%3A+a+protein+structure+alignment+algorithm+based+on+the+TM-score&author=Zhang+Y&author=Skolnick+J&publication+year=2005&journal=Nucleic+Acids+Research&volume=33&doi=10.1093%2Fnar%2Fgki524&pages=2302-2309",openUrlParams:{genre:f,atitle:bM,jtitle:w,title:w,volume:"33",artnum:"5fcd1d7006eec50001661f37",spage:"2302",epage:"2309",date:al,sid:e,aulast:b,aufirst:b,doi:bN,au:b},innerRefId:"ref38",title:bM,pubMedId:"15849316",doi:bN,crossRefLink:"https:\u002F\u002Fdx.doi.org\u002F10.1093\u002Fnar\u002Fgki524",pubMedLink:"https:\u002F\u002Fwww.ncbi.nlm.nih.gov\u002Fpubmed\u002F15849316"}]},{id:"r39",displayNumber:b,existInContent:a,content:"\u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EZheng\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EQ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EDeng\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EY\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ELiu\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EJ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003Evan der Hoek\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EL\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EBerkhout\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EB\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ELu\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EM\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E (\u003Cspan class=\"year\"\u003E2006\u003C\u002Fspan\u003E) \u003Cspan class=\"article-title\"\u003ECore Structure of S2 from the Human Coronavirus NL63 Spike Glycoprotein†,‡\u003C\u002Fspan\u003E. \u003Cspan class=\"source\"\u003EBiochemistry\u003C\u002Fspan\u003E \u003Cspan class=\"volume\"\u003E45\u003C\u002Fspan\u003E(\u003Cspan class=\"issue\"\u003E51\u003C\u002Fspan\u003E), \u003Cspan class=\"fpage\"\u003E15205\u003C\u002Fspan\u003E–\u003Cspan class=\"lpage\"\u003E15215\u003C\u002Fspan\u003E. doi:\u003Cspan class=\"pub-id doi\"\u003E10.1021\u002Fbi061686w\u003C\u002Fspan\u003E\u003Ca class='ref-link' target='_blank' aria-label='CrossRef link for Core Structure of S2 from the Human Coronavirus NL63 Spike Glycoprotein†,‡' href=https:\u002F\u002Fdx.doi.org\u002F10.1021\u002Fbi061686w\u003ECrossRef\u003C\u002Fa\u003E\u003Ca class='ref-link' target='_blank' aria-label='Google Scholar link for Core Structure of S2 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Scholar\u003C\u002Fa\u003E",item:[{googleScholarLink:"https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=Core+Structure+of+S2+from+the+Human+Coronavirus+NL63+Spike+Glycoprotein%E2%80%A0%2C%E2%80%A1&author=Zheng+Q&author=Deng+Y&author=Liu+J&author=van+der+Hoek+L&author=Berkhout+B&author=Lu+M&publication+year=2006&journal=Biochemistry&volume=45&doi=10.1021%2Fbi061686w&pages=15205-15215",openUrlParams:{genre:f,atitle:bO,jtitle:bP,title:bP,volume:"45",artnum:"5fcd1d7006eec50001661f38",spage:"15205",epage:"15215",date:G,sid:e,aulast:b,aufirst:b,doi:bQ,au:b},innerRefId:"ref39",title:bO,doi:bQ,crossRefLink:"https:\u002F\u002Fdx.doi.org\u002F10.1021\u002Fbi061686w",pubMedLink:b}]},{id:"r40",displayNumber:b,existInContent:a,content:"\u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EZheng\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003ESQ\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EPalovcak\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EE\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EArmache\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EJP\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EVerba\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EKA\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003ECheng\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EY\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EAgard\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EDA\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E (\u003Cspan class=\"year\"\u003E2017\u003C\u002Fspan\u003E) \u003Cspan class=\"article-title\"\u003EMotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy\u003C\u002Fspan\u003E. \u003Cspan class=\"source\"\u003ENature Methods\u003C\u002Fspan\u003E \u003Cspan class=\"volume\"\u003E14\u003C\u002Fspan\u003E(\u003Cspan class=\"issue\"\u003E4\u003C\u002Fspan\u003E), \u003Cspan class=\"fpage\"\u003E331\u003C\u002Fspan\u003E–\u003Cspan class=\"lpage\"\u003E332\u003C\u002Fspan\u003E. doi:\u003Cspan class=\"pub-id doi\"\u003E10.1038\u002Fnmeth.4193\u003C\u002Fspan\u003E\u003Ca class='ref-link' target='_blank' aria-label='CrossRef link for MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy' href=https:\u002F\u002Fdx.doi.org\u002F10.1038\u002Fnmeth.4193\u003ECrossRef\u003C\u002Fa\u003E\u003Ca class='ref-link' target='_blank' aria-label='Google Scholar link for MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy' href=https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=MotionCor2%3A+anisotropic+correction+of+beam-induced+motion+for+improved+cryo-electron+microscopy&author=Zheng+SQ&author=Palovcak+E&author=Armache+JP&author=Verba+KA&author=Cheng+Y&author=Agard+DA&publication+year=2017&journal=Nature+Methods&volume=14&doi=10.1038%2Fnmeth.4193&pages=331-332\u003EGoogle Scholar\u003C\u002Fa\u003E\u003Ca class='ref-link' target='_blank' aria-label='PubMed link for MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy' href=https:\u002F\u002Fwww.ncbi.nlm.nih.gov\u002Fpubmed\u002F28250466\u003EPubMed\u003C\u002Fa\u003E",item:[{googleScholarLink:"https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=MotionCor2%3A+anisotropic+correction+of+beam-induced+motion+for+improved+cryo-electron+microscopy&author=Zheng+SQ&author=Palovcak+E&author=Armache+JP&author=Verba+KA&author=Cheng+Y&author=Agard+DA&publication+year=2017&journal=Nature+Methods&volume=14&doi=10.1038%2Fnmeth.4193&pages=331-332",openUrlParams:{genre:f,atitle:bR,jtitle:u,title:u,volume:E,artnum:"5fcd1d7006eec50001661f39",spage:"331",epage:"332",date:n,sid:e,aulast:b,aufirst:b,doi:bS,au:b},innerRefId:"ref40",title:bR,pubMedId:"28250466",doi:bS,crossRefLink:"https:\u002F\u002Fdx.doi.org\u002F10.1038\u002Fnmeth.4193",pubMedLink:"https:\u002F\u002Fwww.ncbi.nlm.nih.gov\u002Fpubmed\u002F28250466"}]},{id:"r41",displayNumber:b,existInContent:a,content:"\u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EZhou\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EP\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EYang\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EXL\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EWang\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EXG\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EHu\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EB\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EZhang\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EL\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E, \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EZhang\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EW\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E and \u003Cspan class=\"string-name\"\u003E\u003Cspan class=\"surname\"\u003EShi\u003C\u002Fspan\u003E, \u003Cspan class=\"given-names\"\u003EZL\u003C\u002Fspan\u003E\u003C\u002Fspan\u003E (\u003Cspan class=\"year\"\u003E2020\u003C\u002Fspan\u003E) \u003Cspan class=\"article-title\"\u003EA pneumonia outbreak associated with a new coronavirus of probable bat origin\u003C\u002Fspan\u003E. \u003Cspan class=\"source\"\u003ENature\u003C\u002Fspan\u003E \u003Cspan class=\"volume\"\u003E579\u003C\u002Fspan\u003E(\u003Cspan class=\"issue\"\u003E7798\u003C\u002Fspan\u003E), \u003Cspan class=\"fpage\"\u003E270\u003C\u002Fspan\u003E–\u003Cspan class=\"lpage\"\u003E273\u003C\u002Fspan\u003E. doi:\u003Cspan class=\"pub-id doi\"\u003E10.1038\u002Fs41586-020-2012-7\u003C\u002Fspan\u003E\u003Ca class='ref-link' target='_blank' aria-label='CrossRef link for A pneumonia outbreak associated with a new coronavirus of probable bat origin' href=https:\u002F\u002Fdx.doi.org\u002F10.1038\u002Fs41586-020-2012-7\u003ECrossRef\u003C\u002Fa\u003E\u003Ca class='ref-link' target='_blank' aria-label='Google Scholar link for A pneumonia outbreak associated with a new coronavirus of probable bat origin' href=https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=A+pneumonia+outbreak+associated+with+a+new+coronavirus+of+probable+bat+origin&author=Zhou+P&author=Yang+XL&author=Wang+XG&author=Hu+B&author=Zhang+L&author=Zhang+W&author=Shi+ZL&publication+year=2020&journal=Nature&volume=579&doi=10.1038%2Fs41586-020-2012-7&pages=270-273\u003EGoogle Scholar\u003C\u002Fa\u003E\u003Ca class='ref-link' target='_blank' aria-label='PubMed link for A pneumonia outbreak associated with a new coronavirus of probable bat origin' href=https:\u002F\u002Fwww.ncbi.nlm.nih.gov\u002Fpubmed\u002F32015507\u003EPubMed\u003C\u002Fa\u003E",item:[{googleScholarLink:"https:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?title=A+pneumonia+outbreak+associated+with+a+new+coronavirus+of+probable+bat+origin&author=Zhou+P&author=Yang+XL&author=Wang+XG&author=Hu+B&author=Zhang+L&author=Zhang+W&author=Shi+ZL&publication+year=2020&journal=Nature&volume=579&doi=10.1038%2Fs41586-020-2012-7&pages=270-273",openUrlParams:{genre:f,atitle:bT,jtitle:bU,title:bU,volume:"579",artnum:"5fcd1d7006eec50001661f3a",spage:"270",epage:"273",date:h,sid:e,aulast:b,aufirst:b,doi:bV,au:b},innerRefId:"ref41",title:bT,pubMedId:"32015507",doi:bV,crossRefLink:"https:\u002F\u002Fdx.doi.org\u002F10.1038\u002Fs41586-020-2012-7",pubMedLink:"https:\u002F\u002Fwww.ncbi.nlm.nih.gov\u002Fpubmed\u002F32015507"}]}],figures:[{contentId:"fig1",label:"Fig. 1.",description:"\u003Cspan class=\"p\"\u003ESingle-particle cryo-EM analysis of \u003Cspan class=\"italic\"\u003Ein-situ\u003C\u002Fspan\u003E structure of the HCoV-NL63 coronavirus spike glycoprotein. (\u003Cspan class=\"italic\"\u003Ea\u003C\u002Fspan\u003E) Representative motion-corrected cryo-EM micrograph. (\u003Cspan class=\"italic\"\u003Eb\u003C\u002Fspan\u003E) Reference-free 2D class averages of computationally extracted spikes. (\u003Cspan class=\"italic\"\u003Ec-d\u003C\u002Fspan\u003E) Reconstructed 3-fold symmetry-imposed cryo-EM map of the spike in the top and side views without (c) and with (\u003Cspan class=\"italic\"\u003Ed\u003C\u002Fspan\u003E) glycans shown. (\u003Cspan class=\"italic\"\u003Ee\u003C\u002Fspan\u003E) Resolution variation maps for 3D reconstruction. Left, whole map view; middle, slice view; right, whole map view at a lower threshold.\u003C\u002Fspan\u003E",thumbnailSrc:"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary-alt:20201206180614-42244-mediumThumb-S2633289220000162_fig1.jpg",enlargedSrc:"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary-alt:20201206180614-52417-optimisedImage-S2633289220000162_fig1.jpg",attrib:[]},{contentId:"fig2",label:"Fig. 2.",description:"\u003Cspan class=\"p\"\u003EModel validation of the HCoV-NL63 coronavirus spike glycoprotein protomer. (\u003Cspan class=\"italic\"\u003Ea\u003C\u002Fspan\u003E) Per-residue cross-correlation coefficient between the model and 3.4-Å map. (\u003Cspan class=\"italic\"\u003Eb\u003C\u002Fspan\u003E) Q-score for each amino acid residue in the model and 3.4-Å map; the orange line represents the expected Q-score of 0.52 at 3.4-Å resolution based on the correlation between Q-scores and map resolutions (Pintilie \u003Cspan class=\"italic\"\u003Eet al.,\u003C\u002Fspan\u003E2020). (\u003Cspan class=\"italic\"\u003Ec–e\u003C\u002Fspan\u003E) Examples of different regions of the map with different resolvability: (\u003Cspan class=\"italic\"\u003Ec\u003C\u002Fspan\u003E) well-resolved, (\u003Cspan class=\"italic\"\u003Ed\u003C\u002Fspan\u003E) poorly-resolved; (\u003Cspan class=\"italic\"\u003Ee\u003C\u002Fspan\u003E) residues not resolved in the previous biochemically purified HCoV-NL63 spike protein structure (PDB ID: 5SZS) and thus their model built \u003Cspan class=\"italic\"\u003Ede novo\u003C\u002Fspan\u003E here. The model is shown as ribbon, with residue Q-scores annotated in colors. The higher Q-score indicates better resolvability.\u003C\u002Fspan\u003E",thumbnailSrc:bW,enlargedSrc:bW,attrib:[]},{contentId:"fig3",label:"Fig. 3.",description:"\u003Cspan class=\"p\"\u003EResolvability of glycans. (\u003Cspan class=\"italic\"\u003Ea\u003C\u002Fspan\u003E) Q-scores analysis for each glycan residue (# starting from 1401) in model and map; the orange line represents the expected Q-score of 0.52 at 3.4-Å resolution based on the correlation between Q-scores and map resolutions of amino acid residues (Pintilie \u003Cspan class=\"italic\"\u003Eet al.,\u003C\u002Fspan\u003E2020). (\u003Cspan class=\"italic\"\u003Eb\u003C\u002Fspan\u003E) Highlights on several glycans. Green: Positive difference density between our and previous map (EMD-8331) suggesting extra glycan densities; Yellow: glycan densities found both in our map and in the previous study. The glycan models were derived from (PDB ID: 5SZS).\u003C\u002Fspan\u003E",thumbnailSrc:"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary-alt:20201206180614-68956-mediumThumb-S2633289220000162_fig3.jpg",enlargedSrc:"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary-alt:20201206180614-85383-optimisedImage-S2633289220000162_fig3.jpg",attrib:[]},{contentId:"tab1",label:"Table 1.",description:"\u003Cspan class=\"p\"\u003ENewly identified glycosylation sites in this study.\u003C\u002Fspan\u003E",thumbnailSrc:bX,enlargedSrc:bX,attrib:[]},{contentId:"fig4",label:"Fig. 4.",description:"\u003Cspan class=\"p\"\u003EStructure comparison between HCoV-NL63 and SARS-CoV-2 spike. (\u003Cspan class=\"italic\"\u003Ea\u003C\u002Fspan\u003E) Comparison of our structure with SARS-CoV-2 spike in closed state (PDB ID: 6VXX) in two different views. Different domains and the linker (Lk) between domains A and B are indicated in different colors. (\u003Cspan class=\"italic\"\u003Eb\u003C\u002Fspan\u003E) Zoom-in view to show the interactions between domain A and domain B in the HCoV-NL63 spike protein. (\u003Cspan class=\"italic\"\u003Ec\u003C\u002Fspan\u003E) Extracted densities of the S2 fusion machinery region with models fitted.\u003C\u002Fspan\u003E",thumbnailSrc:"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary-alt:20201206180614-98554-mediumThumb-S2633289220000162_fig4.jpg",enlargedSrc:"https:\u002F\u002Fstatic.cambridge.org\u002Fbinary\u002Fversion\u002Fid\u002Furn:cambridge.org:id:binary-alt:20201206180614-64037-optimisedImage-S2633289220000162_fig4.jpg",attrib:[]},{contentId:"fig5",label:"Fig. 5.",description:"\u003Cspan class=\"p\"\u003EStructural comparison of domains in HCoV-NL63 and SARS-CoV-2 spikes. (\u003Cspan class=\"italic\"\u003Ea\u003C\u002Fspan\u003E) Ribbon diagram of the spikes. Each domain is shown in different colors. (\u003Cspan class=\"italic\"\u003Eb\u003C\u002Fspan\u003E) Structure-based alignment of corresponding domains (PDB ID: 6VXX for A′, C′, D′ and S2′), analysed by TM-align (Zhang and Skolnick, 2005). For domain B–B′ comparison, PDB ID: 6VW1 was used for domain B′ because it has receptor-binding motif (outlined in dotted ellipse).\u003C\u002Fspan\u003E",thumbnailSrc:bY,enlargedSrc:bY,attrib:[]}]},pdf:{standardResolution:{fileUrl:"\u002Fcore\u002Fservices\u002Faop-cambridge-core\u002Fcontent\u002Fview\u002F6566DF036E29EAE203048C708B48B9EB\u002FS2633289220000162a.pdf\u002Fa-34-a-cryo-electron-microscopy-structure-of-the-human-coronavirus-spike-trimer-computationally-derived-from-vitrified-nl63-virus-particles.pdf",fileSizeInMb:bZ,articleTitle:y,slugTitle:"a-34-a-cryo-electron-microscopy-structure-of-the-human-coronavirus-spike-trimer-computationally-derived-from-vitrified-nl63-virus-particles"},highResolution:g,media:g},classification:[],supplementaryMaterials:[{title:"Zhang et al. supplementary material",description:"\u003Cp\u003EZhang et al. supplementary material\u003C\u002Fp\u003E",contentType:b_,objectType:"application\u002Fpdf",alternatives:[],downloadUrl:"https:\u002F\u002Fstatic.cambridge.org\u002Fcontent\u002Fid\u002Furn:cambridge.org:id:article:S2633289220000162\u002Fresource\u002Fname\u002FS2633289220000162sup001.pdf",size:"1.5 MB"}],relations:{corrections:[],correctionsOriginals:[],retractions:[],retractionsOriginals:[],addendums:[],addendumsOriginals:[],hasAnyRelations:a,hasAnyOriginalArticle:a},settings:{hasAccess:c,isOpenAccess:c,displayRightsLink:c,shouldDisplayCrossMark:a,shouldDisplayNasaAds:a,suppressPdf:a,isShareable:c,isAnnotationsEnabled:a,disableArticleCommentary:a,displayArticleCommentaryAsDiscussionLinks:a,isCommentsEnabled:a,hasContent:c,shouldDisplaySubmitContent:a,isResearchDirections:a,isQuestionCollection:a,isMathjaxEnabled:a},citationCount:8,openUrlParams:"?genre=article&atitle=A%203.4-%C3%85%20cryo-electron%20microscopy%20structure%20of%20the%20human%20coronavirus%20spike%20trimer%20computationally%20derived%20from%20vitrified%20NL63%20virus%20particles&jtitle=QRB%20Discovery&title=QRB%20Discovery&date=2020&volume=1&artnum=e11&sid=https%3A%2F%2Fwww.cambridge.org%2Fcore&aulast=Zhang&aufirst=Kaiming&doi=10.1017\u002Fqrd.2020.16",ecommerceProducts:{digitalSku:"S2633289220000162",paperBackSku:g,hardBackSku:g},peerReviews:{doi:{url:Q,value:R},editors:[],reviews:[{title:"\u003Cdiv class=\"article-title\"\u003EReview: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R0\u002FPR1\u003C\u002Fdiv\u003E",productId:"DAA24F6BB10FBD32F37B29967E845BC2",position:i,sections:[],conflictOfInterests:b$,contributor:{givenNames:"Elena",surname:"Orlova",nameStyle:g,affiliations:[{text:"Biological sciences, Birkbeck University of London, United Kingdom"}],isCorresponding:a,notes:g,isAnonymous:a,fullName:"Elena Orlova",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Elena%20Orlova&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0003-3371-415X"},comments:"\u003Cp\u003E\u003Cspan class=\"italic\"\u003EComments to Author\u003C\u002Fspan\u003E: The manuscript \"A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles\" by Zhang and co-authors reports a structure of the human coronavirus NL63 (HCoV-NL63) spike. This impactful study provides analysis of domain localisations within the HCoV-NL63 S (spike) trimer without chemical fixative in its prefusion conformation. Cryo-EM has been used in this structural study. The results of the research reported in the MS have several major outcomes. Firstly, the authors have proved the faithfulness of structural organisation of the NL63 spike obtained.Two structures (one from vitrified complete virus and another obtained using an expression system forHCoV-NL63 S ectodomain) demonstrate high level of consistency. Secondly, such consistency allowed analysing differences between the NL63 spike and the SARS-CoV-2 S structures, revealing and evaluation sites related to the receptor bindings. Thirdly, the structure of the NL63 spike from the vitrified viruses provides more complete information on glycosylation sites. This study will help to explain discrepancy in the pathogenicity between alpha and beta families of coronaviruses.\u003C\u002Fp\u003E\u003Cp\u003EThe methodologies used for the imaging and reconstruction processing followed by building the atomic modelare on the level of the state-of-the-art. The MS is well written and concise.Overall this is an important study at the current pandemic and linked to pathogenicity of the virus. It is related to the findingmedical means for suppressing infections.\u003C\u002Fp\u003E\u003Cp\u003EIt would be good if the comments listed below will be addressed:\u003C\u002Fp\u003E\u003Cp\u003EComparison of structures NL63 (HCoV-NL63) and SARS-CoV-2spikes indicated large rearrangements between domainsA and B. What is known about similarity (homology) of these domains and linkers between them?While a simplified schematic representation was given inWalls et all (NSMB,2016, Fig4) it does not provide sufficient information for explanation of biological relevance of this conformational differences.It would be useful to see the sequence alignment at least for domains ABCD (as a supplementary figure). Possibly, it will help to explain such big shift of the B domain in the SARS-CoV-2 S and the open conformation of the RBDs. It seems that the linker between A and B is shorter in NL63 so a different mechanism should be used for triggering the receptor binding.\u003C\u002Fp\u003E\u003Cp\u003EIt is rather difficult to find both the upstream helix and locations of the triggers loops within the entire spike structures.Therefore, it would be useful to highlight locations of the S2' trigger-loop region on side views of spikes (Figure 4a). Here may be hidden a very interesting mechanism of the spike activation.\u003C\u002Fp\u003E\u003Cp\u003EThe Fourier-Shell correlation graph should be deposited to the EMDB. Page 18 of the report: the table \"Experimental information\" 4 is practically empty, although these information is present in methods.\u003C\u002Fp\u003E\u003Cp\u003EThe authors have done good fitting and geometry of the model is rather good, but they did not read the report of evaluation of the fit quality:\u003C\u002Fp\u003E\u003Cp\u003E\"A red diamond above a residue indicates a poor fit to the EM map for this residue (all atom inclusion < 40%).\" That effect takes place if the authors have used a too high threshold for the presentation and fitting of the model into the map. So it would make sense to try a lower threshold and the number of red diamonds will be possibly reduced and hopefully will be more consistent with other graphs in the evaluation report.\u003C\u002Fp\u003E\u003Cp\u003EIt would be good to explain why locations of ligands were poorly defined, since too many of them have high percentage of misplacements (both in bonds length and angles). While this fact does not diminish the value of the MS some verbal explanation will be helpful.\u003C\u002Fp\u003E",publishDate:"2020-09-28T00:00:00.000Z",onlinePublishDate:o,reviewerRole:ca,recommendation:x,revisionRound:H},{title:"\u003Cdiv class=\"article-title\"\u003EReview: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R0\u002FPR2\u003C\u002Fdiv\u003E",productId:"2274E00CD9D4DCAE8FC69C89A1CF4932",position:bZ,sections:[],conflictOfInterests:b$,contributor:{givenNames:"Sheemei",surname:"Lok",nameStyle:g,affiliations:[{text:"Emerging Infectious Diseases, Duke-NUS Medical School, Singapore"}],isCorresponding:a,notes:g,isAnonymous:a,fullName:"Sheemei Lok",searchUrl:"\u002Fcore\u002Fsearch?filters%5BauthorTerms%5D=Sheemei%20Lok&eventCode=SE-AU",orcidUrl:"https:\u002F\u002Forcid.org\u002F0000-0003-4631-8041"},comments:"\u003Cp\u003E\n\u003Cspan class=\"italic\"\u003EComments to Author\u003C\u002Fspan\u003E: \"A 3.4Å cryoEM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles\" by Zhang et al\u003C\u002Fp\u003E\u003Cp\u003EThe authors reported a 3.4Å resolution cryoEM structure of the S protein on the NL63 virus. Previously another cryoEM structure of the recombinantly expressed ectodomain of the NL63 S protein was determined to similar resolution (Walls et al., 2016). Structural comparison shows they are highly similar except that the current structure on the virus surface shows more glycosylation sites likely because the virus was grown in mammalian cells compared to the ectodomain S protein that was expressed in insect cells. Their map also showed extended density pointing towards the viral membrane although they are unable to recognize secondary structure elements. Also they showed that the RBD domain of the S proteins on the virus surface are in a \"down\" or \"closed\" state.\u003C\u002Fp\u003E\u003Cp\u003EGlycosylation can shield the protein structures from antibody binding, therefore the level of glycosylation will affect the antigenic property of the S proteins. The results here showed that in mammalian cells, the protein are highly glycosylated. This offer important information perhaps to why antibody response is poor towards coronaviruses. The structural studies here is technically well done.\u003C\u002Fp\u003E\u003Cp\u003EThis reviewer only have minor comments:\u003C\u002Fp\u003E\u003Cp\u003E(1)Page 4 line 113, the authors should put the reference to the map of the purified S ectodomain or its EMDB code.\u003C\u002Fp\u003E\u003Cp\u003E(2)Page 5 line 130 \"As shown in Fig. 1 and 2\", I don't not see any figures regarding the RBD in a downwards conformation in Figure 2. Is that a mistake?\u003C\u002Fp\u003E\u003Cp\u003E(3)There is no title for Table 1 and Supplementary Table S2\u003C\u002Fp\u003E\u003Cp\u003E(4)Figure S1: It is hard to see the overlap of the two maps with and without C3 imposed.\u003C\u002Fp\u003E\u003Cp\u003E(5)Caption of Figure 1: (c-d) should mention the cryoEM map is that of the C3 averaged map or not.\u003C\u002Fp\u003E",publishDate:"2020-09-14T00:00:00.000Z",onlinePublishDate:o,reviewerRole:ca,recommendation:x,revisionRound:H},{title:"\u003Cdiv class=\"article-title\"\u003EDecision: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R0\u002FPR3\u003C\u002Fdiv\u003E",productId:"2C758F9BBF34CB087A51DE54730BF3D0",position:b_,sections:[],contributor:{givenNames:I,surname:J,nameStyle:g,affiliations:[{text:K}],isCorresponding:a,notes:g,isAnonymous:a,fullName:L,searchUrl:M,orcidUrl:N},comments:"\u003Cp\u003E\n\u003Cspan class=\"italic\"\u003EComments to Author\u003C\u002Fspan\u003E: Reviewer #1: \"A 3.4Å cryoEM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles\" by Zhang et al\u003C\u002Fp\u003E\u003Cp\u003EThe authors reported a 3.4Å resolution cryoEM structure of the S protein on the NL63 virus. Previously another cryoEM structure of the recombinantly expressed ectodomain of the NL63 S protein was determined to similar resolution (Walls et al., 2016). Structural comparison shows they are highly similar except that the current structure on the virus surface shows more glycosylation sites likely because the virus was grown in mammalian cells compared to the ectodomain S protein that was expressed in insect cells. Their map also showed extended density pointing towards the viral membrane although they are unable to recognize secondary structure elements. Also they showed that the RBD domain of the S proteins on the virus surface are in a \"down\" or \"closed\" state.\u003C\u002Fp\u003E\u003Cp\u003EGlycosylation can shield the protein structures from antibody binding, therefore the level of glycosylation will affect the antigenic property of the S proteins. The results here showed that in mammalian cells, the protein are highly glycosylated. This offer important information perhaps to why antibody response is poor towards coronaviruses. The structural studies here is technically well done.\u003C\u002Fp\u003E\u003Cp\u003EThis reviewer only have minor comments:\u003C\u002Fp\u003E\u003Cp\u003E(1)Page 4 line 113, the authors should put the reference to the map of the purified S ectodomain or its EMDB code.\u003C\u002Fp\u003E\u003Cp\u003E(2)Page 5 line 130 \"As shown in Fig. 1 and 2\", I don't not see any figures regarding the RBD in a downwards conformation in Figure 2. Is that a mistake?\u003C\u002Fp\u003E\u003Cp\u003E(3)There is no title for Table 1 and Supplementary Table S2\u003C\u002Fp\u003E\u003Cp\u003E(4)Figure S1: It is hard to see the overlap of the two maps with and without C3 imposed.\u003C\u002Fp\u003E\u003Cp\u003E(5)Caption of Figure 1: (c-d) should mention the cryoEM map is that of the C3 averaged map or not.\u003C\u002Fp\u003E\u003Cp\u003EReviewer #2: The manuscript \"A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles\" by Zhang and co-authors reports a structure of the human coronavirus NL63 (HCoV-NL63) spike. This impactful study provides analysis of domain localisations within the HCoV-NL63 S (spike) trimer without chemical fixative in its prefusion conformation. Cryo-EM has been used in this structural study. The results of the research reported in the MS have several major outcomes. Firstly, the authors have proved the faithfulness of structural organisation of the NL63 spike obtained.Two structures (one from vitrified complete virus and another obtained using an expression system forHCoV-NL63 S ectodomain) demonstrate high level of consistency. Secondly, such consistency allowed analysing differences between the NL63 spike and the SARS-CoV-2 S structures, revealing and evaluation sites related to the receptor bindings. Thirdly, the structure of the NL63 spike from the vitrified viruses provides more complete information on glycosylation sites. This study will help to explain discrepancy in the pathogenicity between alpha and beta families of coronaviruses.\u003C\u002Fp\u003E\u003Cp\u003EThe methodologies used for the imaging and reconstruction processing followed by building the atomic modelare on the level of the state-of-the-art. The MS is well written and concise.Overall this is an important study at the current pandemic and linked to pathogenicity of the virus. It is related to the findingmedical means for suppressing infections.\u003C\u002Fp\u003E\u003Cp\u003EIt would be good if the comments listed below will be addressed:\u003C\u002Fp\u003E\u003Cp\u003EComparison of structures NL63 (HCoV-NL63) and SARS-CoV-2spikes indicated large rearrangements between domainsA and B. What is known about similarity (homology) of these domains and linkers between them?While a simplified schematic representation was given inWalls et all (NSMB,2016, Fig4) it does not provide sufficient information for explanation of biological relevance of this conformational differences.It would be useful to see the sequence alignment at least for domains ABCD (as a supplementary figure). Possibly, it will help to explain such big shift of the B domain in the SARS-CoV-2 S and the open conformation of the RBDs. It seems that the linker between A and B is shorter in NL63 so a different mechanism should be used for triggering the receptor binding.\u003C\u002Fp\u003E\u003Cp\u003EIt is rather difficult to find both the upstream helix and locations of the triggers loops within the entire spike structures.Therefore, it would be useful to highlight locations of the S2' trigger-loop region on side views of spikes (Figure 4a). Here may be hidden a very interesting mechanism of the spike activation.\u003C\u002Fp\u003E\u003Cp\u003EThe Fourier-Shell correlation graph should be deposited to the EMDB. Page 18 of the report: the table \"Experimental information\" 4 is practically empty, although these information is present in methods.\u003C\u002Fp\u003E\u003Cp\u003EThe authors have done good fitting and geometry of the model is rather good, but they did not read the report of evaluation of the fit quality:\u003C\u002Fp\u003E\u003Cp\u003E\"A red diamond above a residue indicates a poor fit to the EM map for this residue (all atom inclusion < 40%).\" That effect takes place if the authors have used a too high threshold for the presentation and fitting of the model into the map. So it would make sense to try a lower threshold and the number of red diamonds will be possibly reduced and hopefully will be more consistent with other graphs in the evaluation report.\u003C\u002Fp\u003E\u003Cp\u003EIt would be good to explain why locations of ligands were poorly defined, since too many of them have high percentage of misplacements (both in bonds length and angles). While this fact does not diminish the value of the MS some verbal explanation will be helpful.\u003C\u002Fp\u003E",onlinePublishDate:o,reviewerRole:O,recommendation:x,revisionRound:H},{title:"\u003Cdiv class=\"article-title\"\u003EDecision: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — R1\u002FPR4\u003C\u002Fdiv\u003E",productId:"E2C45115C6ACA2E9DAEF737AF7C24EAE",position:4,sections:[],contributor:{givenNames:I,surname:J,nameStyle:g,affiliations:[{text:K}],isCorresponding:a,notes:g,isAnonymous:a,fullName:L,searchUrl:M,orcidUrl:N},comments:cb,onlinePublishDate:o,reviewerRole:O,recommendation:x,revisionRound:W},{title:"\u003Cdiv class=\"article-title\"\u003EDecision: A 3.4-Å cryo-EM structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles — 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of Virology","Acta Crystallographica Section D Biological Crystallography","Proceedings of the National Academy of Sciences","2017","2020-11-17T00:00:00.000Z","Department of Bioengineering and James H. Clark Center, Stanford University, Stanford, CA94305, USA","QRB Discovery","2018","Protein Science","Nature Structural & Molecular Biology","Nature Methods","Science","Nucleic Acids Research","minor-revision","A 3.4-Å cryo-electron microscopy structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles","Division of CryoEM and Bioimaging, SSRL, SLAC National Accelerator Laboratory, Menlo Park, CA94025, USA","66","2010","2009","unknown","14","2004","2006","0","Bengt J. F.","Nordén","Chemistry and Chemical Engineering, Chalmers University of Technology, Sweden","Bengt J. F. 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Utilizes Heparan Sulfate Proteoglycans for Attachment to Target Cells","10.1128\u002FJVI.02078-14","Entry of Human Coronavirus NL63 into the Cell","10.1128\u002FJVI.01933-17","Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen","10.1073\u002Fpnas.1707304114","Structures of MERS-CoV spike glycoprotein in complex with sialoside attachment receptors","2019","10.1038\u002Fs41594-019-0334-7","UCSF Chimera?A visualization system for exploratory research and analysis","Journal of Computational Chemistry","10.1002\u002Fjcc.20084","Measurement of atom resolvability in cryo-EM maps with Q-scores","10.1038\u002Fs41592-020-0731-1","Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions","Journal of Structural Biology","10.1016\u002Fj.jsb.2010.03.007","Co-circulation of three camel coronavirus species and recombination of MERS-CoVs in Saudi 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Glycoprotein","Cell","10.1016\u002Fj.cell.2020.02.058","Review of Bats and SARS","Emerging Infectious Diseases","10.3201\u002Feid1212.060401","Discovery of a subgenotype of human coronavirus NL63 associated with severe lower respiratory tract infection in China, 2018","Emerging Microbes & Infections","10.1080\u002F22221751.2020.1717999","Cryo-Electron Tomography and Subtomogram Averaging","The Resolution Revolution: Recent Advances In cryoEM","367","Exploitation of glycosylation in enveloped virus pathobiology","Biochimica et Biophysica Acta (BBA) – General Subjects","10.1016\u002Fj.bbagen.2019.05.012","Vulnerabilities in coronavirus glycan shields despite extensive glycosylation","Nature Communications","10.1038\u002Fs41467-020-16567-0","SWISS-MODEL: homology modelling of protein structures and complexes","10.1093\u002Fnar\u002Fgky427","Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation","10.1126\u002Fscience.abb2507","Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor","10.1073\u002Fpnas.0908837106","TM-align: a protein structure alignment algorithm based on the TM-score","10.1093\u002Fnar\u002Fgki524","Core Structure of S2 from the Human Coronavirus NL63 Spike Glycoprotein†,‡","Biochemistry","10.1021\u002Fbi061686w","MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy","10.1038\u002Fnmeth.4193","A pneumonia outbreak associated with a new coronavirus of probable bat 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If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. <a href="/core/help">Find out more about saving content to Dropbox</a>. </p> </div> </div> <div class="row book-title"> <div class="small-12 columns"> <div class="heading_08"><div class="title">A 3.4-Å cryo-electron microscopy structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles</div></div> </div> </div> <div class="row book-details book-overview"> <div class="small-12 columns"> <ul> <li class="volume-issue">Volume 1</li> <li class="author"> <a href="/core/search?filters%5BauthorTerms%5D=Kaiming Zhang&eventCode=SE-AU" class="more-by-this-author ">Kaiming Zhang</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0003-0414-4776" aria-label="Open the ORCID record for Kaiming Zhang in new tab/window"></a> <sup data-affiliation-id="a1" class="">(a1)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=Shanshan Li&eventCode=SE-AU" class="more-by-this-author ">Shanshan Li</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0002-7041-5960" aria-label="Open the ORCID record for Shanshan Li in new tab/window"></a> <sup data-affiliation-id="a1" class="">(a1)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=Grigore Pintilie&eventCode=SE-AU" class="more-by-this-author ">Grigore Pintilie</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0002-0848-5335" aria-label="Open the ORCID record for Grigore Pintilie in new tab/window"></a> <sup data-affiliation-id="a1" class="">(a1)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=David Chmielewski&eventCode=SE-AU" class="more-by-this-author ">David Chmielewski</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0002-4498-7949" aria-label="Open the ORCID record for David Chmielewski in new tab/window"></a> <sup data-affiliation-id="a2" class="">(a2)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=Michael F. 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If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. <a href="/core/help">Find out more about saving content to Google Drive</a>. </p> </div> </div> <div class="row book-title"> <div class="small-12 columns"> <div class="heading_08"><div class="title">A 3.4-Å cryo-electron microscopy structure of the human coronavirus spike trimer computationally derived from vitrified NL63 virus particles</div></div> </div> </div> <div class="row book-details book-overview"> <div class="small-12 columns"> <ul> <li class="volume-issue">Volume 1</li> <li class="author"> <a href="/core/search?filters%5BauthorTerms%5D=Kaiming Zhang&eventCode=SE-AU" class="more-by-this-author ">Kaiming Zhang</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0003-0414-4776" aria-label="Open the ORCID record for Kaiming Zhang in new tab/window"></a> <sup data-affiliation-id="a1" class="">(a1)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=Shanshan Li&eventCode=SE-AU" class="more-by-this-author ">Shanshan Li</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0002-7041-5960" aria-label="Open the ORCID record for Shanshan Li in new tab/window"></a> <sup data-affiliation-id="a1" class="">(a1)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=Grigore Pintilie&eventCode=SE-AU" class="more-by-this-author ">Grigore Pintilie</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0002-0848-5335" aria-label="Open the ORCID record for Grigore Pintilie in new tab/window"></a> <sup data-affiliation-id="a1" class="">(a1)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=David Chmielewski&eventCode=SE-AU" class="more-by-this-author ">David Chmielewski</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0002-4498-7949" aria-label="Open the ORCID record for David Chmielewski in new tab/window"></a> <sup data-affiliation-id="a2" class="">(a2)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=Michael F. 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Schmid in new tab/window"></a> <sup data-affiliation-id="a3" class="">(a3)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=Graham Simmons&eventCode=SE-AU" class="more-by-this-author ">Graham Simmons</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0002-9615-7023" aria-label="Open the ORCID record for Graham Simmons in new tab/window"></a> <sup data-affiliation-id="a4" class="">(a4)</sup><span class="separator ">, </span><a href="/core/search?filters%5BauthorTerms%5D=Jing Jin&eventCode=SE-AU" class="more-by-this-author ">Jing Jin</a><a target="_blank" class="orcid-logo " href="https://orcid.org/0000-0003-3994-8600" aria-label="Open the ORCID record for Jing Jin in new tab/window"></a> <sup data-affiliation-id="a4" class="">(a4)</sup> <sup data-affiliation-id="a3" class="">(a3)</sup><span class="separator "> and </span><a href="/core/search?filters%5BauthorTerms%5D=Wah Chiu&eventCode=SE-AU" class="more-by-this-author ">Wah 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fill="#0072CF" d="M20.4 25.3V15.2h-4.9v2.2h1.1v7.9h-1.1v2.2h6v-2.2h-1.1zm-1.9-11.4c1 0 1.9-1 1.9-2.2 0-1.2-.8-2.2-1.9-2.2s-1.9 1-1.9 2.2c0 1.2.9 2.2 1.9 2.2z"/> </svg> </a> </span> <div id="comment-email-tip_--x--" data-dropdown-content role="dialog" aria-modal="true" aria-hidden="true" tabindex="-1" class="f-dropdown content medium" data-remove-focus="true" aria-label="Email information"> <div class="close-container"> <a href="#" class="button small transparent-no-border radius tooltip-close-btn" id="tooltip-close-link-comment-email-tip_--x--"> <span class="custom-tooltip-button-remove"> <span class="sr-only">Close Email help</span> <svg width="20" height="20" viewBox="0 0 20 20" xmlns="http://www.w3.org/2000/svg" xmlns:xlink="http://www.w3.org/1999/xlink" aria-hidden="true" focusable="false"> <defs> <path d="M9.986 0C4.479 0 0 4.434 0 9.916c0 5.469 4.465 9.916 9.986 9.916 5.507 0 9.986-4.433 9.986-9.916C19.958 4.434 15.493 0 9.986 0z" id="a-comment-email-tip_--x--"/> <mask id="b-comment-email-tip_--x--" x="0" y="0" width="19.972" height="19.832" fill="#fff"><use xlink:href="#a-comment-email-tip_--x--"/></mask> </defs> <g fill="none" fill-rule="evenodd"> <use stroke="#436FCC" mask="url(#b-comment-email-tip_--x--)" stroke-width="2" xlink:href="#a-comment-email-tip_--x--"/> <path d="M14.778 13.325a.983.983 0 0 1 0 1.385.982.982 0 0 1-.704.28c-.254 0-.507-.098-.704-.28l-3.352-3.329-3.353 3.329a.973.973 0 0 1-.69.28 1.01 1.01 0 0 1-.69-.28.983.983 0 0 1 0-1.385l3.352-3.328-3.352-3.33a.983.983 0 0 1 0-1.384 1 1 0 0 1 1.395 0l3.352 3.329 3.352-3.329a1 1 0 0 1 1.394 0 .983.983 0 0 1 0 1.385l-3.352 3.329 3.352 3.328z" fill="#436FCC"/> </g> </svg> </span> </a> </div> <p id="info-comment-email-tip_--x--" class="text-left">Your email address will be used in order to notify you when your comment has been reviewed by the moderator and in case the author(s) of the article or the moderator need to contact you directly.</p> </div> <input name="emailAddress_--x--" 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