Combination of KIR and HLA gene variants augments the risk of developing birdshot chorioretinopathy in HLA-A*29-positive individuals

<!DOCTYPE html> <html lang="en" class="grade-c"> <head> <title>Combination of KIR and HLA gene variants augments the risk of developing birdshot chorioretinopathy in HLA-A*29-positive individuals | Genes & Immunity</title> <link rel="alternate" type="application/rss+xml" href="https://www.nature.com/gene.rss"/> <link rel="preconnect" href="https://cmp.nature.com" crossorigin> <meta http-equiv="X-UA-Compatible" content="IE=edge"> <meta name="applicable-device" content="pc,mobile"> <meta name="viewport" content="width=device-width,initial-scale=1.0,maximum-scale=5,user-scalable=yes"> <meta name="360-site-verification" content="5a2dc4ab3fcb9b0393241ffbbb490480" /> <script data-test="dataLayer"> window.dataLayer = [{"content":{"category":{"contentType":"original article","legacy":{"webtrendsPrimaryArticleType":"research","webtrendsSubjectTerms":null,"webtrendsContentCategory":null,"webtrendsContentCollection":null,"webtrendsContentGroup":"Genes & 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Although HLA-A29 occurs frequently in all populations, BCR affects only a small percentage of HLA-A29-positive Caucasians, indicating additional susceptibility factors for BCR. Discovery of HLA class I-specific killer cell immunoglobulin-like receptors (KIR) led to a series of epidemiological studies implicating KIR–HLA gene combinations in disease. Here, we characterized KIR–HLA pairs in BCR patients and controls carrying HLA-A*29 as well as controls lacking HLA-A*29. KIR–HLA pairs implicated for weak inhibition (KIR2DL2/3+HLA-C1 and KIR3DL1+HLA-Bw4T80) in combination with activating KIR genes associated with autoimmunity (KIR2DS2, 2DS3 and 2DS4) augment the risk of developing BCR in HLA-A*29-positive individuals. The reciprocal association of strong inhibitory pairs (KIR3DL1+HLA-Bw4I80 and KIR2DL1+HLA-C2) in combination with those implicated in protection from infection (KIR3DS1+HLA-Bw4I80 and KIR2DS1+HLA-C2) was observed in HLA-A*29-negative controls. These results suggest that a profound effect of KIR2DS2/S3/S4 in the absence of strong inhibition may enhance the activation of natural killer cells and T-cell subsets against intraocular self-antigens, thereby contributing to pathogenesis of BCR.","datePublished":"2008-03-13T00:00:00Z","dateModified":"2008-03-13T00:00:00Z","pageStart":"249","pageEnd":"258","sameAs":"https://doi.org/10.1038/gene.2008.13","keywords":["natural killer cells","autoimmunity","MHC","birdshot chorioretinopathy","killer cell immunoglobulin-like receptors","disease association","Biomedicine","general","Human Genetics","Immunology","Cancer Research","Gene 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UCLA Immunogenetics Center, David Geffen School of Medicine at UCLA, University of California at Los Angeles, Los Angeles, USA","@type":"PostalAddress"},"@type":"Organization"}],"email":"rrajalingam@mednet.ucla.edu","@type":"Person"}],"isAccessibleForFree":false,"hasPart":{"isAccessibleForFree":false,"cssSelector":".main-content","@type":"WebPageElement"},"@type":"ScholarlyArticle"},"@context":"https://schema.org","@type":"WebPage"}</script> <link rel="canonical" href="https://www.nature.com/articles/gene200813"> <meta name="journal_id" content="41435"/> <meta name="dc.title" content="Combination of KIR and HLA gene variants augments the risk of developing birdshot chorioretinopathy in HLA-A*29-positive individuals"/> <meta name="dc.source" content="Genes & Immunity 2008 9:3"/> <meta name="dc.format" content="text/html"/> <meta name="dc.publisher" content="Nature Publishing Group"/> <meta name="dc.date" content="2008-03-13"/> <meta name="dc.type" content="OriginalPaper"/> <meta name="dc.language" content="En"/> <meta name="dc.copyright" content="2008 Springer Nature Limited"/> <meta name="dc.rights" content="2008 Springer Nature Limited"/> <meta name="dc.rightsAgent" content="journalpermissions@springernature.com"/> <meta name="dc.description" content="Birdshot chorioretinopathy (BCR), a chronic ocular inflammatory disease with characteristic choroidal lymphocytic infiltrates, has been strongly associated with human leukocyte antigen (HLA)-A29. Although HLA-A29 occurs frequently in all populations, BCR affects only a small percentage of HLA-A29-positive Caucasians, indicating additional susceptibility factors for BCR. Discovery of HLA class I-specific killer cell immunoglobulin-like receptors (KIR) led to a series of epidemiological studies implicating KIR–HLA gene combinations in disease. Here, we characterized KIR–HLA pairs in BCR patients and controls carrying HLA-A*29 as well as controls lacking HLA-A*29. KIR–HLA pairs implicated for weak inhibition (KIR2DL2/3+HLA-C1 and KIR3DL1+HLA-Bw4T80) in combination with activating KIR genes associated with autoimmunity (KIR2DS2, 2DS3 and 2DS4) augment the risk of developing BCR in HLA-A*29-positive individuals. The reciprocal association of strong inhibitory pairs (KIR3DL1+HLA-Bw4I80 and KIR2DL1+HLA-C2) in combination with those implicated in protection from infection (KIR3DS1+HLA-Bw4I80 and KIR2DS1+HLA-C2) was observed in HLA-A*29-negative controls. These results suggest that a profound effect of KIR2DS2/S3/S4 in the absence of strong inhibition may enhance the activation of natural killer cells and T-cell subsets against intraocular self-antigens, thereby contributing to pathogenesis of BCR."/> <meta name="prism.issn" content="1476-5470"/> <meta name="prism.publicationName" content="Genes & Immunity"/> <meta name="prism.publicationDate" content="2008-03-13"/> <meta name="prism.volume" content="9"/> <meta name="prism.number" content="3"/> <meta name="prism.section" content="OriginalPaper"/> <meta name="prism.startingPage" content="249"/> <meta name="prism.endingPage" content="258"/> <meta name="prism.copyright" content="2008 Springer Nature Limited"/> <meta name="prism.rightsAgent" content="journalpermissions@springernature.com"/> <meta name="prism.url" content="https://www.nature.com/articles/gene200813"/> <meta name="prism.doi" content="doi:10.1038/gene.2008.13"/> <meta name="citation_pdf_url" content="https://www.nature.com/articles/gene200813.pdf"/> <meta name="citation_fulltext_html_url" content="https://www.nature.com/articles/gene200813"/> <meta name="citation_journal_title" content="Genes & Immunity"/> <meta name="citation_journal_abbrev" content="Genes Immun"/> <meta name="citation_publisher" content="Nature Publishing Group"/> <meta name="citation_issn" content="1476-5470"/> <meta name="citation_title" content="Combination of KIR and HLA gene variants augments the risk of developing birdshot chorioretinopathy in HLA-A*29-positive individuals"/> <meta name="citation_volume" content="9"/> <meta name="citation_issue" content="3"/> <meta name="citation_publication_date" content="2008/04"/> <meta name="citation_online_date" content="2008/03/13"/> <meta name="citation_firstpage" content="249"/> <meta name="citation_lastpage" content="258"/> <meta name="citation_article_type" content="Article"/> <meta name="citation_language" content="en"/> <meta name="dc.identifier" content="doi:10.1038/gene.2008.13"/> <meta name="DOI" content="10.1038/gene.2008.13"/> <meta name="size" content="291418"/> <meta name="citation_doi" content="10.1038/gene.2008.13"/> <meta name="citation_springer_api_url" content="http://api.springer.com/xmldata/jats?q=doi:10.1038/gene.2008.13&api_key="/> <meta name="description" content="Birdshot chorioretinopathy (BCR), a chronic ocular inflammatory disease with characteristic choroidal lymphocytic infiltrates, has been strongly associated with human leukocyte antigen (HLA)-A29. Although HLA-A29 occurs frequently in all populations, BCR affects only a small percentage of HLA-A29-positive Caucasians, indicating additional susceptibility factors for BCR. Discovery of HLA class I-specific killer cell immunoglobulin-like receptors (KIR) led to a series of epidemiological studies implicating KIR–HLA gene combinations in disease. Here, we characterized KIR–HLA pairs in BCR patients and controls carrying HLA-A*29 as well as controls lacking HLA-A*29. KIR–HLA pairs implicated for weak inhibition (KIR2DL2/3+HLA-C1 and KIR3DL1+HLA-Bw4T80) in combination with activating KIR genes associated with autoimmunity (KIR2DS2, 2DS3 and 2DS4) augment the risk of developing BCR in HLA-A*29-positive individuals. The reciprocal association of strong inhibitory pairs (KIR3DL1+HLA-Bw4I80 and KIR2DL1+HLA-C2) in combination with those implicated in protection from infection (KIR3DS1+HLA-Bw4I80 and KIR2DS1+HLA-C2) was observed in HLA-A*29-negative controls. These results suggest that a profound effect of KIR2DS2/S3/S4 in the absence of strong inhibition may enhance the activation of natural killer cells and T-cell subsets against intraocular self-antigens, thereby contributing to pathogenesis of BCR."/> <meta name="dc.creator" content="Levinson, R D"/> <meta name="dc.creator" content="Du, Z"/> <meta name="dc.creator" content="Luo, L"/> <meta name="dc.creator" content="Monnet, D"/> <meta name="dc.creator" content="Tabary, T"/> <meta name="dc.creator" content="Brezin, A P"/> <meta name="dc.creator" content="Zhao, L"/> <meta name="dc.creator" content="Gjertson, D W"/> <meta name="dc.creator" content="Holland, G N"/> <meta name="dc.creator" content="Reed, E F"/> <meta name="dc.creator" content="Cohen, J H M"/> <meta name="dc.creator" content="Rajalingam, R"/> <meta name="dc.subject" content="Biomedicine, general"/> <meta name="dc.subject" content="Human Genetics"/> <meta name="dc.subject" content="Immunology"/> <meta name="dc.subject" content="Cancer Research"/> <meta name="dc.subject" content="Gene Expression"/> <meta name="citation_reference" content="citation_journal_title=Prog Retin Eye Res; 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10)"/> </svg> </li><li class="c-breadcrumbs__item" id="breadcrumb3" itemprop="itemListElement" itemscope itemtype="https://schema.org/ListItem"> <span itemprop="name">article</span><meta itemprop="position" content="4"></li> </ol> </div> </nav> </div> <div class="u-container u-mt-32 u-mb-32 u-clearfix" id="content" data-component="article-container" data-container-type="article"> <main class="c-article-main-column u-float-left js-main-column" data-track-component="article body"> <article lang="en"> <div class="c-article-header"> <header> <ul class="c-article-identifiers" data-test="article-identifier"> <li class="c-article-identifiers__item" data-test="article-category">Original Article</li> <li class="c-article-identifiers__item">Published: <time datetime="2008-03-13">13 March 2008</time></li> </ul> <h1 class="c-article-title" data-test="article-title" data-article-title="">Combination of <i>KIR</i> and <i>HLA</i> gene variants augments the risk of developing birdshot chorioretinopathy in <i>HLA-A*29</i>-positive individuals</h1> <ul class="c-article-author-list c-article-author-list--short" data-test="authors-list" data-component-authors-activator="authors-list"><li class="c-article-author-list__item"><a data-test="author-name" data-track="click" data-track-action="open author" data-track-label="link" href="#auth-R_D-Levinson-Aff1" data-author-popup="auth-R_D-Levinson-Aff1" data-author-search="Levinson, R D">R D Levinson</a><sup class="u-js-hide"><a href="#Aff1">1</a></sup><sup class="u-js-hide"> <a href="#na1">na1</a></sup>, </li><li class="c-article-author-list__item"><a data-test="author-name" data-track="click" data-track-action="open author" data-track-label="link" href="#auth-Z-Du-Aff2" data-author-popup="auth-Z-Du-Aff2" data-author-search="Du, Z">Z Du</a><sup class="u-js-hide"><a href="#Aff2">2</a></sup><sup class="u-js-hide"> <a href="#na1">na1</a></sup>, </li><li class="c-article-author-list__item 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data-author-popup="auth-D_W-Gjertson-Aff2-Aff5" data-author-search="Gjertson, D W">D W Gjertson</a><sup class="u-js-hide"><a href="#Aff2">2</a>,<a href="#Aff5">5</a></sup>, </li><li class="c-article-author-list__item c-article-author-list__item--hide-small-screen"><a data-test="author-name" data-track="click" data-track-action="open author" data-track-label="link" href="#auth-G_N-Holland-Aff1" data-author-popup="auth-G_N-Holland-Aff1" data-author-search="Holland, G N">G N Holland</a><sup class="u-js-hide"><a href="#Aff1">1</a></sup>, </li><li class="c-article-author-list__item c-article-author-list__item--hide-small-screen"><a data-test="author-name" data-track="click" data-track-action="open author" data-track-label="link" href="#auth-E_F-Reed-Aff2" data-author-popup="auth-E_F-Reed-Aff2" data-author-search="Reed, E F">E F Reed</a><sup class="u-js-hide"><a href="#Aff2">2</a></sup>, </li><li class="c-article-author-list__item c-article-author-list__item--hide-small-screen"><a 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class="c-article-metrics-bar u-list-reset"> <li class=" c-article-metrics-bar__item" data-test="access-count"> <p class="c-article-metrics-bar__count">1222 <span class="c-article-metrics-bar__label">Accesses</span></p> </li> <li class="c-article-metrics-bar__item" data-test="citation-count"> <p class="c-article-metrics-bar__count">35 <span class="c-article-metrics-bar__label">Citations</span></p> </li> <li class="c-article-metrics-bar__item"> <p class="c-article-metrics-bar__details"><a href="/articles/gene200813/metrics" data-track="click" data-track-action="view metrics" data-track-label="link" rel="nofollow">Metrics <span class="u-visually-hidden">details</span></a></p> </li> </ul> </div> </header> </div> <div class="c-article-body"> <section aria-labelledby="Abs1" data-title="Abstract" lang="en"><div class="c-article-section" id="Abs1-section"><h2 class="c-article-section__title js-section-title js-c-reading-companion-sections-item" id="Abs1">Abstract</h2><div class="c-article-section__content" id="Abs1-content"><p>Birdshot chorioretinopathy (BCR), a chronic ocular inflammatory disease with characteristic choroidal lymphocytic infiltrates, has been strongly associated with human leukocyte antigen (HLA)-A29. Although HLA-A29 occurs frequently in all populations, BCR affects only a small percentage of HLA-A29-positive Caucasians, indicating additional susceptibility factors for BCR. Discovery of HLA class I-specific killer cell immunoglobulin-like receptors (KIR) led to a series of epidemiological studies implicating <i>KIR–HLA</i> gene combinations in disease. Here, we characterized <i>KIR–HLA</i> pairs in BCR patients and controls carrying <i>HLA-A*29</i> as well as controls lacking <i>HLA-A*29</i>. <i>KIR–HLA</i> pairs implicated for weak inhibition (<i>KIR2DL2/3+HLA-C1</i> and <i>KIR3DL1+HLA-Bw4</i><sup><i>T80</i></sup>) in combination with activating <i>KIR</i> genes associated with autoimmunity (<i>KIR2DS2</i>, <i>2DS3</i> and <i>2DS4</i>) augment the risk of developing BCR in <i>HLA-A*29</i>-positive individuals. The reciprocal association of strong inhibitory pairs (<i>KIR3DL1+HLA-Bw4</i><sup><i>I80</i></sup> and <i>KIR2DL1+HLA-C2</i>) in combination with those implicated in protection from infection (<i>KIR3DS1+HLA-Bw4</i><sup><i>I80</i></sup> and <i>KIR2DS1+HLA-C2</i>) was observed in <i>HLA-A*29</i>-negative controls. These results suggest that a profound effect of KIR2DS2/S3/S4 in the absence of strong inhibition may enhance the activation of natural killer cells and T-cell subsets against intraocular self-antigens, thereby contributing to pathogenesis of BCR.</p></div></div></section> <div class="js-context-bar-sticky-point-mobile" data-track-context="article body"> <div class="c-nature-box c-nature-box--side c-nature-box--access-to-pdf" data-component="entitlement-box" data-test="entitlement-box"> <div class="js-access-button"> <a href="https://wayf.springernature.com?redirect_uri=https%3A%2F%2Fwww.nature.com%2Farticles%2Fgene200813" class="c-article__button" data-test="ra21"> <svg class="u-icon" width="18" height="18" aria-hidden="true" focusable="false"><use href="#icon-institution"></use></svg> <span class="c-article__button-text">Access through your institution</span> </a> </div> <div class="js-buy-button" data-test="entitlement-box-buy-button"> <a href="#access-options" 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We thank Damian Goodridge, Conexio Genomics, Western Australia for his help in building and optimizing <i>KIR</i> libraries for the use in Assign software.</p></div></div></section><section aria-labelledby="author-information" data-title="Author information"><div class="c-article-section" id="author-information-section"><h2 class="c-article-section__title js-section-title js-c-reading-companion-sections-item" id="author-information">Author information</h2><div class="c-article-section__content" id="author-information-content"><span class="c-article-author-information__subtitle u-visually-hidden" id="author-notes">Author notes</span><ol class="c-article-author-information__list"><li class="c-article-author-information__item" id="na1"><p>R D Levinson and Z Du: These authors contributed equally to this work.</p></li></ol><h3 class="c-article__sub-heading" id="affiliations">Authors and Affiliations</h3><ol class="c-article-author-affiliation__list"><li id="Aff1"><p class="c-article-author-affiliation__address">Ocular Inflammatory Disease Center, Jules Stein Eye Institute, David Geffen School of Medicine at UCLA, University of California at Los Angeles, Los Angeles, CA, USA</p><p class="c-article-author-affiliation__authors-list">R D Levinson & G N Holland</p></li><li id="Aff2"><p class="c-article-author-affiliation__address">Department of Pathology and Laboratory Medicine, UCLA Immunogenetics Center, David Geffen School of Medicine at UCLA, University of California at Los Angeles, Los Angeles, CA, USA</p><p class="c-article-author-affiliation__authors-list">Z Du, L Luo, D W Gjertson, E F Reed & R Rajalingam</p></li><li id="Aff3"><p class="c-article-author-affiliation__address">Service d′ophtalmologie, Hôpital Cochin Assistance Publique, Université Paris Descartes, Hôpitaux de Paris, France</p><p class="c-article-author-affiliation__authors-list">D Monnet & A P Brezin</p></li><li id="Aff4"><p 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href="/search?query=birdshot%20chorioretinopathy&facet-discipline="Biomedicine"" data-track="click" data-track-action="view keyword" data-track-label="link">birdshot chorioretinopathy</a></span></li><li class="c-article-subject-list__subject"><span><a href="/search?query=killer%20cell%20immunoglobulin-like%20receptors&facet-discipline="Biomedicine"" data-track="click" data-track-action="view keyword" data-track-label="link">killer cell immunoglobulin-like receptors</a></span></li><li class="c-article-subject-list__subject"><span><a href="/search?query=disease%20association&facet-discipline="Biomedicine"" data-track="click" data-track-action="view keyword" data-track-label="link">disease association</a></span></li></ul><div data-component="article-info-list"></div></div></div></div></div></section> </div> <section> <div class="c-article-section js-article-section" id="further-reading-section" data-test="further-reading-section"> <h2 class="c-article-section__title js-section-title 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Combination of KIR and HLA gene variants augments the risk of developing birdshot chorioretinopathy in HLA-A*29-positive individuals | Genes & Immunity