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Comparative Proteomics of ccRCC Cell Lines to Identify Kidney Cancer Progression Factors | Cancer Genomics & Proteomics
<!DOCTYPE html> <html lang="en" dir="ltr" xmlns="http://www.w3.org/1999/xhtml" xmlns:mml="http://www.w3.org/1998/Math/MathML"> <head prefix="og: http://ogp.me/ns# article: http://ogp.me/ns/article# book: http://ogp.me/ns/book#" > <!--[if IE]><![endif]--> <link rel="dns-prefetch" href="//cdn.jsdelivr.net" /> <link rel="dns-prefetch" href="//cdn.foxycart.com" /> <link rel="dns-prefetch" href="//scholar.google.com" /> <meta http-equiv="Content-Type" content="text/html; charset=utf-8" /> <meta name="Generator" content="Drupal 7 (http://drupal.org)" /> <link rel="canonical" href="https://cgp.iiarjournals.org/content/21/6/645" /> <link rel="alternate" type="application/pdf" title="Full Text (PDF)" href="/content/21/6/645.full.pdf" /> <link rel="alternate" type="text/plain" title="Full Text (Plain)" href="/content/21/6/645.full.txt" /> <link rel="alternate" type="application/vnd.ms-powerpoint" title="Powerpoint" href="/content/21/6/645.ppt" /> <meta name="issue_cover_image" content="https://cgp.iiarjournals.org/sites/default/files/highwire/cgp/21/6.cover-source.jpg" /> <meta name="type" content="article" /> <meta name="category" content="research-article" /> <meta name="HW.identifier" content="/cgp/21/6/645.atom" /> <meta name="HW.pisa" content="cgp;21/6/645" /> <meta name="DC.Format" content="text/html" /> <meta name="DC.Language" content="en" /> <meta name="DC.Title" content="Comparative Proteomics of ccRCC Cell Lines to Identify Kidney Cancer Progression Factors" /> <meta name="DC.Identifier" content="10.21873/cgp.20480" /> <meta name="DC.Date" content="2024-11-01" /> <meta name="DC.Publisher" content="International Institute of Anticancer Research" /> <meta name="DC.Rights" content="Copyright © 2024, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0)." /> <meta name="DC.AccessRights" content="open-access" /> <meta name="DC.Description" content="Background/Aim: Clear cell renal cell carcinoma (ccRCC) is the most common type of kidney cancer, accounting for approximately 75% of kidney cancers. The objective of this study was to identify novel progression markers for ccRCC based on proteomics, with the goal of stage determination and early diagnosis of kidney cancer patients. Materials and Methods: We performed quantitative global proteomics coupled with Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) and high-resolution tandem mass spectrometry on kidney-derived cells, including HEK-293, 786-O (primary ccRCC), and Caki-1 (metastatic ccRCC) cells, to investigate the novel progression factors of ccRCC. Results: In this study, a total of 1,106 proteins were quantified. The Gene Ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were conducted for differentially expressed proteins (DEPs) that were increased in ccRCC cells compared to HEK-293 cells. Ultimately, 99 DEPs including 75 up-regulated and 24 down-regulated proteins, that were significantly altered in both ccRCC cells, were identified. Among DEPs, vimentin was identified as the most significantly changed protein. Its increased expression in ccRCC was verified through immunoblotting in ccRCC cell lines and immunohistochemistry in kidney tumors. Conclusion: From the global proteomics data detected in ccRCC, we propose 99 DEPs including vimentin as progression factors." /> <meta name="DC.Contributor" content="JUHEE PARK" /> <meta name="DC.Contributor" content="HYUNCHAE SIM" /> <meta name="DC.Contributor" content="EUN HYE LEE" /> <meta name="DC.Contributor" content="BUM SOO KIM" /> <meta name="DC.Contributor" content="JAE-WOOK CHUNG" /> <meta name="DC.Contributor" content="YUN-SOK HA" /> <meta name="DC.Contributor" content="TAE GYUN KWON" /> <meta name="DC.Contributor" content="SANGKYU LEE" /> <meta name="DC.Contributor" content="JUN NYUNG LEE" /> <meta name="article:published_time" content="2024-11-01" /> <meta name="article:section" content="Articles" /> <meta name="citation_title" content="Comparative Proteomics of ccRCC Cell Lines to Identify Kidney Cancer Progression Factors" /> <meta name="citation_abstract" lang="en" content="<p>Background/Aim: Clear cell renal cell carcinoma (ccRCC) is the most common type of kidney cancer, accounting for approximately 75% of kidney cancers. The objective of this study was to identify novel progression markers for ccRCC based on proteomics, with the goal of stage determination and early diagnosis of kidney cancer patients. Materials and Methods: We performed quantitative global proteomics coupled with Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) and high-resolution tandem mass spectrometry on kidney-derived cells, including HEK-293, 786-O (primary ccRCC), and Caki-1 (metastatic ccRCC) cells, to investigate the novel progression factors of ccRCC. Results: In this study, a total of 1,106 proteins were quantified. The Gene Ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were conducted for differentially expressed proteins (DEPs) that were increased in ccRCC cells compared to HEK-293 cells. Ultimately, 99 DEPs including 75 up-regulated and 24 down-regulated proteins, that were significantly altered in both ccRCC cells, were identified. Among DEPs, vimentin was identified as the most significantly changed protein. Its increased expression in ccRCC was verified through immunoblotting in ccRCC cell lines and immunohistochemistry in kidney tumors. Conclusion: From the global proteomics data detected in ccRCC, we propose 99 DEPs including vimentin as progression factors.</p>" /> <meta name="citation_journal_title" content="Cancer Genomics & Proteomics" /> <meta name="citation_publisher" content="International Institute of Anticancer Research" /> <meta name="citation_publication_date" content="2024/11/01" /> <meta name="citation_mjid" content="cgp;21/6/645" /> <meta name="citation_id" content="21/6/645" /> <meta name="citation_public_url" content="https://cgp.iiarjournals.org/content/21/6/645" /> <meta name="citation_abstract_html_url" content="https://cgp.iiarjournals.org/content/21/6/645.abstract" /> <meta name="citation_full_html_url" content="https://cgp.iiarjournals.org/content/21/6/645.full" /> <meta name="citation_pdf_url" content="https://cgp.iiarjournals.org/content/cgp/21/6/645.full.pdf" /> <meta name="citation_issn" content="1109-6535" /> <meta name="citation_issn" content="1790-6245" /> <meta name="citation_doi" content="10.21873/cgp.20480" /> <meta name="citation_pmid" content="39467626" /> <meta name="citation_volume" content="21" /> <meta name="citation_issue" content="6" /> <meta name="citation_article_type" content="Research Article" /> <meta name="citation_section" content="Articles" /> <meta name="citation_firstpage" content="645" /> <meta name="citation_lastpage" content="652" /> <meta name="citation_access" content="all" /> <meta name="citation_author" content="JUHEE PARK" /> <meta name="citation_author_institution" content="College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea" /> <meta name="citation_author" content="HYUNCHAE SIM" /> <meta name="citation_author_institution" content="School of Pharmacy, Sungkyunkwan University, Suwon, Republic of Korea" /> <meta name="citation_author" content="EUN HYE LEE" /> <meta name="citation_author_institution" content="Joint Institute for Regenerative Medicine, Kyungpook National University, Daegu, Republic of Korea" /> <meta name="citation_author" content="BUM SOO KIM" /> <meta name="citation_author_institution" content="Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea" /> <meta name="citation_author" content="JAE-WOOK CHUNG" /> <meta name="citation_author_institution" content="Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea" /> <meta name="citation_author" content="YUN-SOK HA" /> <meta name="citation_author_institution" content="Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea" /> <meta name="citation_author" content="TAE GYUN KWON" /> <meta name="citation_author_institution" content="Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea" /> <meta name="citation_author" content="SANGKYU LEE" /> <meta name="citation_author_institution" content="School of Pharmacy, Sungkyunkwan University, Suwon, Republic of Korea" /> <meta name="citation_author_email" content="sangkyu@skku.edu" /> <meta name="citation_author" content="JUN NYUNG LEE" /> <meta name="citation_author_institution" content="Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea" /> <meta name="citation_author_email" content="ljnlover@gmail.com" /> <meta name="citation_reference" content="citation_journal_title=CA Cancer J Clin;citation_author=RL. 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Cheng;citation_title=Annexin A2 in renal cell carcinoma: Expression, function, and prognostic significance;citation_pages=22.e11-22.e21;citation_volume=33;citation_year=2015;citation_issue=1;citation_pmid=25284003;citation_doi=10.1016/j.urolonc.2014.08.015" /> <meta name="citation_reference" content="citation_journal_title=Semin Cancer Biol;citation_author=QK. Li;citation_author=CP. Pavlovich;citation_author=H. Zhang;citation_author=CR. Kinsinger;citation_author=DW. Chan;citation_title=Challenges and opportunities in the proteomic characterization of clear cell renal cell carcinoma (ccRCC): A critical step towards the personalized care of renal cancers;citation_pages=8-15;citation_volume=55;citation_year=2019;citation_pmid=30055950;citation_doi=10.1016/j.semcancer.2018.06.004" /> <meta name="citation_fulltext_world_readable" content="" /> <meta name="twitter:title" content="Comparative Proteomics of ccRCC Cell Lines to Identify Kidney Cancer Progression Factors" /> <meta name="twitter:card" content="summary_large_image" /> <meta name="twitter:image" content="https://cgp.iiarjournals.org/sites/default/files/highwire/cgp/21/6.cover-source.jpg" /> <meta name="twitter:description" content="Background/Aim: Clear cell renal cell carcinoma (ccRCC) is the most common type of kidney cancer, accounting for approximately 75% of kidney cancers. The objective of this study was to identify novel progression markers for ccRCC based on proteomics, with the goal of stage determination and early diagnosis of kidney cancer patients. Materials and Methods: We performed quantitative global proteomics coupled with Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) and high-resolution tandem mass spectrometry on kidney-derived cells, including HEK-293, 786-O (primary ccRCC), and Caki-1 (metastatic ccRCC) cells, to investigate the novel progression factors of ccRCC. Results: In this study, a total of 1,106 proteins were quantified. The Gene Ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were conducted for differentially expressed proteins (DEPs) that were increased in ccRCC cells compared to HEK-293 cells. Ultimately, 99 DEPs including 75 up-regulated and 24 down-regulated proteins, that were significantly altered in both ccRCC cells, were identified. Among DEPs, vimentin was identified as the most significantly changed protein. Its increased expression in ccRCC was verified through immunoblotting in ccRCC cell lines and immunohistochemistry in kidney tumors. Conclusion: From the global proteomics data detected in ccRCC, we propose 99 DEPs including vimentin as progression factors." /> <meta name="og-title" property="og:title" content="Comparative Proteomics of ccRCC Cell Lines to Identify Kidney Cancer Progression Factors" /> <meta name="og-url" property="og:url" content="https://cgp.iiarjournals.org/content/21/6/645" /> <meta name="og-site-name" property="og:site_name" content="Cancer Genomics & Proteomics" /> <meta name="og-description" property="og:description" content="Background/Aim: Clear cell renal cell carcinoma (ccRCC) is the most common type of kidney cancer, accounting for approximately 75% of kidney cancers. The objective of this study was to identify novel progression markers for ccRCC based on proteomics, with the goal of stage determination and early diagnosis of kidney cancer patients. Materials and Methods: We performed quantitative global proteomics coupled with Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) and high-resolution tandem mass spectrometry on kidney-derived cells, including HEK-293, 786-O (primary ccRCC), and Caki-1 (metastatic ccRCC) cells, to investigate the novel progression factors of ccRCC. Results: In this study, a total of 1,106 proteins were quantified. The Gene Ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were conducted for differentially expressed proteins (DEPs) that were increased in ccRCC cells compared to HEK-293 cells. Ultimately, 99 DEPs including 75 up-regulated and 24 down-regulated proteins, that were significantly altered in both ccRCC cells, were identified. Among DEPs, vimentin was identified as the most significantly changed protein. Its increased expression in ccRCC was verified through immunoblotting in ccRCC cell lines and immunohistochemistry in kidney tumors. Conclusion: From the global proteomics data detected in ccRCC, we propose 99 DEPs including vimentin as progression factors." /> <meta name="og-type" property="og:type" content="article" /> <meta name="og-image" property="og:image" content="https://cgp.iiarjournals.org/sites/default/files/highwire/cgp/21/6.cover-source.jpg" /> <link rel="shortlink" href="/node/30750" /> <link rel="shortcut icon" href="https://cgp.iiarjournals.org/sites/default/files/images/favicon.ico" type="image/vnd.microsoft.icon" /> <meta name="viewport" content="width=device-width, initial-scale=1" /> <title>Comparative Proteomics of ccRCC Cell Lines to Identify Kidney Cancer Progression Factors | Cancer Genomics & Proteomics</title> <link type="text/css" rel="stylesheet" href="/sites/default/files/advagg_css/css__QEy_BpbtMcsqv3xURK855GSs2fFjOibU10yA758Mn4c__NucWi_bEk5E3BNVDtTt2nhiPtE1A5I24YwRDQ2fojJ0__BUE-77oZ9b7ju8egUDRLeURapp069HUD6yhoj0q3uMw.css" media="all" /> <link type="text/css" rel="stylesheet" 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first" data-delta="0">JUHEE PARK</span>, <span class="highwire-citation-author" data-delta="1">HYUNCHAE SIM</span>, <span class="highwire-citation-author" data-delta="2">EUN HYE LEE</span>, <span class="highwire-citation-author" data-delta="3">BUM SOO KIM</span>, <span class="highwire-citation-author" data-delta="4">JAE-WOOK CHUNG</span>, <span class="highwire-citation-author" data-delta="5">YUN-SOK HA</span>, <span class="highwire-citation-author" data-delta="6">TAE GYUN KWON</span>, <span class="highwire-citation-author" data-delta="7">SANGKYU LEE</span> and <span class="highwire-citation-author" data-delta="8">JUN NYUNG LEE</span></span></div> <div class="highwire-cite-metadata"><span class="highwire-cite-metadata-journal highwire-cite-metadata">Cancer Genomics & Proteomics </span><span class="highwire-cite-metadata-date highwire-cite-metadata">November 2024, </span><span class="highwire-cite-metadata-volume highwire-cite-metadata">21 </span><span class="highwire-cite-metadata-issue highwire-cite-metadata">(6) </span><span class="highwire-cite-metadata-pages highwire-cite-metadata">645-652; </span><span class="highwire-cite-metadata-doi highwire-cite-metadata">DOI: https://doi.org/10.21873/cgp.20480 </span></div> <div class="highwire-cite-extras"><span class="highwire-foxycart-add-to-cart-ahah highwire-foxycart-add-to-cart-ahah" data-text="Add to Cart (%short-price)" data-apath="/cgp/21/6/645.atom" data-type="link" data-font-icon="" data-parent-id="30742"></span></div> </div> <div id="hw-article-author-popups-top-node-30750--6861370700" style="display: none;"><div class="author-tooltip-0"><div class="author-tooltip-name">JUHEE PARK </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>1</span>College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=JUHEE%2BPARK%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=PARK%20J&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3AJUHEE%2BPARK%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-1"><div class="author-tooltip-name">HYUNCHAE SIM </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>2</span>School of Pharmacy, Sungkyunkwan University, Suwon, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=HYUNCHAE%2BSIM%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=SIM%20H&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3AHYUNCHAE%2BSIM%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-2"><div class="author-tooltip-name">EUN HYE LEE </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>3</span>Joint Institute for Regenerative Medicine, Kyungpook National University, Daegu, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=EUN%2BHYE%2BLEE%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=LEE%20EH&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3AEUN%2BHYE%2BLEE%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-3"><div class="author-tooltip-name">BUM SOO KIM </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>4</span>Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=BUM%2BSOO%2BKIM%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=KIM%20BS&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3ABUM%2BSOO%2BKIM%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-4"><div class="author-tooltip-name">JAE-WOOK CHUNG </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>4</span>Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=JAE-WOOK%2BCHUNG%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=CHUNG%20J&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3AJAE-WOOK%2BCHUNG%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-5"><div class="author-tooltip-name">YUN-SOK HA </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>4</span>Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=YUN-SOK%2BHA%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=HA%20Y&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3AYUN-SOK%2BHA%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-6"><div class="author-tooltip-name">TAE GYUN KWON </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>4</span>Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=TAE%2BGYUN%2BKWON%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=KWON%20TG&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3ATAE%2BGYUN%2BKWON%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-7"><div class="author-tooltip-name">SANGKYU LEE </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>2</span>School of Pharmacy, Sungkyunkwan University, Suwon, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=SANGKYU%2BLEE%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=LEE%20S&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link"><a href="/search/author1%3ASANGKYU%2BLEE%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li><li class="author-corresp-email-link last"><span>For correspondence: <a href="mailto:sangkyu@skku.edu" class="" data-icon-position="" data-hide-link-title="0">sangkyu@skku.edu</a></span></li></ul></div><div class="author-tooltip-8"><div class="author-tooltip-name">JUN NYUNG LEE </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>4</span>Department of Urology, School of Medicine, Kyungpook National University, Daegu, Republic of Korea</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=JUN%2BNYUNG%2BLEE%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a 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src="https://cgp.iiarjournals.org/sites/all/modules/contrib/panels_ajax_tab/images/loading.gif" alt="Loading" title="Loading" /></div><div class="panels-ajax-tab-wrap-jnl_iiar_tab_art"><div class="panel-display panel-1col clearfix" > <div class="panel-panel panel-col"> <div><div class="panel-pane pane-highwire-markup" > <div class="pane-content"> <div class="highwire-markup"><div xmlns="http://www.w3.org/1999/xhtml" data-highwire-cite-ref-tooltip-instance="highwire_reflinks_tooltip" class="content-block-markup" xmlns:xhtml="http://www.w3.org/1999/xhtml"><div class="article fulltext-view "><span class="highwire-journal-article-marker-start"></span><div class="section abstract" id="abstract-1"><h2>Abstract</h2><p id="p-3">Background/Aim: Clear cell renal cell carcinoma (ccRCC) is the most common type of kidney cancer, accounting for approximately 75% of kidney cancers. The objective of this study was to identify novel progression markers for ccRCC based on proteomics, with the goal of stage determination and early diagnosis of kidney cancer patients. Materials and Methods: We performed quantitative global proteomics coupled with Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) and high-resolution tandem mass spectrometry on kidney-derived cells, including HEK-293, 786-O (primary ccRCC), and Caki-1 (metastatic ccRCC) cells, to investigate the novel progression factors of ccRCC. Results: In this study, a total of 1,106 proteins were quantified. The Gene Ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were conducted for differentially expressed proteins (DEPs) that were increased in ccRCC cells compared to HEK-293 cells. Ultimately, 99 DEPs including 75 up-regulated and 24 down-regulated proteins, that were significantly altered in both ccRCC cells, were identified. Among DEPs, vimentin was identified as the most significantly changed protein. Its increased expression in ccRCC was verified through immunoblotting in ccRCC cell lines and immunohistochemistry in kidney tumors. Conclusion: From the global proteomics data detected in ccRCC, we propose 99 DEPs including vimentin as progression factors.</p></div><span class="kwd-group-title">Key Words:</span><ul class="kwd-group"><li class="kwd"><a href="/keyword/clear-cell-renal-carcinoma" class="hw-term hw-article-keyword hw-article-keyword-clear-cell-renal-carcinoma" rel="nofollow">Clear cell renal carcinoma</a></li><li class="kwd"><a href="/keyword/comparative-proteomics" class="hw-term hw-article-keyword hw-article-keyword-comparative-proteomics" rel="nofollow">comparative proteomics</a></li><li class="kwd"><a href="/keyword/stable-isotope-labeling-amino-acids-cell-culture-silac" class="hw-term hw-article-keyword hw-article-keyword-stable-isotope-labeling-by-amino-acids-in-cell-culture-silac" rel="nofollow">Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC)</a></li><li class="kwd"><a href="/keyword/vimentin" class="hw-term hw-article-keyword hw-article-keyword-vimentin" rel="nofollow">vimentin</a></li></ul><p id="p-4">Renal cell carcinoma (RCC), a type of cancer that develops in the kidneys, is the most common kidney cancer accounting for 3% of all cancer diagnoses (<a id="xref-ref-1-1" class="xref-bibr" href="#ref-1">1</a>). In 2023, an estimated 81,800 new cases of kidney cancer were documented in the United States, with an approximately 14,890 deaths. The incidence rate has continued to rise annually by about 1% in men and women. RCC has various subtypes, with clear cell renal cell carcinoma (ccRCC) being the most common, accounting for 75-80% of cases (<a id="xref-ref-2-1" class="xref-bibr" href="#ref-2">2</a>). Patients with ccRCC tend to have a poorer prognosis than those with other RCC subtypes, and ccRCC is prone to lung, bone, and lymph node metastases (<a id="xref-ref-3-1" class="xref-bibr" href="#ref-3">3</a>). Locally occurring RCC can be treated with partial or radical nephrectomy, active surveillance, or ablation (<a id="xref-ref-4-1" class="xref-bibr" href="#ref-4">4</a>-<a id="xref-ref-6-1" class="xref-bibr" href="#ref-6">6</a>). However, despite undergoing kidney surgery, approximately 30% of patients with localized RCC eventually experience metastasis (<a id="xref-ref-7-1" class="xref-bibr" href="#ref-7">7</a>-<a id="xref-ref-9-1" class="xref-bibr" href="#ref-9">9</a>). Patients with metastatic RCC (mRCC) have a 5-year survival rate of less than 10% and a median survival period of 1.5 years, indicating poor prognosis (<a id="xref-ref-10-1" class="xref-bibr" href="#ref-10">10</a>, <a id="xref-ref-11-1" class="xref-bibr" href="#ref-11">11</a>).</p><p id="p-5">Furthermore, RCC is highly resistant to chemotherapy and has a low response rate to cytokine therapy, leading to treatment failure (<a id="xref-ref-12-1" class="xref-bibr" href="#ref-12">12</a>, <a id="xref-ref-13-1" class="xref-bibr" href="#ref-13">13</a>). Almost one-third of patients with RCC present with metastasis at the time of diagnosis which is attributed to nonspecific early-stage symptoms and lack of effective diagnostic methods (<a id="xref-ref-14-1" class="xref-bibr" href="#ref-14">14</a>).</p><p id="p-6">Proteomics can contribute to more comprehensive functional information than genomics or transcriptomics as it better reflects unknown physiological cellular states at the proteome level (<a id="xref-ref-15-1" class="xref-bibr" href="#ref-15">15</a>-<a id="xref-ref-17-1" class="xref-bibr" href="#ref-17">17</a>). Most modern proteomics studies have utilized mass spectrometry (MS)-based methods, due to their high sensitivity in protein detection and identification. In recent years, advancements in MS instruments and data analysis paved way for significant improvement in the field of proteomics (<a id="xref-ref-18-1" class="xref-bibr" href="#ref-18">18</a>). Specially, the utility of stable isotope labeling methods, that is, Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC), has provided significant flexibility in employing quantitative proteomic techniques to examine protein changes within complex samples (<a id="xref-ref-19-1" class="xref-bibr" href="#ref-19">19</a>). The combination of SILAC and high-resolution (HR) MS enables comparative global proteomics analysis offering extensive information on the proteomic characteristics of cancer progression.</p><p id="p-7">Early detection of most cancers can lead to high survival rates of up to 90% for 5- and even 10-year periods, whereas late-stage detection can strikingly reduce survival rates to 10% or lower (<a id="xref-ref-20-1" class="xref-bibr" href="#ref-20">20</a>). Thus, identifying candidate progression markers for cancer diagnosis and prognosis in clinical settings is crucial, as early cancer detection can provide significant benefits to patients (<a id="xref-ref-21-1" class="xref-bibr" href="#ref-21">21</a>, <a id="xref-ref-22-1" class="xref-bibr" href="#ref-22">22</a>). In this study, we labeled ccRCC cell lines using SILAC and identified differentially expressed proteins (DEPs) by HR MS-based proteomic analysis to uncover factors associated with ccRCC progression.</p><div class="section materials-methods" id="sec-1"><h2 class="">Materials and Methods</h2><p id="p-8"><em>Cell culture</em>. Three human ccRCC cell lines, including HEK-293, 786-O, and Caki-1, were used, and were all grown in high glucose containing Dulbecco modified Eagle medium (DMEM - high glucose) containing 10% fetal bovine serum (FBS, Hyclone, Marlborough, MA, USA) and 1% penicillin/streptomycin (Gibco, Waltham, MA, USA) at 37°C with 5% CO<sub>2</sub> in a humidified incubator. The cell culture medium was replaced every 2 days and harvested using 0.25% trypsin-EDTA. HEK-293 and Caki-1 cells were obtained from Korea Cell Line Bank and 786-O cell was purchased from ATCC (Manassas, VA, USA).</p><p id="p-9"><em>SILAC label and proteomics sample preparation</em>. For SILAC labeling, HEK-293 and 786-O cell lines were grown in SILAC medium (Thermo Fisher Scientific, Rockford, IL, USA) and isotope-labeled amino acids (CIL, Andover, MA, USA) were added in each medium with 10% FBS and 1% P/S. The cells grown in “heavy” medium were labeled with K8R10 (Lys8, <sup>13</sup>C<sub>6</sub>-<sup>15</sup>N<sub>2</sub>; Arg10, <sup>13</sup>C<sub>6</sub>-<sup>15</sup>N<sub>4</sub>), while those grown in “medium” were labeled with K4R6 (Lys4, D<sub>4</sub>; Arg6, <sup>13</sup>C<sub>6</sub>); a normal DMEM medium (K0R0) was used for cells grown in “light”. Each cell was cultured at least five times in 150-mm cell culture dishes (Corning, NY, USA), and SILAC labeling efficiency test was performed. After assessing that the labeling efficiency was over 98%, the cells including light, medium, and heavy medium were grown in sufficient quantities for use in the next experiment. Each labeled cell was prepared in biological triplicates. All cell lines were grown to approximately 85% confluence in 150-mm cell culture dishes and harvested for use in the experiment, and the cell pellets were stored at −80°C until use.</p><p id="p-10">The frozen cell pellets were dissolved using a radio-immunoprecipitation assay (RIPA) buffer (Thermo Fisher Scientific) including the Halt protease inhibitor cocktail (Thermo Fisher Scientific). Samples were sonicated five times each, centrifuged at 4°C (12,000 × <em>g</em> for 10 min), and the supernatant was collected from centrifuged samples and transferred to new tubes. Protein concentration was measured using the bicinchoninic acid colorimetric assay kit (Thermo Fisher Scientific). For the reduction and alkylation, 150-mM dithiothreitol was added into each sample for reduction and incubated at 56°C for 30 min in a shaking incubator, and then a 600-mM iodoacetamide was added for alkylation in the dark for 30 min at room temperature (RT). Next, 10% trichloroacetic acid was added to purify the lysed proteins at 4°C for 4 h and the protein pellets were washed twice using ice-cold acetone after the protein samples were centrifuged. Prior to adding trypsin, 50-mM ammonium bicarbonate was added and repeatedly vortexed and sonicated to re-dissolve. Trypsin was added to re-dissolved protein samples to digest proteins with a ratio of 1:50 (trypsin:protein) and incubated at 37°C overnight after measuring the pH. Lastly, 10% trifluoroacetic acid was added to quench the digestion and centrifugation was performed to extract the supernatant. The peptide samples were dried in speed-vac and kept at −80°C until use.</p><p id="p-11"><em>nanoHPLC and Mass spectrometric analysis</em>. Before analysis, peptides were desalted using C18 resin-packed Zip-Tip (Millipore, Burlington, MA, USA). The desalted peptide was separated using a NanoLC-Ultra HPLC (Eksigent Technology, Dublin, CA, USA) connected to a homemade column packed with Jupiter Proteo (Phenomenex, Torrance, CA, USA). The column was equipped with an NSI Ion Source (Thermo Fisher Scientific, Waltham, MA, USA). For the mobile phase, 0.1% formic acid containing water and acetonitrile were used as solvents A and B, respectively. A linear gradient of 3%-23% solvent B for 50 min, with a flow rate of 300 nl/min, was used for every sample. The eluted peptides were analyzed using LTQ Orbitrap Velos MS/MS instrument (Thermo Fisher Scientific, Waltham, MA, USA). The ionization source voltage was set to 1.8 kV, and the capillary temperature was 300°C. In tandem MS scans, data-dependent analysis (DDA) scans were acquired, and the top 10 most abundant peptide precursor ions in the range of 300–2,000 m/z were fragmented <em>via</em> collision-induced dissociation (CID) of 28% normalized collision energy (NCE). The MS/MS proteomic data have been deposited to the ProteomeXchange Consortium <em>via</em> the PRIDE (<a id="xref-ref-23-1" class="xref-bibr" href="#ref-23">23</a>) partner repository with the dataset identifier PXD045898.</p><p id="p-12"><em>Peak alignment and bioinformatics</em>. To match MS/MS spectra against identified proteins from the Uniprot human reference proteome database (Release 2021_02), the MaxQuant (version 1.6.10.43) search engine was used. Labels Arg6 and Lys4 for “medium” and Arg10 and Lys8 for “heavy” were set to quantify the proteins. Oxidation (M) and Acetyl (Protein N-term) were set as variables, and Carbamidomethyl (C) was a fixed modification. Trypsin/P was set as a digest enzyme with a specific mode. The precursor peptide tolerance was set to 20 ppm and revert decoy mode was employed. The false discovery rate (FDR) was set to 0.01 and 40 for the andromeda score for identification.</p><p id="p-13">Three comparison groups were used for comparative proteomics analysis, differentially expressed protein (DEPs were defined as fold change (FC), which was calculated from a ratio of intensity in each labeling within the same protein group. To measure the linear correlation between biological replications, the Pearson correlation coefficient was performed. Protein groups that have an absolute value of log2 transformed FC ≥1 were picked up and performed Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis through the DAVID functional annotation tool. DEPs were adjusted to z-scoring and then clustered into five types using the hierarchical clustering algorithm, and trends were visualized using the graphical representation heatmap technique in the Perseus software platform (version 2.1.4.0). The volcano plot visualized through the log2 transformed FC complied with both-sided student’s <em>t</em>-test <em>p</em>-value, with statistical significance set as <em>p</em><0.05.</p><p id="p-14"><em>Western blotting to validate quantitative proteome data</em>. The pellet of ccRCC SILAC cell lines were sonicated and dissolved using RIPA buffer containing Halt protease inhibitor cocktail (Thermo Fisher Scientific, Rockford, IL, USA) to extract proteins. Next, 5-μg of proteins was separated <em>via</em> 10% sodium dodecyl-sulfate polyacrylamide gel electrophoresis gel for 90 min and transferred onto polyvinylidene difluoride membrane for 110 min. After completing the transfer step, the membranes were blocked using 5% BSA in TBST for 2 h at RT and then incubated with the primary antibodies in 5% BSA at 4°C overnight. Vimentin and β-actin were used as the primary antibodies and diluted at 1:2,000 and 1:1,000, respectively. The membranes were washed three times with TBST every 10 min. The second antibody was diluted at 1:2,000 in 5% BSA and incubated at RT for 2 h. Thereafter, the membrane was washed with TBST again three times every 10 min, and the protein bands were detected using ECL™ prime western blotting detection reagents (Cytiva, Buckinghamshire, UK) to visualize the bands. Finally, we analyzed the signal using iBright 1500 (Thermo, Waltham, MA, USA).</p><p id="p-15"><em>Immunohistochemistry (IHC)</em>. In this study, the biosamples used were provided by the Kyungpook National University Chilgok Hospital (the patient’s consent was obtained prior to procurement of all tumor tissues, IRB KNUCH 2016-05-021-020) and were stored at 80°C until required. For IHC, tissues were fixed in 4% formaldehyde and formed into paraffin blocks. Then, sections were cut into 4-um thickness and attached to coated glass slides. Sections underwent antigen retrieval and blocked in citrated antigen retrieval buffer and 5% BSA after deparaffinization and hydration, respectively. The primary antibody (Abcam) was diluted as per manufacturer’s recommendations and used at 4°C for 18 h. A secondary antibody (1:1,000) was applied for 1 h at RT. Sections were dehydrated and cleared using alcohol and xylene and then mounted with 4′,6-diamidino-2-phenylindole (DAPI) in a mounting medium.</p></div><div class="section results" id="sec-2"><h2 class="">Results</h2><p id="p-16"><em>Comparative proteomics analysis of ccRCC cell lines</em>. We analyzed proteins using comparative proteomic analysis, analysis was performed to identify proteins involved in cancer progression in ccRCC cell lines (<a id="xref-fig-1-1" class="xref-fig" href="#F1">Figure 1A</a>). In this study, three subtypes of RCC cells, such as HEK-293, 786-O, and Caki-1, were selected. HEK-293, a cell line isolated from the kidneys of human embryos, was used as the normal group in this experiment, while 786-O and Caki-1 cells were used as model cells representing primary and metastatic ccRCC, respectively (<a id="xref-ref-24-1" class="xref-bibr" href="#ref-24">24</a>). Samples were analyzed using HR MS, and peak alignments were performed in MaxQuant (v.1.6.10.43, <a href="https://www.maxquant.org/">https://www.maxquant.org/</a>) against a <em>Homo sapiens</em> database (Uniprot, uploaded December 2018) with an FDR ≤1% and score ≥40. In total, 1,448 proteins were identified, and 1,106 proteins were quantified. Among them, there were 347 DEPs in 786-O <em>vs.</em> HEK-293, 345 DEPs in Caki-1 <em>vs.</em> HEK-293, and 89 DEPs in Caki-1 <em>vs.</em> 786-O (<a id="xref-fig-1-2" class="xref-fig" href="#F1">Figure 1B</a>). Proteins demonstrating a ratio ≥2.0 were considered up-regulated, while those with a ratio of ≤0.5 were classified as down-regulated. Pearson correlation coefficient values were used to examine the technical coefficients in biological triplicates for the SILAC-tagged ratio.</p><div id="F1" class="fig pos-float odd"><div class="highwire-figure"><div class="fig-inline-img-wrapper"><div class="fig-inline-img"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F1.large.jpg?width=800&height=600&carousel=1" title="Overview workflow and result of quantitative proteomic analysis. (A) Experimental layout of SILAC labeling in clear cell renal cell carcinoma (ccRCC) cell lines and global proteomic analysis by liquid chromatography-mass spectrometry. (B) The number of DEPs in ccRCC cell lines. Heavy, SILAC medium labeled with K8R10 (Lys8, 13C6–15N2; Arg10, 13C6–15N4); medium, SILAC medium labeled with K4R6 (Lys4, D4; Arg6, 13C6); and light, normal Dulbecco modified Eagle medium (K0R0). This experiment was performed in biological triplicates. DEPs: Differentially expressed proteins; SILAC: stable isotope labeling by amino acids in cell culture." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-1437670056" data-figure-caption="<div class="highwire-markup"><div xmlns="http://www.w3.org/1999/xhtml">Overview workflow and result of quantitative proteomic analysis. (A) Experimental layout of SILAC labeling in clear cell renal cell carcinoma (ccRCC) cell lines and global proteomic analysis by liquid chromatography-mass spectrometry. (B) The number of DEPs in ccRCC cell lines. Heavy, SILAC medium labeled with K8R10 (Lys8, <sup>13</sup>C<sub>6</sub>–<sup>15</sup>N<sub>2</sub>; Arg10, <sup>13</sup>C<sub>6</sub>–<sup>15</sup>N<sub>4</sub>); medium, SILAC medium labeled with K4R6 (Lys4, D<sub>4</sub>; Arg6, <sup>13</sup>C<sub>6</sub>); and light, normal Dulbecco modified Eagle medium (K0R0). This experiment was performed in biological triplicates. DEPs: Differentially expressed proteins; SILAC: stable isotope labeling by amino acids in cell culture.</div></div>" data-icon-position="" data-hide-link-title="0"><span class="hw-responsive-img"><img class="highwire-fragment fragment-image lazyload" alt="Figure 1." src="data:image/gif;base64,R0lGODlhAQABAIAAAAAAAP///yH5BAEAAAAALAAAAAABAAEAAAIBRAA7" data-src="https://cgp.iiarjournals.org/content/cgp/21/6/645/F1.medium.gif" width="440" height="308"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 1." src="https://cgp.iiarjournals.org/content/cgp/21/6/645/F1.medium.gif" width="440" height="308"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F1.large.jpg?download=true" class="highwire-figure-link highwire-figure-link-download" title="Download Figure 1." data-icon-position="" data-hide-link-title="0">Download figure</a></li><li class="new-tab"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F1.large.jpg" class="highwire-figure-link highwire-figure-link-newtab" target="_blank" data-icon-position="" data-hide-link-title="0">Open in new tab</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/30777" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div><div class="fig-caption" xmlns:xhtml="http://www.w3.org/1999/xhtml"><span class="fig-label">Figure 1.</span> <p id="p-17" class="first-child">Overview workflow and result of quantitative proteomic analysis. (A) Experimental layout of SILAC labeling in clear cell renal cell carcinoma (ccRCC) cell lines and global proteomic analysis by liquid chromatography-mass spectrometry. (B) The number of DEPs in ccRCC cell lines. Heavy, SILAC medium labeled with K8R10 (Lys8, <sup>13</sup>C<sub>6</sub>–<sup>15</sup>N<sub>2</sub>; Arg10, <sup>13</sup>C<sub>6</sub>–<sup>15</sup>N<sub>4</sub>); medium, SILAC medium labeled with K4R6 (Lys4, D<sub>4</sub>; Arg6, <sup>13</sup>C<sub>6</sub>); and light, normal Dulbecco modified Eagle medium (K0R0). This experiment was performed in biological triplicates. DEPs: Differentially expressed proteins; SILAC: stable isotope labeling by amino acids in cell culture.</p><div class="sb-div caption-clear"></div></div></div><p id="p-18">Next, unsupervised hierarchical clustering of the quantitative protein data was performed to produce protein clusters with similar patterns among RCC cell lines (<a id="xref-fig-2-1" class="xref-fig" href="#F2">Figure 2</a>). The quantitative ratio of DEPs was re-normalized using the Z-score. Based on the clustering analysis conducted for each cell line, five groups (A-E) were generated that contained 71, 199, 104, 358, and 374 DEPs. Among the five clusters, we focused on Cluster B, which was sequentially increased in 786-O and Caki-1 cells compared to HEK-293. Proteins in Cluster B correlate with the progression from primary to metastatic ccRCC.</p><div id="F2" class="fig pos-float odd"><div class="highwire-figure"><div class="fig-inline-img-wrapper"><div class="fig-inline-img"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F2.large.jpg?width=800&height=600&carousel=1" title="Unsupervised hierarchical clustering of proteins altered among ccRCC cell lines. (A) Cluster analysis and patterns with each group. (B) Functional enrichment analysis of proteins in Cluster B." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-1437670056" data-figure-caption="<div class="highwire-markup">Unsupervised hierarchical clustering of proteins altered among ccRCC cell lines. (A) Cluster analysis and patterns with each group. (B) Functional enrichment analysis of proteins in Cluster B.</div>" data-icon-position="" data-hide-link-title="0"><span class="hw-responsive-img"><img class="highwire-fragment fragment-image lazyload" alt="Figure 2." src="data:image/gif;base64,R0lGODlhAQABAIAAAAAAAP///yH5BAEAAAAALAAAAAABAAEAAAIBRAA7" data-src="https://cgp.iiarjournals.org/content/cgp/21/6/645/F2.medium.gif" width="404" height="440"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 2." src="https://cgp.iiarjournals.org/content/cgp/21/6/645/F2.medium.gif" width="404" height="440"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F2.large.jpg?download=true" class="highwire-figure-link highwire-figure-link-download" title="Download Figure 2." data-icon-position="" data-hide-link-title="0">Download figure</a></li><li class="new-tab"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F2.large.jpg" class="highwire-figure-link highwire-figure-link-newtab" target="_blank" data-icon-position="" data-hide-link-title="0">Open in new tab</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/30768" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div><div class="fig-caption"><span class="fig-label">Figure 2.</span> <p id="p-19" class="first-child">Unsupervised hierarchical clustering of proteins altered among ccRCC cell lines. (A) Cluster analysis and patterns with each group. (B) Functional enrichment analysis of proteins in Cluster B.</p><div class="sb-div caption-clear"></div></div></div><p id="p-20">In GO and KEGG enrichment analysis using DAVID to understand the potential functional implications of the DEPs identified in Cluster B, we selected the top two terms with respect to biological process (GOBP), cellular component (GOCC), molecular function (GOMF), and KEGG (<a id="xref-fig-2-2" class="xref-fig" href="#F2">Figure 2</a>). The GOBP showed that proteins in Cluster B were involved in proteasome-mediated ubiquitin-dependent protein catabolic process and tumor necrosis factor-mediated signaling pathway categories. In the GOMF analysis, manganese ion binding and metallopeptidase activity were enriched in Cluster B. For the KEGG pathway enrichment analysis, the proteins in Cluster B were mainly associated with proteasomes and phagosomes.</p><p id="p-21"><em>Characterization of ccRCC progression markers</em>. To investigate the proteins involved in the progression to cancer and metastasis, we compared RCC and mRCC cell lines with their respective control cell line. We identified significantly differentially expressed proteins (sDEPs) in the 786-O <em>vs.</em> HEK-293 and Caki-1 <em>vs.</em> HEK-293 groups, respectively, and these findings were visualized using volcano plots (<a id="xref-fig-3-1" class="xref-fig" href="#F3">Figure 3A</a>) sDEPs were filtered using a criterion of <em>p</em><0.05 and a change in expression greater than or equal to two-fold (log2 scale ≤1 and ≥1). First, 160 sDEPs were identified between 786-O and HEK-293 cells, with 119 proteins being up-regulated and 41 proteins being down-regulated. A total of 162 sDEPs were identified between Caki-1and HEK-293 cells, with 105 up-regulated and 56 down-regulated, respectively. There were 75 commonly up-regulated sDEPs and 24 common down-regulated sDEPs in 786-O and Caki-1 cells compared to HEK-293 cells.</p><div id="F3" class="fig pos-float odd"><div class="highwire-figure"><div class="fig-inline-img-wrapper"><div class="fig-inline-img"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F3.large.jpg?width=800&height=600&carousel=1" title="Validation of expression levels of vimentin in cell and tissue samples. (A) Volcano plot results of DEPs in 786-O vs. HEK-293 and Caki-1 vs. HEK-293 cells. (B) Immunoblotting assay result for vimentin and the expression ratio compared to β-actin in each cell line. (B) The results represent the vimentin expression levels in each tissue sample through immunochemical staining. (Normal, T1G3, T3G3, and mRCC). Blue: DAPI; red: vimentin. DEPs: Differentially expressed proteins." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-1437670056" data-figure-caption="<div class="highwire-markup">Validation of expression levels of vimentin in cell and tissue samples. (A) Volcano plot results of DEPs in 786-O vs. HEK-293 and Caki-1 vs. HEK-293 cells. (B) Immunoblotting assay result for vimentin and the expression ratio compared to β-actin in each cell line. (B) The results represent the vimentin expression levels in each tissue sample through immunochemical staining. (Normal, T1G3, T3G3, and mRCC). Blue: DAPI; red: vimentin. DEPs: Differentially expressed proteins.</div>" data-icon-position="" data-hide-link-title="0"><span class="hw-responsive-img"><img class="highwire-fragment fragment-image lazyload" alt="Figure 3." src="data:image/gif;base64,R0lGODlhAQABAIAAAAAAAP///yH5BAEAAAAALAAAAAABAAEAAAIBRAA7" data-src="https://cgp.iiarjournals.org/content/cgp/21/6/645/F3.medium.gif" width="440" height="428"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 3." src="https://cgp.iiarjournals.org/content/cgp/21/6/645/F3.medium.gif" width="440" height="428"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F3.large.jpg?download=true" class="highwire-figure-link highwire-figure-link-download" title="Download Figure 3." data-icon-position="" data-hide-link-title="0">Download figure</a></li><li class="new-tab"><a href="https://cgp.iiarjournals.org/content/cgp/21/6/645/F3.large.jpg" class="highwire-figure-link highwire-figure-link-newtab" target="_blank" data-icon-position="" data-hide-link-title="0">Open in new tab</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/30764" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div><div class="fig-caption"><span class="fig-label">Figure 3.</span> <p id="p-22" class="first-child">Validation of expression levels of vimentin in cell and tissue samples. (A) Volcano plot results of DEPs in 786-O vs. HEK-293 and Caki-1 vs. HEK-293 cells. (B) Immunoblotting assay result for vimentin and the expression ratio compared to β-actin in each cell line. (B) The results represent the vimentin expression levels in each tissue sample through immunochemical staining. (Normal, T1G3, T3G3, and mRCC). Blue: DAPI; red: vimentin. DEPs: Differentially expressed proteins.</p><div class="sb-div caption-clear"></div></div></div><p id="p-23">To explore ccRCC progression markers, we focused on sDEPs that were frequently increased in 786-O and Caki-1 cells compared to HEK-293, among which vimentin (VIM) was most significantly increased in 786-O and Caki-1 cells. The top 25 proteins were selected based on the ratio between 786-O and HEK-293 cells and were shown in <a id="xref-table-wrap-1-1" class="xref-table" href="#T1">Table I</a>. Following vimentin (VIM), annexin A2 (ANXA2) and A4 (ANXA4) were increased, followed by aldo–keto reductase family 1 member B1 (AKR1B1), which was also up-regulated in both cells.</p><div id="T1" class="table pos-float"><div class="table-inline table-callout-links"><div class="callout"><span>View this table:</span><ul class="callout-links"><li class="view-inline first"><a href="" class="table-expand-inline" data-table-url="/highwire/markup/30760/expansion?postprocessors=highwire_tables%2Chighwire_reclass%2Chighwire_figures%2Chighwire_math%2Chighwire_inline_linked_media%2Chighwire_embed&table-expand-inline=1" data-icon-position="" data-hide-link-title="0">View inline</a></li><li class="view-popup"><a href="/highwire/markup/30760/expansion?width=1000&height=500&iframe=true&postprocessors=highwire_tables%2Chighwire_reclass%2Chighwire_figures%2Chighwire_math%2Chighwire_inline_linked_media%2Chighwire_embed" class="colorbox colorbox-load table-expand-popup" rel="gallery-fragment-tables" data-icon-position="" data-hide-link-title="0">View popup</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/30760" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div></div><div class="table-caption"><span class="table-label">Table I.</span> <p id="p-24" class="first-child">A list of top 25 proteins commonly increased in 786-O and Caki-1 compared to HEK-293 cells.</p><div class="sb-div caption-clear"></div></div></div><p id="p-25"><em>Verification of DEPs in ccRCC cell lines and RCC tissue</em>. In both groups, vimentin was identified among the proteins with the largest FC. To determine its association with cancer progression, validation experiments were conducted in the ccRCC cell lines and RCC tissue (<a id="xref-fig-3-2" class="xref-fig" href="#F3">Figure 3B</a> and <a id="xref-fig-3-3" class="xref-fig" href="#F3">C</a>). Immunoblotting analysis was performed to verify vimentin expression in each cell line. The results showed increased vimentin expression in 786-O compared to HEK-293 and an increase in Caki-1. Moreover, the immunoblotting results from three replicates confirmed increased expression in 786-O and Caki-1 cells (<a id="xref-fig-3-4" class="xref-fig" href="#F3">Figure 3B</a>). In RCC tissue, we performed IHC to correlate vimentin expression in patient tissue samples, IHC was performed: normal, T1G3, T3G3, and mRCC. As the tumor grade increased, the strong signals of positive cells for vimentin were increased in the mRCC group; the strongest positive reactivity and the highest number of positive cells were observed.</p></div><div class="section discussion" id="sec-3"><h2 class="">Discussion</h2><p id="p-26">Vimentin is a major constituent of the intermediate filament family of proteins, and its overexpression in cancer is associated with increased tumor growth, invasion, and poor prognosis (<a id="xref-ref-25-1" class="xref-bibr" href="#ref-25">25</a>). In prostate cancer, vimentin was found to be overexpressed in prostate cancer cell lines CL1 and PC-3M-1E8 which are linked in heightened cell invasiveness (<a id="xref-ref-26-1" class="xref-bibr" href="#ref-26">26</a>, <a id="xref-ref-27-1" class="xref-bibr" href="#ref-27">27</a>). The correlation between high vimentin expression and increased cancer cell migration and invasion has been established in various cancer types (<a id="xref-ref-25-2" class="xref-bibr" href="#ref-25">25</a>). Additionally, the effects of vimentin overexpression on cancer have been evaluated not only in cell lines but also in human patients where it has been associated with reduced survival, particularly in cases with metastasis. For example, in non-small-cell lung cancer (NSCLC), vimentin is known to regulate invasiveness (<a id="xref-ref-28-1" class="xref-bibr" href="#ref-28">28</a>) and its overexpression was identified as an independent prognosticator for poor survival in patients with resected NSCLC (<a id="xref-ref-29-1" class="xref-bibr" href="#ref-29">29</a>). Given the role of vimentin in other cancers, we hypothesized that vimentin overexpression in ccRCC may also be important in RCC progression.</p><p id="p-27">Although vimentin was the most commonly increased proteins in the ccRCC cell lines identified by quantitative proteomics analysis, annexin A2 was the second most increased protein. Annexins are a family of calcium-regulated phospholipids-binding proteins widely expressed in various cell and tissue types (<a id="xref-ref-30-1" class="xref-bibr" href="#ref-30">30</a>). A total of 12 annexin proteins exist in humans, and annexin A2 is the one most extensively studied, and found to be involved in diverse cell functions and processes, such as cell exocytosis, endocytosis, migration, and proliferation. In previous studies, an increased annexin A2 expression has been found in RCC, which has been found to promote RCC migration, invasion, and proliferation (<a id="xref-ref-31-1" class="xref-bibr" href="#ref-31">31</a>-<a id="xref-ref-33-1" class="xref-bibr" href="#ref-33">33</a>). Although annexin A2 was not directly evaluated for increased expression through immunoblotting in this study, as vimentin was, dy, it is well recognized as a factor involved in RCC progression.</p><p id="p-28">Given that ccRCC is the most common type of kidney cancer, accounting for approximately 75% of kidney cancers, various omics studies are being conducted to understand the underlying mechanisms of cancer progression, establish early diagnostic markers, and discover potential therapeutic targets (<a id="xref-ref-34-1" class="xref-bibr" href="#ref-34">34</a>). In this study, we identified a total of 1,448 proteins and quantified 1,106 proteins in SILAC-labeled cell lines derived from kidneys, such as HEK-293, 786-O, and Caki-1 cells based on MS-based proteomic analysis. To explore progression factors in kidney cancer, we ultimately identified 99 DEPs that were significantly altered in 786-O and Caki-1 cells. In conclusion, we propose 99 DEPs including vimentin as potential modulators of ccRCC progression. However, in this study, only vimentin, the most significantly increased protein, was validated by immunoblotting. Further studies are needed to investigate the molecular regulatory mechanisms of vimentin in the progression of ccRCC.</p></div><div class="section ack" id="ack-1"><h2 class="">Acknowledgements</h2><p id="p-35">This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (2019R1A2C1004046) (2021R1G1A1092985) (2022R1I1A3069482) (2023R1A2C3003807), by the Korean Fund for Regenerative Medicine (KFRM) grant funded by the Korea government (the Ministry of Science and ICT, the Ministry of Health & Welfare) (23A0206L1), and the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare (HR22C1832).</p></div><div class="section fn-group" id="fn-group-1"><h2>Footnotes</h2><ul><li class="fn" id="fn-1"><p id="p-1"><a class="rev-xref" href="#xref-fn-1-1">↵</a><span class="fn-label">*</span> These Authors contributed equally to this study.</p></li><li class="fn" id="fn-2"><p id="p-29"><strong>Data and Material Availability</strong></p><p id="p-30">Data are available <em>via</em> ProteomeXchange with identifier PXD045898.</p></li><li class="fn" id="fn-3"><p id="p-31"><strong>Conflicts of Interest</strong></p><p id="p-32">The Authors declare no conflicts of interest.</p></li><li class="fn" id="fn-4"><p id="p-33"><strong>Authors’ Contributions</strong></p><p id="p-34">Conceptualization: Park, J., Lee, S. and Lee, J.N.; Methodology and analysis: Park, J., Sim, H., and Lee, E.H.; Resources: Lee, J. N.; Data curation: Park, J., Sim, H., and Lee, S.; Writing: Park, J., Lee, E.H., Lee, S. and Lee, J.N.; Funding acquisition: Kim, B.S., Kwon, T.G. and Lee, J.N.</p></li></ul></div><ul class="history-list"><li xmlns:hwp="http://schema.highwire.org/Journal" class="received" hwp:start="2024-04-05"><span class="received-label">Received </span>April 5, 2024.</li><li xmlns:hwp="http://schema.highwire.org/Journal" class="rev-recd" hwp:start="2024-08-11"><span class="rev-recd-label">Revision received </span>August 11, 2024.</li><li xmlns:hwp="http://schema.highwire.org/Journal" class="accepted" hwp:start="2024-08-20"><span class="accepted-label">Accepted </span>August 20, 2024.</li></ul><ul class="copyright-statement"><li class="fn" id="copyright-statement-1">Copyright © 2024, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved</li></ul><div class="license" id="license-1"><p id="p-2">This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (<a href="https://creativecommons.org/licenses/by-nc-nd/4.0" rel="license">https://creativecommons.org/licenses/by-nc-nd/4.0</a>).</p></div><div class="section ref-list" id="ref-list-1"><h2 class="">References</h2><ol class="cit-list"><li><a class="rev-xref-ref" href="#xref-ref-1-1" title="View reference 1 in text" id="ref-1">↵</a><div class="cit ref-cit ref-journal" id="cit-21.6.645.1" data-doi="10.3322/caac.21763"><div class="cit-metadata"><ol class="cit-auth-list"><li><span class="cit-auth"><span class="cit-name-surname">Siegel</span> <span class="cit-name-given-names">RL</span></span>, </li><li><span class="cit-auth"><span class="cit-name-surname">Miller</span> <span class="cit-name-given-names">KD</span></span>, </li><li><span 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