Melanoma cells undergo aggressive coalescence in a 3D Matrigel model that is repressed by anti-CD44
Using unique computer-assisted 3D reconstruction software, it was previously demonstrated that tumorigenic cell lines derived from breast tumors, when seeded in a 3D Matrigel model, grew as clonal aggregates which, after approximately 100 hours, underwent coalescence mediated by specialized cells, e...
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| Veröffentlicht in: | PloS one 2017-03, Vol.12 (3), p.e0173400-e0173400 |
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| creator | Wessels, Deborah Lusche, Daniel F Voss, Edward Kuhl, Spencer Buchele, Emma C Klemme, Michael R Russell, Kanoe B Ambrose, Joseph Soll, Benjamin A Bossler, Aaron Milhem, Mohammed Goldman, Charles Soll, David R |
| description | Using unique computer-assisted 3D reconstruction software, it was previously demonstrated that tumorigenic cell lines derived from breast tumors, when seeded in a 3D Matrigel model, grew as clonal aggregates which, after approximately 100 hours, underwent coalescence mediated by specialized cells, eventually forming a highly structured large spheroid. Non-tumorigenic cells did not undergo coalescence. Because histological sections of melanomas forming in patients suggest that melanoma cells migrate and coalesce to form tumors, we tested whether they also underwent coalescence in a 3D Matrigel model. Melanoma cells exiting fragments of three independent melanomas or from secondary cultures derived from them, and cells from the melanoma line HTB-66, all underwent coalescence mediated by specialized cells in the 3D model. Normal melanocytes did not. However, coalescence of melanoma cells differed from that of breast-derived tumorigenic cell lines in that they 1) coalesced immediately, 2) underwent coalescence as individual cells as well as aggregates, 3) underwent coalescence far faster and 4) ultimately formed long, flat, fenestrated aggregates that were extremely dynamic. A screen of 51 purified monoclonal antibodies (mAbs) targeting cell surface-associated molecules revealed that two mAbs, anti-beta 1 integrin/(CD29) and anti-CD44, blocked melanoma cell coalescence. They also blocked coalescence of tumorigenic cells derived from a breast tumor. These results add weight to the commonality of coalescence as a characteristic of tumorigenic cells, as well as the usefulness of the 3D Matrigel model and software for both investigating the mechanisms regulating tumorigenesis and screening for potential anti-tumorigenesis mAbs. |
| doi_str_mv | 10.1371/journal.pone.0173400 |
| format | Article |
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Non-tumorigenic cells did not undergo coalescence. Because histological sections of melanomas forming in patients suggest that melanoma cells migrate and coalesce to form tumors, we tested whether they also underwent coalescence in a 3D Matrigel model. Melanoma cells exiting fragments of three independent melanomas or from secondary cultures derived from them, and cells from the melanoma line HTB-66, all underwent coalescence mediated by specialized cells in the 3D model. Normal melanocytes did not. However, coalescence of melanoma cells differed from that of breast-derived tumorigenic cell lines in that they 1) coalesced immediately, 2) underwent coalescence as individual cells as well as aggregates, 3) underwent coalescence far faster and 4) ultimately formed long, flat, fenestrated aggregates that were extremely dynamic. A screen of 51 purified monoclonal antibodies (mAbs) targeting cell surface-associated molecules revealed that two mAbs, anti-beta 1 integrin/(CD29) and anti-CD44, blocked melanoma cell coalescence. They also blocked coalescence of tumorigenic cells derived from a breast tumor. These results add weight to the commonality of coalescence as a characteristic of tumorigenic cells, as well as the usefulness of the 3D Matrigel model and software for both investigating the mechanisms regulating tumorigenesis and screening for potential anti-tumorigenesis mAbs.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0173400</identifier><identifier>PMID: 28264026</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aggregates ; Antibodies, Monoclonal - pharmacology ; Biology ; Biology and Life Sciences ; Biomarkers ; Biotechnology ; Breast ; Breast cancer ; Cancer cells ; CD29 antigen ; CD44 antigen ; Cell Adhesion ; Cell Line ; Cell migration ; Cell surface ; Cell Tracking ; Coalescence ; Coalescing ; Collagen ; Commonality ; Computer programs ; Dosage and administration ; Drug Combinations ; Forming ; Genetic aspects ; Humans ; Hyaluronan Receptors - metabolism ; Integrin beta1 - metabolism ; Laminin ; Medicine and Health Sciences ; Melanocytes ; Melanocytes - metabolism ; Melanoma ; Melanoma - metabolism ; Melanoma - pathology ; Metastasis ; Microscopy ; Monoclonal antibodies ; Phenotype ; Proteoglycans ; Research and Analysis Methods ; Spheroids, Cellular ; Studies ; Three dimensional models ; Tumor Cells, Cultured ; Tumorigenesis ; Tumors</subject><ispartof>PloS one, 2017-03, Vol.12 (3), p.e0173400-e0173400</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Wessels et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2017 Wessels et al 2017 Wessels et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c655t-b7c591307fbc768837c973d2e4e2d96e5f5c3cc257c12dcbfd493f73630fcc8b3</citedby><cites>FETCH-LOGICAL-c655t-b7c591307fbc768837c973d2e4e2d96e5f5c3cc257c12dcbfd493f73630fcc8b3</cites><orcidid>0000-0002-5059-0315</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5338862/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5338862/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28264026$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Slominski, Andrzej T.</contributor><creatorcontrib>Wessels, Deborah</creatorcontrib><creatorcontrib>Lusche, Daniel F</creatorcontrib><creatorcontrib>Voss, Edward</creatorcontrib><creatorcontrib>Kuhl, Spencer</creatorcontrib><creatorcontrib>Buchele, Emma C</creatorcontrib><creatorcontrib>Klemme, Michael R</creatorcontrib><creatorcontrib>Russell, Kanoe B</creatorcontrib><creatorcontrib>Ambrose, Joseph</creatorcontrib><creatorcontrib>Soll, Benjamin A</creatorcontrib><creatorcontrib>Bossler, Aaron</creatorcontrib><creatorcontrib>Milhem, Mohammed</creatorcontrib><creatorcontrib>Goldman, Charles</creatorcontrib><creatorcontrib>Soll, David R</creatorcontrib><title>Melanoma cells undergo aggressive coalescence in a 3D Matrigel model that is repressed by anti-CD44</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Using unique computer-assisted 3D reconstruction software, it was previously demonstrated that tumorigenic cell lines derived from breast tumors, when seeded in a 3D Matrigel model, grew as clonal aggregates which, after approximately 100 hours, underwent coalescence mediated by specialized cells, eventually forming a highly structured large spheroid. Non-tumorigenic cells did not undergo coalescence. Because histological sections of melanomas forming in patients suggest that melanoma cells migrate and coalesce to form tumors, we tested whether they also underwent coalescence in a 3D Matrigel model. Melanoma cells exiting fragments of three independent melanomas or from secondary cultures derived from them, and cells from the melanoma line HTB-66, all underwent coalescence mediated by specialized cells in the 3D model. Normal melanocytes did not. However, coalescence of melanoma cells differed from that of breast-derived tumorigenic cell lines in that they 1) coalesced immediately, 2) underwent coalescence as individual cells as well as aggregates, 3) underwent coalescence far faster and 4) ultimately formed long, flat, fenestrated aggregates that were extremely dynamic. A screen of 51 purified monoclonal antibodies (mAbs) targeting cell surface-associated molecules revealed that two mAbs, anti-beta 1 integrin/(CD29) and anti-CD44, blocked melanoma cell coalescence. They also blocked coalescence of tumorigenic cells derived from a breast tumor. These results add weight to the commonality of coalescence as a characteristic of tumorigenic cells, as well as the usefulness of the 3D Matrigel model and software for both investigating the mechanisms regulating tumorigenesis and screening for potential anti-tumorigenesis mAbs.</description><subject>Aggregates</subject><subject>Antibodies, Monoclonal - pharmacology</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Biomarkers</subject><subject>Biotechnology</subject><subject>Breast</subject><subject>Breast cancer</subject><subject>Cancer cells</subject><subject>CD29 antigen</subject><subject>CD44 antigen</subject><subject>Cell Adhesion</subject><subject>Cell Line</subject><subject>Cell migration</subject><subject>Cell surface</subject><subject>Cell Tracking</subject><subject>Coalescence</subject><subject>Coalescing</subject><subject>Collagen</subject><subject>Commonality</subject><subject>Computer programs</subject><subject>Dosage and administration</subject><subject>Drug Combinations</subject><subject>Forming</subject><subject>Genetic aspects</subject><subject>Humans</subject><subject>Hyaluronan Receptors - metabolism</subject><subject>Integrin beta1 - metabolism</subject><subject>Laminin</subject><subject>Medicine and Health Sciences</subject><subject>Melanocytes</subject><subject>Melanocytes - metabolism</subject><subject>Melanoma</subject><subject>Melanoma - metabolism</subject><subject>Melanoma - pathology</subject><subject>Metastasis</subject><subject>Microscopy</subject><subject>Monoclonal antibodies</subject><subject>Phenotype</subject><subject>Proteoglycans</subject><subject>Research and Analysis Methods</subject><subject>Spheroids, Cellular</subject><subject>Studies</subject><subject>Three dimensional models</subject><subject>Tumor Cells, 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T.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Melanoma cells undergo aggressive coalescence in a 3D Matrigel model that is repressed by anti-CD44</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-03-06</date><risdate>2017</risdate><volume>12</volume><issue>3</issue><spage>e0173400</spage><epage>e0173400</epage><pages>e0173400-e0173400</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Using unique computer-assisted 3D reconstruction software, it was previously demonstrated that tumorigenic cell lines derived from breast tumors, when seeded in a 3D Matrigel model, grew as clonal aggregates which, after approximately 100 hours, underwent coalescence mediated by specialized cells, eventually forming a highly structured large spheroid. Non-tumorigenic cells did not undergo coalescence. Because histological sections of melanomas forming in patients suggest that melanoma cells migrate and coalesce to form tumors, we tested whether they also underwent coalescence in a 3D Matrigel model. Melanoma cells exiting fragments of three independent melanomas or from secondary cultures derived from them, and cells from the melanoma line HTB-66, all underwent coalescence mediated by specialized cells in the 3D model. Normal melanocytes did not. However, coalescence of melanoma cells differed from that of breast-derived tumorigenic cell lines in that they 1) coalesced immediately, 2) underwent coalescence as individual cells as well as aggregates, 3) underwent coalescence far faster and 4) ultimately formed long, flat, fenestrated aggregates that were extremely dynamic. 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| recordid | cdi_plos_journals_1874721050 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Aggregates Antibodies, Monoclonal - pharmacology Biology Biology and Life Sciences Biomarkers Biotechnology Breast Breast cancer Cancer cells CD29 antigen CD44 antigen Cell Adhesion Cell Line Cell migration Cell surface Cell Tracking Coalescence Coalescing Collagen Commonality Computer programs Dosage and administration Drug Combinations Forming Genetic aspects Humans Hyaluronan Receptors - metabolism Integrin beta1 - metabolism Laminin Medicine and Health Sciences Melanocytes Melanocytes - metabolism Melanoma Melanoma - metabolism Melanoma - pathology Metastasis Microscopy Monoclonal antibodies Phenotype Proteoglycans Research and Analysis Methods Spheroids, Cellular Studies Three dimensional models Tumor Cells, Cultured Tumorigenesis Tumors |
| title | Melanoma cells undergo aggressive coalescence in a 3D Matrigel model that is repressed by anti-CD44 |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-26T09%3A08%3A37IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Melanoma%20cells%20undergo%20aggressive%20coalescence%20in%20a%203D%20Matrigel%20model%20that%20is%20repressed%20by%20anti-CD44&rft.jtitle=PloS%20one&rft.au=Wessels,%20Deborah&rft.date=2017-03-06&rft.volume=12&rft.issue=3&rft.spage=e0173400&rft.epage=e0173400&rft.pages=e0173400-e0173400&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0173400&rft_dat=%3Cgale_plos_%3EA484264590%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1874721050&rft_id=info:pmid/28264026&rft_galeid=A484264590&rft_doaj_id=oai_doaj_org_article_6d777a850b8641f88679938c708d805f&rfr_iscdi=true |