Acquisition of anoikis resistance up-regulates syndecan-4 expression in endothelial cells
Anoikis is a programmed cell death induced upon cell detachment from extracellular matrix, behaving as a critical mechanism in preventing adherent-independent cell growth and attachment to an inappropriate matrix, thus avoiding colonization of distant organs. Cell adhesion plays an important role in...
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| Veröffentlicht in: | PloS one 2014-12, Vol.9 (12), p.e116001-e116001 |
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| creator | Carneiro, Bruna Ribeiro Pernambuco Filho, Paulo Castanho A Mesquita, Ana Paula de Sousa da Silva, Douglas Santos Pinhal, Maria Aparecida S Nader, Helena B Lopes, Carla Cristina |
| description | Anoikis is a programmed cell death induced upon cell detachment from extracellular matrix, behaving as a critical mechanism in preventing adherent-independent cell growth and attachment to an inappropriate matrix, thus avoiding colonization of distant organs. Cell adhesion plays an important role in neoplastic transformation. Tumors produce several molecules that facilitate their proliferation, invasion and maintenance, especially proteoglycans. The syndecan-4, a heparan sulfate proteoglycan, can act as a co-receptor of growth factors and proteins of the extracellular matrix by increasing the affinity of adhesion molecules to their specific receptors. It participates together with integrins in cell adhesion at focal contacts connecting the extracellular matrix to the cytoskeleton. Changes in the expression of syndecan-4 have been observed in tumor cells, indicating its involvement in cancer. This study investigates the role of syndecan-4 in the process of anoikis and cell transformation. Endothelial cells were submitted to sequential cycles of forced anchorage impediment and distinct lineages were obtained. Anoikis-resistant endothelial cells display morphological alterations, high rate of proliferation, poor adhesion to fibronectin, laminin and collagen IV and deregulation of the cell cycle, becoming less serum-dependent. Furthermore, anoikis-resistant cell lines display a high invasive potential and a low rate of apoptosis. This is accompanied by an increase in the levels of heparan sulfate and chondroitin sulfate as well as by changes in the expression of syndecan-4 and heparanase. These results indicate that syndecan-4 plays a important role in acquisition of anoikis resistance and that the conferral of anoikis resistance may suffice to transform endothelial cells. |
| doi_str_mv | 10.1371/journal.pone.0116001 |
| format | Article |
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Cell adhesion plays an important role in neoplastic transformation. Tumors produce several molecules that facilitate their proliferation, invasion and maintenance, especially proteoglycans. The syndecan-4, a heparan sulfate proteoglycan, can act as a co-receptor of growth factors and proteins of the extracellular matrix by increasing the affinity of adhesion molecules to their specific receptors. It participates together with integrins in cell adhesion at focal contacts connecting the extracellular matrix to the cytoskeleton. Changes in the expression of syndecan-4 have been observed in tumor cells, indicating its involvement in cancer. This study investigates the role of syndecan-4 in the process of anoikis and cell transformation. Endothelial cells were submitted to sequential cycles of forced anchorage impediment and distinct lineages were obtained. Anoikis-resistant endothelial cells display morphological alterations, high rate of proliferation, poor adhesion to fibronectin, laminin and collagen IV and deregulation of the cell cycle, becoming less serum-dependent. Furthermore, anoikis-resistant cell lines display a high invasive potential and a low rate of apoptosis. This is accompanied by an increase in the levels of heparan sulfate and chondroitin sulfate as well as by changes in the expression of syndecan-4 and heparanase. These results indicate that syndecan-4 plays a important role in acquisition of anoikis resistance and that the conferral of anoikis resistance may suffice to transform endothelial cells.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0116001</identifier><identifier>PMID: 25549223</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adhesion ; Animals ; Anoikis ; Aorta - cytology ; Apoptosis ; Biology and Life Sciences ; Bromodeoxyuridine - pharmacology ; Cancer ; Cell Adhesion ; Cell adhesion & migration ; Cell adhesion molecules ; Cell Cycle ; Cell death ; Cell proliferation ; Cell Transformation, Neoplastic - genetics ; Cell Transformation, Neoplastic - metabolism ; Cells, Cultured ; Chondroitin sulfate ; Collagen (type IV) ; Colonization ; Cytoskeleton ; Deregulation ; Diadema ; Endothelial cells ; Endothelial Cells - metabolism ; Extracellular matrix ; Extracellular Matrix - metabolism ; Fibronectin ; Genetic transformation ; Glucuronidase - genetics ; Glucuronidase - metabolism ; Growth factors ; Heparan sulfate ; Integrins ; Invasiveness ; Kinases ; Laminin ; Organs ; Proteins ; Proteoglycans ; Rabbits ; Receptors ; Rodents ; Sulfates ; Syndecan-4 - genetics ; Syndecan-4 - metabolism ; Transformation ; Tumor cells ; Tumors ; Up-Regulation</subject><ispartof>PloS one, 2014-12, Vol.9 (12), p.e116001-e116001</ispartof><rights>2014 Carneiro 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>2014 Carneiro et al 2014 Carneiro et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-ae83a9fef9f67388f8129f8acb8d4ef838ae4a949acd990a79842aaa2502842c3</citedby><cites>FETCH-LOGICAL-c526t-ae83a9fef9f67388f8129f8acb8d4ef838ae4a949acd990a79842aaa2502842c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4280138/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4280138/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25549223$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Carneiro, Bruna Ribeiro</creatorcontrib><creatorcontrib>Pernambuco Filho, Paulo Castanho A</creatorcontrib><creatorcontrib>Mesquita, Ana Paula de Sousa</creatorcontrib><creatorcontrib>da Silva, Douglas Santos</creatorcontrib><creatorcontrib>Pinhal, Maria Aparecida S</creatorcontrib><creatorcontrib>Nader, Helena B</creatorcontrib><creatorcontrib>Lopes, Carla Cristina</creatorcontrib><title>Acquisition of anoikis resistance up-regulates syndecan-4 expression in endothelial cells</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Anoikis is a programmed cell death induced upon cell detachment from extracellular matrix, behaving as a critical mechanism in preventing adherent-independent cell growth and attachment to an inappropriate matrix, thus avoiding colonization of distant organs. Cell adhesion plays an important role in neoplastic transformation. Tumors produce several molecules that facilitate their proliferation, invasion and maintenance, especially proteoglycans. The syndecan-4, a heparan sulfate proteoglycan, can act as a co-receptor of growth factors and proteins of the extracellular matrix by increasing the affinity of adhesion molecules to their specific receptors. It participates together with integrins in cell adhesion at focal contacts connecting the extracellular matrix to the cytoskeleton. Changes in the expression of syndecan-4 have been observed in tumor cells, indicating its involvement in cancer. This study investigates the role of syndecan-4 in the process of anoikis and cell transformation. Endothelial cells were submitted to sequential cycles of forced anchorage impediment and distinct lineages were obtained. Anoikis-resistant endothelial cells display morphological alterations, high rate of proliferation, poor adhesion to fibronectin, laminin and collagen IV and deregulation of the cell cycle, becoming less serum-dependent. Furthermore, anoikis-resistant cell lines display a high invasive potential and a low rate of apoptosis. This is accompanied by an increase in the levels of heparan sulfate and chondroitin sulfate as well as by changes in the expression of syndecan-4 and heparanase. These results indicate that syndecan-4 plays a important role in acquisition of anoikis resistance and that the conferral of anoikis resistance may suffice to transform endothelial cells.</description><subject>Adhesion</subject><subject>Animals</subject><subject>Anoikis</subject><subject>Aorta - cytology</subject><subject>Apoptosis</subject><subject>Biology and Life Sciences</subject><subject>Bromodeoxyuridine - pharmacology</subject><subject>Cancer</subject><subject>Cell Adhesion</subject><subject>Cell adhesion & migration</subject><subject>Cell adhesion molecules</subject><subject>Cell Cycle</subject><subject>Cell death</subject><subject>Cell proliferation</subject><subject>Cell Transformation, Neoplastic - genetics</subject><subject>Cell Transformation, Neoplastic - metabolism</subject><subject>Cells, Cultured</subject><subject>Chondroitin sulfate</subject><subject>Collagen (type IV)</subject><subject>Colonization</subject><subject>Cytoskeleton</subject><subject>Deregulation</subject><subject>Diadema</subject><subject>Endothelial cells</subject><subject>Endothelial Cells - 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cytology</topic><topic>Apoptosis</topic><topic>Biology and Life Sciences</topic><topic>Bromodeoxyuridine - pharmacology</topic><topic>Cancer</topic><topic>Cell Adhesion</topic><topic>Cell adhesion & migration</topic><topic>Cell adhesion molecules</topic><topic>Cell Cycle</topic><topic>Cell death</topic><topic>Cell proliferation</topic><topic>Cell Transformation, Neoplastic - genetics</topic><topic>Cell Transformation, Neoplastic - metabolism</topic><topic>Cells, Cultured</topic><topic>Chondroitin sulfate</topic><topic>Collagen (type IV)</topic><topic>Colonization</topic><topic>Cytoskeleton</topic><topic>Deregulation</topic><topic>Diadema</topic><topic>Endothelial cells</topic><topic>Endothelial Cells - metabolism</topic><topic>Extracellular matrix</topic><topic>Extracellular Matrix - metabolism</topic><topic>Fibronectin</topic><topic>Genetic transformation</topic><topic>Glucuronidase - genetics</topic><topic>Glucuronidase - metabolism</topic><topic>Growth factors</topic><topic>Heparan sulfate</topic><topic>Integrins</topic><topic>Invasiveness</topic><topic>Kinases</topic><topic>Laminin</topic><topic>Organs</topic><topic>Proteins</topic><topic>Proteoglycans</topic><topic>Rabbits</topic><topic>Receptors</topic><topic>Rodents</topic><topic>Sulfates</topic><topic>Syndecan-4 - 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Cell adhesion plays an important role in neoplastic transformation. Tumors produce several molecules that facilitate their proliferation, invasion and maintenance, especially proteoglycans. The syndecan-4, a heparan sulfate proteoglycan, can act as a co-receptor of growth factors and proteins of the extracellular matrix by increasing the affinity of adhesion molecules to their specific receptors. It participates together with integrins in cell adhesion at focal contacts connecting the extracellular matrix to the cytoskeleton. Changes in the expression of syndecan-4 have been observed in tumor cells, indicating its involvement in cancer. This study investigates the role of syndecan-4 in the process of anoikis and cell transformation. Endothelial cells were submitted to sequential cycles of forced anchorage impediment and distinct lineages were obtained. Anoikis-resistant endothelial cells display morphological alterations, high rate of proliferation, poor adhesion to fibronectin, laminin and collagen IV and deregulation of the cell cycle, becoming less serum-dependent. Furthermore, anoikis-resistant cell lines display a high invasive potential and a low rate of apoptosis. This is accompanied by an increase in the levels of heparan sulfate and chondroitin sulfate as well as by changes in the expression of syndecan-4 and heparanase. These results indicate that syndecan-4 plays a important role in acquisition of anoikis resistance and that the conferral of anoikis resistance may suffice to transform endothelial cells.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25549223</pmid><doi>10.1371/journal.pone.0116001</doi><oa>free_for_read</oa></addata></record> |
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| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adhesion Animals Anoikis Aorta - cytology Apoptosis Biology and Life Sciences Bromodeoxyuridine - pharmacology Cancer Cell Adhesion Cell adhesion & migration Cell adhesion molecules Cell Cycle Cell death Cell proliferation Cell Transformation, Neoplastic - genetics Cell Transformation, Neoplastic - metabolism Cells, Cultured Chondroitin sulfate Collagen (type IV) Colonization Cytoskeleton Deregulation Diadema Endothelial cells Endothelial Cells - metabolism Extracellular matrix Extracellular Matrix - metabolism Fibronectin Genetic transformation Glucuronidase - genetics Glucuronidase - metabolism Growth factors Heparan sulfate Integrins Invasiveness Kinases Laminin Organs Proteins Proteoglycans Rabbits Receptors Rodents Sulfates Syndecan-4 - genetics Syndecan-4 - metabolism Transformation Tumor cells Tumors Up-Regulation |
| title | Acquisition of anoikis resistance up-regulates syndecan-4 expression in endothelial cells |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-10T11%3A50%3A54IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Acquisition%20of%20anoikis%20resistance%20up-regulates%20syndecan-4%20expression%20in%20endothelial%20cells&rft.jtitle=PloS%20one&rft.au=Carneiro,%20Bruna%20Ribeiro&rft.date=2014-12-30&rft.volume=9&rft.issue=12&rft.spage=e116001&rft.epage=e116001&rft.pages=e116001-e116001&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0116001&rft_dat=%3Cproquest_plos_%3E1641426320%3C/proquest_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1641029971&rft_id=info:pmid/25549223&rft_doaj_id=oai_doaj_org_article_6820c3fb0b304614a66da6dfda4d48b2&rfr_iscdi=true |