Anterior gradient protein-2 is a regulator of cellular adhesion in prostate cancer
Anterior Gradient Protein (AGR-2) is reported to be over-expressed in many epithelial cancers and promotes metastasis. A clear-cut mechanism for its observed function(s) has not been previously identified. We found significant upregulation of AGR-2 expression in a bone metastatic prostate cancer cel...
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| Veröffentlicht in: | PloS one 2014-02, Vol.9 (2), p.e89940 |
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| creator | Chanda, Diptiman Lee, Joo Hyoung Sawant, Anandi Hensel, Jonathan A Isayeva, Tatyana Reilly, Stephanie D Siegal, Gene P Smith, Claire Grizzle, William Singh, Raj Ponnazhagan, Selvarangan |
| description | Anterior Gradient Protein (AGR-2) is reported to be over-expressed in many epithelial cancers and promotes metastasis. A clear-cut mechanism for its observed function(s) has not been previously identified. We found significant upregulation of AGR-2 expression in a bone metastatic prostate cancer cell line, PC3, following culturing in bone marrow-conditioned medium. Substantial AGR-2 expression was also confirmed in prostate cancer tissue specimens in patients with bone lesions. By developing stable clones of PC3 cells with varying levels of AGR-2 expression, we identified that abrogation of AGR-2 significantly reduced cellular attachment to fibronectin, collagen I, collagen IV, laminin I and fibrinogen. Loss of cellular adhesion was associated with sharp decrease in the expression of α4, α5, αV, β3 and β4 integrins. Failure to undergo apoptosis following detachment is a hallmark of epithelial cancer metastasis. The AGR-2-silenced PC3 cells showed higher resistance to Tumor necrosis factor-related apoptosis- inducing ligand (TRAIL) induced apoptosis in vitro. This observation was also supported by significantly reduced Caspase-3 expression in AGR-2-silenced PC3 cells, which is a key effector of both extrinsic and intrinsic death signaling pathways. These data suggest that AGR-2 influence prostate cancer metastasis by regulation of cellular adhesion and apoptosis. |
| doi_str_mv | 10.1371/journal.pone.0089940 |
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A clear-cut mechanism for its observed function(s) has not been previously identified. We found significant upregulation of AGR-2 expression in a bone metastatic prostate cancer cell line, PC3, following culturing in bone marrow-conditioned medium. Substantial AGR-2 expression was also confirmed in prostate cancer tissue specimens in patients with bone lesions. By developing stable clones of PC3 cells with varying levels of AGR-2 expression, we identified that abrogation of AGR-2 significantly reduced cellular attachment to fibronectin, collagen I, collagen IV, laminin I and fibrinogen. Loss of cellular adhesion was associated with sharp decrease in the expression of α4, α5, αV, β3 and β4 integrins. Failure to undergo apoptosis following detachment is a hallmark of epithelial cancer metastasis. The AGR-2-silenced PC3 cells showed higher resistance to Tumor necrosis factor-related apoptosis- inducing ligand (TRAIL) induced apoptosis in vitro. This observation was also supported by significantly reduced Caspase-3 expression in AGR-2-silenced PC3 cells, which is a key effector of both extrinsic and intrinsic death signaling pathways. These data suggest that AGR-2 influence prostate cancer metastasis by regulation of cellular adhesion and apoptosis.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0089940</identifier><identifier>PMID: 24587138</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adhesion ; Androgens ; Animals ; Apoptosis ; Biology ; Bone cancer ; Bone lesions ; Bone marrow ; Bone Marrow - metabolism ; Bone Marrow - pathology ; Breast cancer ; Cancer ; Cancer metastasis ; Caspase ; Caspase-3 ; Cell adhesion & migration ; Cell Adhesion - drug effects ; Cell Adhesion - genetics ; Cell Death - drug effects ; Cell Death - genetics ; Cell Line, Tumor ; Cell Movement - genetics ; Cell Proliferation ; Cluster Analysis ; Collagen ; Collagen (type I) ; Collagen (type IV) ; Conditioning ; Development and progression ; Fibrinogen ; Fibronectin ; Fibronectins ; Gene Expression ; Gene Expression Profiling ; Gene Silencing ; Genomics ; Humans ; Immunoglobulins ; Integrins ; Integrins - genetics ; Integrins - metabolism ; Laboratories ; Laminin ; Lesions ; Male ; Medicine ; Metastases ; Metastasis ; Mice ; Mucoproteins ; Neoplasm Metastasis ; Oncogene Proteins ; Pathology ; Prostate cancer ; Prostatic Neoplasms - genetics ; Prostatic Neoplasms - metabolism ; Prostatic Neoplasms - pathology ; Proteins ; Proteins - genetics ; Proteins - metabolism ; Resistance factors ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Signaling ; TNF-Related Apoptosis-Inducing Ligand - pharmacology ; TRAIL protein</subject><ispartof>PloS one, 2014-02, Vol.9 (2), p.e89940</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Chanda 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 Chanda et al 2014 Chanda et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-92bec115a2b59d9e49a1e21b4436cb7cfe62da38cf89b346d7b74eddf56b23b3</citedby><cites>FETCH-LOGICAL-c692t-92bec115a2b59d9e49a1e21b4436cb7cfe62da38cf89b346d7b74eddf56b23b3</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/PMC3937391/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3937391/$$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/24587138$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chanda, Diptiman</creatorcontrib><creatorcontrib>Lee, Joo Hyoung</creatorcontrib><creatorcontrib>Sawant, Anandi</creatorcontrib><creatorcontrib>Hensel, Jonathan A</creatorcontrib><creatorcontrib>Isayeva, Tatyana</creatorcontrib><creatorcontrib>Reilly, Stephanie D</creatorcontrib><creatorcontrib>Siegal, Gene P</creatorcontrib><creatorcontrib>Smith, Claire</creatorcontrib><creatorcontrib>Grizzle, William</creatorcontrib><creatorcontrib>Singh, Raj</creatorcontrib><creatorcontrib>Ponnazhagan, Selvarangan</creatorcontrib><title>Anterior gradient protein-2 is a regulator of cellular adhesion in prostate cancer</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Anterior Gradient Protein (AGR-2) is reported to be over-expressed in many epithelial cancers and promotes metastasis. A clear-cut mechanism for its observed function(s) has not been previously identified. We found significant upregulation of AGR-2 expression in a bone metastatic prostate cancer cell line, PC3, following culturing in bone marrow-conditioned medium. Substantial AGR-2 expression was also confirmed in prostate cancer tissue specimens in patients with bone lesions. By developing stable clones of PC3 cells with varying levels of AGR-2 expression, we identified that abrogation of AGR-2 significantly reduced cellular attachment to fibronectin, collagen I, collagen IV, laminin I and fibrinogen. Loss of cellular adhesion was associated with sharp decrease in the expression of α4, α5, αV, β3 and β4 integrins. Failure to undergo apoptosis following detachment is a hallmark of epithelial cancer metastasis. The AGR-2-silenced PC3 cells showed higher resistance to Tumor necrosis factor-related apoptosis- inducing ligand (TRAIL) induced apoptosis in vitro. This observation was also supported by significantly reduced Caspase-3 expression in AGR-2-silenced PC3 cells, which is a key effector of both extrinsic and intrinsic death signaling pathways. These data suggest that AGR-2 influence prostate cancer metastasis by regulation of cellular adhesion and apoptosis.</description><subject>Adhesion</subject><subject>Androgens</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Biology</subject><subject>Bone cancer</subject><subject>Bone lesions</subject><subject>Bone marrow</subject><subject>Bone Marrow - metabolism</subject><subject>Bone Marrow - pathology</subject><subject>Breast cancer</subject><subject>Cancer</subject><subject>Cancer metastasis</subject><subject>Caspase</subject><subject>Caspase-3</subject><subject>Cell adhesion & migration</subject><subject>Cell Adhesion - drug effects</subject><subject>Cell Adhesion - genetics</subject><subject>Cell Death - drug effects</subject><subject>Cell Death - genetics</subject><subject>Cell Line, Tumor</subject><subject>Cell Movement - genetics</subject><subject>Cell Proliferation</subject><subject>Cluster Analysis</subject><subject>Collagen</subject><subject>Collagen (type I)</subject><subject>Collagen (type IV)</subject><subject>Conditioning</subject><subject>Development and progression</subject><subject>Fibrinogen</subject><subject>Fibronectin</subject><subject>Fibronectins</subject><subject>Gene Expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Silencing</subject><subject>Genomics</subject><subject>Humans</subject><subject>Immunoglobulins</subject><subject>Integrins</subject><subject>Integrins - genetics</subject><subject>Integrins - metabolism</subject><subject>Laboratories</subject><subject>Laminin</subject><subject>Lesions</subject><subject>Male</subject><subject>Medicine</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Mucoproteins</subject><subject>Neoplasm Metastasis</subject><subject>Oncogene Proteins</subject><subject>Pathology</subject><subject>Prostate cancer</subject><subject>Prostatic Neoplasms - genetics</subject><subject>Prostatic Neoplasms - metabolism</subject><subject>Prostatic Neoplasms - pathology</subject><subject>Proteins</subject><subject>Proteins - genetics</subject><subject>Proteins - metabolism</subject><subject>Resistance factors</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Signaling</subject><subject>TNF-Related Apoptosis-Inducing Ligand - pharmacology</subject><subject>TRAIL protein</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkttr1EAYxYMotlb_A9GAIPqw69xymZfCUrwsFAq1-Dp8mfmSnZLNrDMT0f_e2W5aNtIHCeQy-Z3zZU5Olr2mZEl5RT_dutEP0C93bsAlIbWUgjzJTqnkbFEywp8e3Z9kL0K4JaTgdVk-z06YKOqK8vo0u14NEb11Pu88GItDzHfeRbTDguU25JB77MYeYiJcm2vs-_TkczAbDNYNuR32ghAhYq5h0OhfZs9a6AO-mq5n2c2XzzcX3xaXV1_XF6vLhS4liwvJGtSUFsCaQhqJQgJFRhsheKmbSrdYMgO81m0tGy5KUzWVQGPaomwYb_hZ9vZgu-tdUFMaQdGCcFLWFWOJWB8I4-BW7bzdgv-jHFh1t-B8p8BHq3tUNVQaGU_jjRAEqhooKwUUFQctuDHJ63yaNjZbNDoF5aGfmc7fDHajOvdLcckrLmky-DAZePdzxBDV1oZ9nDCgG---W9BCpFNC3_2DPr67ieogbcAOrUtz9d5UrURVV5JwKhK1fIRKh8Gt1ak6rU3rM8HHmSAxEX_HDsYQ1Pr79f-zVz_m7PsjdoPQx01w_RhTicIcFAdQp1oFj-1DyJSoffPv01D75qup-Un25vgHPYjuq87_Ag_B_gU</recordid><startdate>20140227</startdate><enddate>20140227</enddate><creator>Chanda, Diptiman</creator><creator>Lee, Joo Hyoung</creator><creator>Sawant, Anandi</creator><creator>Hensel, Jonathan A</creator><creator>Isayeva, Tatyana</creator><creator>Reilly, Stephanie D</creator><creator>Siegal, Gene P</creator><creator>Smith, Claire</creator><creator>Grizzle, William</creator><creator>Singh, Raj</creator><creator>Ponnazhagan, Selvarangan</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140227</creationdate><title>Anterior gradient protein-2 is a regulator of cellular adhesion in prostate cancer</title><author>Chanda, Diptiman ; Lee, Joo Hyoung ; Sawant, Anandi ; Hensel, Jonathan A ; Isayeva, Tatyana ; Reilly, Stephanie D ; Siegal, Gene P ; Smith, Claire ; Grizzle, William ; Singh, Raj ; Ponnazhagan, Selvarangan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-92bec115a2b59d9e49a1e21b4436cb7cfe62da38cf89b346d7b74eddf56b23b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Adhesion</topic><topic>Androgens</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Biology</topic><topic>Bone cancer</topic><topic>Bone lesions</topic><topic>Bone marrow</topic><topic>Bone Marrow - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chanda, Diptiman</au><au>Lee, Joo Hyoung</au><au>Sawant, Anandi</au><au>Hensel, Jonathan A</au><au>Isayeva, Tatyana</au><au>Reilly, Stephanie D</au><au>Siegal, Gene P</au><au>Smith, Claire</au><au>Grizzle, William</au><au>Singh, Raj</au><au>Ponnazhagan, Selvarangan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Anterior gradient protein-2 is a regulator of cellular adhesion in prostate cancer</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-02-27</date><risdate>2014</risdate><volume>9</volume><issue>2</issue><spage>e89940</spage><pages>e89940-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Anterior Gradient Protein (AGR-2) is reported to be over-expressed in many epithelial cancers and promotes metastasis. A clear-cut mechanism for its observed function(s) has not been previously identified. We found significant upregulation of AGR-2 expression in a bone metastatic prostate cancer cell line, PC3, following culturing in bone marrow-conditioned medium. Substantial AGR-2 expression was also confirmed in prostate cancer tissue specimens in patients with bone lesions. By developing stable clones of PC3 cells with varying levels of AGR-2 expression, we identified that abrogation of AGR-2 significantly reduced cellular attachment to fibronectin, collagen I, collagen IV, laminin I and fibrinogen. Loss of cellular adhesion was associated with sharp decrease in the expression of α4, α5, αV, β3 and β4 integrins. Failure to undergo apoptosis following detachment is a hallmark of epithelial cancer metastasis. The AGR-2-silenced PC3 cells showed higher resistance to Tumor necrosis factor-related apoptosis- inducing ligand (TRAIL) induced apoptosis in vitro. This observation was also supported by significantly reduced Caspase-3 expression in AGR-2-silenced PC3 cells, which is a key effector of both extrinsic and intrinsic death signaling pathways. These data suggest that AGR-2 influence prostate cancer metastasis by regulation of cellular adhesion and apoptosis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24587138</pmid><doi>10.1371/journal.pone.0089940</doi><tpages>e89940</tpages><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_1503068722 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Adhesion Androgens Animals Apoptosis Biology Bone cancer Bone lesions Bone marrow Bone Marrow - metabolism Bone Marrow - pathology Breast cancer Cancer Cancer metastasis Caspase Caspase-3 Cell adhesion & migration Cell Adhesion - drug effects Cell Adhesion - genetics Cell Death - drug effects Cell Death - genetics Cell Line, Tumor Cell Movement - genetics Cell Proliferation Cluster Analysis Collagen Collagen (type I) Collagen (type IV) Conditioning Development and progression Fibrinogen Fibronectin Fibronectins Gene Expression Gene Expression Profiling Gene Silencing Genomics Humans Immunoglobulins Integrins Integrins - genetics Integrins - metabolism Laboratories Laminin Lesions Male Medicine Metastases Metastasis Mice Mucoproteins Neoplasm Metastasis Oncogene Proteins Pathology Prostate cancer Prostatic Neoplasms - genetics Prostatic Neoplasms - metabolism Prostatic Neoplasms - pathology Proteins Proteins - genetics Proteins - metabolism Resistance factors RNA, Messenger - genetics RNA, Messenger - metabolism Signaling TNF-Related Apoptosis-Inducing Ligand - pharmacology TRAIL protein |
| title | Anterior gradient protein-2 is a regulator of cellular adhesion in prostate cancer |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T15%3A29%3A59IST&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=Anterior%20gradient%20protein-2%20is%20a%20regulator%20of%20cellular%20adhesion%20in%20prostate%20cancer&rft.jtitle=PloS%20one&rft.au=Chanda,%20Diptiman&rft.date=2014-02-27&rft.volume=9&rft.issue=2&rft.spage=e89940&rft.pages=e89940-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0089940&rft_dat=%3Cgale_plos_%3EA478790314%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=1503068722&rft_id=info:pmid/24587138&rft_galeid=A478790314&rft_doaj_id=oai_doaj_org_article_8a7ce2321bd440a78a1264a573ac43dd&rfr_iscdi=true |