Long pentraxin-3 as an epithelial-stromal fibroblast growth factor-targeting inhibitor in prostate cancer
Fibroblast growth factors (FGFs) exert autocrine/paracrine functions in prostate cancer by stimulating angiogenesis and tumour growth. Here dihydrotestosterone (DHT) up‐regulates FGF2 and FGF8b production in murine TRAMP‐C2 prostate cancer cells, activating a FGF‐dependent autocrine loop of stimulat...
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| Veröffentlicht in: | The Journal of pathology 2013-06, Vol.230 (2), p.228-238 |
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| creator | Ronca, Roberto Alessi, Patrizia Coltrini, Daniela Di Salle, Emanuela Giacomini, Arianna Leali, Daria Corsini, Michela Belleri, Mirella Tobia, Chiara Garlanda, Cecilia Bonomi, Elisa Tardanico, Regina Vermi, William Presta, Marco |
| description | Fibroblast growth factors (FGFs) exert autocrine/paracrine functions in prostate cancer by stimulating angiogenesis and tumour growth. Here dihydrotestosterone (DHT) up‐regulates FGF2 and FGF8b production in murine TRAMP‐C2 prostate cancer cells, activating a FGF‐dependent autocrine loop of stimulation. The soluble pattern recognition receptor long pentraxin‐3 (PTX3) acts as a natural FGF antagonist that binds FGF2 and FGF8b via its N‐terminal domain. We demonstrate that recombinant PTX3 protein and the PTX3‐derived pentapeptide Ac‐ARPCA‐NH2 abolish the mitogenic response of murine TRAMP‐C2 cells and human LNCaP prostate cancer cells to DHT and FGFs. Also, PTX3 hampers the angiogenic activity of DHT‐activated TRAMP‐C2 cells on the chick embryo chorioallantoic membrane (CAM). Accordingly, human PTX3 overexpression inhibits the mitogenic activity exerted by DHT or FGFs on hPTX3_TRAMP‐C2 cell transfectants and their angiogenic activity. Also, hPTX3_TRAMP‐C2 cells show a dramatic decrease of their angiogenic and tumourigenic potential when grafted in syngeneic or immunodeficient athymic male mice. A similar inhibitory effect is observed when TRAMP‐C2 cells overexpress only the FGF‐binding N‐terminal PTX3 domain. In keeping with the anti‐tumour activity of PTX3 in experimental prostate cancer, immunohistochemical analysis of prostate needle biopsies from primary prostate adenocarcinoma patients shows that parenchymal PTX3 expression, abundant in basal cells of normal glands, is lost in high‐grade prostatic intraepithelial neoplasia and in invasive tumour areas. These results identify PTX3 as a potent FGF antagonist endowed with anti‐angiogenic and anti‐neoplastic activity in prostate cancer. Copyright © 2013 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd. |
| doi_str_mv | 10.1002/path.4181 |
| format | Article |
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Here dihydrotestosterone (DHT) up‐regulates FGF2 and FGF8b production in murine TRAMP‐C2 prostate cancer cells, activating a FGF‐dependent autocrine loop of stimulation. The soluble pattern recognition receptor long pentraxin‐3 (PTX3) acts as a natural FGF antagonist that binds FGF2 and FGF8b via its N‐terminal domain. We demonstrate that recombinant PTX3 protein and the PTX3‐derived pentapeptide Ac‐ARPCA‐NH2 abolish the mitogenic response of murine TRAMP‐C2 cells and human LNCaP prostate cancer cells to DHT and FGFs. Also, PTX3 hampers the angiogenic activity of DHT‐activated TRAMP‐C2 cells on the chick embryo chorioallantoic membrane (CAM). Accordingly, human PTX3 overexpression inhibits the mitogenic activity exerted by DHT or FGFs on hPTX3_TRAMP‐C2 cell transfectants and their angiogenic activity. Also, hPTX3_TRAMP‐C2 cells show a dramatic decrease of their angiogenic and tumourigenic potential when grafted in syngeneic or immunodeficient athymic male mice. A similar inhibitory effect is observed when TRAMP‐C2 cells overexpress only the FGF‐binding N‐terminal PTX3 domain. In keeping with the anti‐tumour activity of PTX3 in experimental prostate cancer, immunohistochemical analysis of prostate needle biopsies from primary prostate adenocarcinoma patients shows that parenchymal PTX3 expression, abundant in basal cells of normal glands, is lost in high‐grade prostatic intraepithelial neoplasia and in invasive tumour areas. These results identify PTX3 as a potent FGF antagonist endowed with anti‐angiogenic and anti‐neoplastic activity in prostate cancer. Copyright © 2013 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</description><identifier>ISSN: 0022-3417</identifier><identifier>EISSN: 1096-9896</identifier><identifier>DOI: 10.1002/path.4181</identifier><identifier>PMID: 23424081</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>Adenocarcinoma - drug therapy ; Adenocarcinoma - metabolism ; Adenocarcinoma - pathology ; androgen ; Animals ; Antineoplastic Agents - pharmacology ; C-Reactive Protein - pharmacology ; Cell Line, Tumor ; Chick Embryo ; Chorioallantoic Membrane - blood supply ; Chorioallantoic Membrane - drug effects ; Dihydrotestosterone - pharmacology ; FGF ; Humans ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Nude ; Mitogens - antagonists & inhibitors ; Neovascularization, Physiologic - drug effects ; pentraxin ; Prostate - drug effects ; Prostate - metabolism ; Prostate - pathology ; prostate cancer ; Prostatic Intraepithelial Neoplasia - metabolism ; Prostatic Intraepithelial Neoplasia - pathology ; Prostatic Neoplasms - drug therapy ; Prostatic Neoplasms - metabolism ; Prostatic Neoplasms - pathology ; Recombinant Proteins - pharmacology ; Serum Amyloid P-Component - pharmacology ; tumour growth</subject><ispartof>The Journal of pathology, 2013-06, Vol.230 (2), p.228-238</ispartof><rights>Copyright © 2013 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3911-acd68b8d15fccd42a78aa9a9480d2619d172cbad2c5e423df0a4fff8b9e7aab03</citedby><cites>FETCH-LOGICAL-c3911-acd68b8d15fccd42a78aa9a9480d2619d172cbad2c5e423df0a4fff8b9e7aab03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fpath.4181$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fpath.4181$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,781,785,1418,27929,27930,45579,45580</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23424081$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ronca, Roberto</creatorcontrib><creatorcontrib>Alessi, Patrizia</creatorcontrib><creatorcontrib>Coltrini, Daniela</creatorcontrib><creatorcontrib>Di Salle, Emanuela</creatorcontrib><creatorcontrib>Giacomini, Arianna</creatorcontrib><creatorcontrib>Leali, Daria</creatorcontrib><creatorcontrib>Corsini, Michela</creatorcontrib><creatorcontrib>Belleri, Mirella</creatorcontrib><creatorcontrib>Tobia, Chiara</creatorcontrib><creatorcontrib>Garlanda, Cecilia</creatorcontrib><creatorcontrib>Bonomi, Elisa</creatorcontrib><creatorcontrib>Tardanico, Regina</creatorcontrib><creatorcontrib>Vermi, William</creatorcontrib><creatorcontrib>Presta, Marco</creatorcontrib><title>Long pentraxin-3 as an epithelial-stromal fibroblast growth factor-targeting inhibitor in prostate cancer</title><title>The Journal of pathology</title><addtitle>J. Pathol</addtitle><description>Fibroblast growth factors (FGFs) exert autocrine/paracrine functions in prostate cancer by stimulating angiogenesis and tumour growth. Here dihydrotestosterone (DHT) up‐regulates FGF2 and FGF8b production in murine TRAMP‐C2 prostate cancer cells, activating a FGF‐dependent autocrine loop of stimulation. The soluble pattern recognition receptor long pentraxin‐3 (PTX3) acts as a natural FGF antagonist that binds FGF2 and FGF8b via its N‐terminal domain. We demonstrate that recombinant PTX3 protein and the PTX3‐derived pentapeptide Ac‐ARPCA‐NH2 abolish the mitogenic response of murine TRAMP‐C2 cells and human LNCaP prostate cancer cells to DHT and FGFs. Also, PTX3 hampers the angiogenic activity of DHT‐activated TRAMP‐C2 cells on the chick embryo chorioallantoic membrane (CAM). Accordingly, human PTX3 overexpression inhibits the mitogenic activity exerted by DHT or FGFs on hPTX3_TRAMP‐C2 cell transfectants and their angiogenic activity. Also, hPTX3_TRAMP‐C2 cells show a dramatic decrease of their angiogenic and tumourigenic potential when grafted in syngeneic or immunodeficient athymic male mice. A similar inhibitory effect is observed when TRAMP‐C2 cells overexpress only the FGF‐binding N‐terminal PTX3 domain. In keeping with the anti‐tumour activity of PTX3 in experimental prostate cancer, immunohistochemical analysis of prostate needle biopsies from primary prostate adenocarcinoma patients shows that parenchymal PTX3 expression, abundant in basal cells of normal glands, is lost in high‐grade prostatic intraepithelial neoplasia and in invasive tumour areas. These results identify PTX3 as a potent FGF antagonist endowed with anti‐angiogenic and anti‐neoplastic activity in prostate cancer. Copyright © 2013 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</description><subject>Adenocarcinoma - drug therapy</subject><subject>Adenocarcinoma - metabolism</subject><subject>Adenocarcinoma - pathology</subject><subject>androgen</subject><subject>Animals</subject><subject>Antineoplastic Agents - pharmacology</subject><subject>C-Reactive Protein - pharmacology</subject><subject>Cell Line, Tumor</subject><subject>Chick Embryo</subject><subject>Chorioallantoic Membrane - blood supply</subject><subject>Chorioallantoic Membrane - drug effects</subject><subject>Dihydrotestosterone - pharmacology</subject><subject>FGF</subject><subject>Humans</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Nude</subject><subject>Mitogens - antagonists & inhibitors</subject><subject>Neovascularization, Physiologic - drug effects</subject><subject>pentraxin</subject><subject>Prostate - drug effects</subject><subject>Prostate - metabolism</subject><subject>Prostate - pathology</subject><subject>prostate cancer</subject><subject>Prostatic Intraepithelial Neoplasia - metabolism</subject><subject>Prostatic Intraepithelial Neoplasia - pathology</subject><subject>Prostatic Neoplasms - drug therapy</subject><subject>Prostatic Neoplasms - metabolism</subject><subject>Prostatic Neoplasms - pathology</subject><subject>Recombinant Proteins - pharmacology</subject><subject>Serum Amyloid P-Component - pharmacology</subject><subject>tumour growth</subject><issn>0022-3417</issn><issn>1096-9896</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kE1PGzEQhq2qVQkfB_4AstRLezD4a9frI0IUKkWUQyqO1qzXTgyb3cV2BPz7OkrgUKknj-xnnvG8CJ0yes4o5RcT5NW5ZA37hGaM6proRtef0ay8cSIkUwfoMKVHSqnWVfUVHXAhuaQNm6EwH4clntyQI7yGgQgMCcOA3RTyyvUBepJyHNfQYx_aOLY9pIyXcXzJK-zB5jGSDHHpciieMKxCG8pdqfAUx5QhO2xhsC4eoy8e-uRO9ucR-vPzenF1S-a_b35dXc6JFZoxArarm7bpWOWt7SQH1QBo0LKhHa-Z7pjitoWO28pJLjpPQXrvm1Y7BdBScYS-77xl_vPGpWzWIVnX9zC4cZMMExWrGeWqKui3f9DHcROH8rstRTnjmspC_dhRtiyUovNmimEN8c0warb5m23-Zpt_Yc_2xk27dt0H-R54AS52wEvo3dv_Teb-cnG7V5JdR0jZvX50QHwytRKqMg93N0bNF-rh_k4aJf4CzR-goA</recordid><startdate>201306</startdate><enddate>201306</enddate><creator>Ronca, Roberto</creator><creator>Alessi, Patrizia</creator><creator>Coltrini, Daniela</creator><creator>Di Salle, Emanuela</creator><creator>Giacomini, Arianna</creator><creator>Leali, Daria</creator><creator>Corsini, Michela</creator><creator>Belleri, Mirella</creator><creator>Tobia, Chiara</creator><creator>Garlanda, Cecilia</creator><creator>Bonomi, Elisa</creator><creator>Tardanico, Regina</creator><creator>Vermi, William</creator><creator>Presta, Marco</creator><general>John Wiley & Sons, Ltd</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><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>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201306</creationdate><title>Long pentraxin-3 as an epithelial-stromal fibroblast growth factor-targeting inhibitor in prostate cancer</title><author>Ronca, Roberto ; Alessi, Patrizia ; Coltrini, Daniela ; Di Salle, Emanuela ; Giacomini, Arianna ; Leali, Daria ; Corsini, Michela ; Belleri, Mirella ; Tobia, Chiara ; Garlanda, Cecilia ; Bonomi, Elisa ; Tardanico, Regina ; Vermi, William ; Presta, Marco</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3911-acd68b8d15fccd42a78aa9a9480d2619d172cbad2c5e423df0a4fff8b9e7aab03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Adenocarcinoma - drug therapy</topic><topic>Adenocarcinoma - metabolism</topic><topic>Adenocarcinoma - pathology</topic><topic>androgen</topic><topic>Animals</topic><topic>Antineoplastic Agents - pharmacology</topic><topic>C-Reactive Protein - pharmacology</topic><topic>Cell Line, Tumor</topic><topic>Chick Embryo</topic><topic>Chorioallantoic Membrane - blood supply</topic><topic>Chorioallantoic Membrane - drug effects</topic><topic>Dihydrotestosterone - pharmacology</topic><topic>FGF</topic><topic>Humans</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Nude</topic><topic>Mitogens - antagonists & inhibitors</topic><topic>Neovascularization, Physiologic - drug effects</topic><topic>pentraxin</topic><topic>Prostate - drug effects</topic><topic>Prostate - metabolism</topic><topic>Prostate - pathology</topic><topic>prostate cancer</topic><topic>Prostatic Intraepithelial Neoplasia - metabolism</topic><topic>Prostatic Intraepithelial Neoplasia - pathology</topic><topic>Prostatic Neoplasms - drug therapy</topic><topic>Prostatic Neoplasms - metabolism</topic><topic>Prostatic Neoplasms - pathology</topic><topic>Recombinant Proteins - pharmacology</topic><topic>Serum Amyloid P-Component - pharmacology</topic><topic>tumour growth</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ronca, Roberto</creatorcontrib><creatorcontrib>Alessi, Patrizia</creatorcontrib><creatorcontrib>Coltrini, Daniela</creatorcontrib><creatorcontrib>Di Salle, Emanuela</creatorcontrib><creatorcontrib>Giacomini, Arianna</creatorcontrib><creatorcontrib>Leali, Daria</creatorcontrib><creatorcontrib>Corsini, Michela</creatorcontrib><creatorcontrib>Belleri, Mirella</creatorcontrib><creatorcontrib>Tobia, Chiara</creatorcontrib><creatorcontrib>Garlanda, Cecilia</creatorcontrib><creatorcontrib>Bonomi, Elisa</creatorcontrib><creatorcontrib>Tardanico, Regina</creatorcontrib><creatorcontrib>Vermi, William</creatorcontrib><creatorcontrib>Presta, Marco</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Journal of pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ronca, Roberto</au><au>Alessi, Patrizia</au><au>Coltrini, Daniela</au><au>Di Salle, Emanuela</au><au>Giacomini, Arianna</au><au>Leali, Daria</au><au>Corsini, Michela</au><au>Belleri, Mirella</au><au>Tobia, Chiara</au><au>Garlanda, Cecilia</au><au>Bonomi, Elisa</au><au>Tardanico, Regina</au><au>Vermi, William</au><au>Presta, Marco</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Long pentraxin-3 as an epithelial-stromal fibroblast growth factor-targeting inhibitor in prostate cancer</atitle><jtitle>The Journal of pathology</jtitle><addtitle>J. Pathol</addtitle><date>2013-06</date><risdate>2013</risdate><volume>230</volume><issue>2</issue><spage>228</spage><epage>238</epage><pages>228-238</pages><issn>0022-3417</issn><eissn>1096-9896</eissn><abstract>Fibroblast growth factors (FGFs) exert autocrine/paracrine functions in prostate cancer by stimulating angiogenesis and tumour growth. Here dihydrotestosterone (DHT) up‐regulates FGF2 and FGF8b production in murine TRAMP‐C2 prostate cancer cells, activating a FGF‐dependent autocrine loop of stimulation. The soluble pattern recognition receptor long pentraxin‐3 (PTX3) acts as a natural FGF antagonist that binds FGF2 and FGF8b via its N‐terminal domain. We demonstrate that recombinant PTX3 protein and the PTX3‐derived pentapeptide Ac‐ARPCA‐NH2 abolish the mitogenic response of murine TRAMP‐C2 cells and human LNCaP prostate cancer cells to DHT and FGFs. Also, PTX3 hampers the angiogenic activity of DHT‐activated TRAMP‐C2 cells on the chick embryo chorioallantoic membrane (CAM). Accordingly, human PTX3 overexpression inhibits the mitogenic activity exerted by DHT or FGFs on hPTX3_TRAMP‐C2 cell transfectants and their angiogenic activity. Also, hPTX3_TRAMP‐C2 cells show a dramatic decrease of their angiogenic and tumourigenic potential when grafted in syngeneic or immunodeficient athymic male mice. A similar inhibitory effect is observed when TRAMP‐C2 cells overexpress only the FGF‐binding N‐terminal PTX3 domain. In keeping with the anti‐tumour activity of PTX3 in experimental prostate cancer, immunohistochemical analysis of prostate needle biopsies from primary prostate adenocarcinoma patients shows that parenchymal PTX3 expression, abundant in basal cells of normal glands, is lost in high‐grade prostatic intraepithelial neoplasia and in invasive tumour areas. These results identify PTX3 as a potent FGF antagonist endowed with anti‐angiogenic and anti‐neoplastic activity in prostate cancer. Copyright © 2013 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>23424081</pmid><doi>10.1002/path.4181</doi><tpages>11</tpages></addata></record> |
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| subjects | Adenocarcinoma - drug therapy Adenocarcinoma - metabolism Adenocarcinoma - pathology androgen Animals Antineoplastic Agents - pharmacology C-Reactive Protein - pharmacology Cell Line, Tumor Chick Embryo Chorioallantoic Membrane - blood supply Chorioallantoic Membrane - drug effects Dihydrotestosterone - pharmacology FGF Humans Male Mice Mice, Inbred C57BL Mice, Nude Mitogens - antagonists & inhibitors Neovascularization, Physiologic - drug effects pentraxin Prostate - drug effects Prostate - metabolism Prostate - pathology prostate cancer Prostatic Intraepithelial Neoplasia - metabolism Prostatic Intraepithelial Neoplasia - pathology Prostatic Neoplasms - drug therapy Prostatic Neoplasms - metabolism Prostatic Neoplasms - pathology Recombinant Proteins - pharmacology Serum Amyloid P-Component - pharmacology tumour growth |
| title | Long pentraxin-3 as an epithelial-stromal fibroblast growth factor-targeting inhibitor in prostate cancer |
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