{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T23:45:29Z","timestamp":1790293529223,"version":"4.1.0"},"reference-count":23,"publisher":"Wiley","issue":"8","license":[{"start":{"date-parts":[[2019,7,9]],"date-time":"2019-07-09T00:00:00Z","timestamp":1562630400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Cancer Science"],"published-print":{"date-parts":[[2019,8]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Although direct adhesion of cancer cells to the mesothelial cell layer is considered to be a key step for peritoneal invasion of ovarian cancer cell masses (<jats:styled-content style=\"fixed-case\">OCM<\/jats:styled-content>), we recently identified a different strategy for the peritoneal invasion of <jats:styled-content style=\"fixed-case\">OCM<\/jats:styled-content>. In 6 out of 20 cases of ovarian carcinoma, extraperitoneal growth of the <jats:styled-content style=\"fixed-case\">OCM<\/jats:styled-content> was observed along with the neovascularization of feeding vessels, which connect the intraperitoneal host stroma and extraperitoneal lesions through the intact mesothelial cell layer. As an early step, the <jats:styled-content style=\"fixed-case\">OCMs<\/jats:styled-content> anchor in the extraperitoneal fibrin networks and then induce the migration of <jats:styled-content style=\"fixed-case\">CD<\/jats:styled-content>34\u2010positive and vascular endothelial growth factor A (<jats:styled-content style=\"fixed-case\">VEGF<\/jats:styled-content>\u2010A)\u2010positive endothelial cells, constructing extraperitoneal vascular networks around the <jats:styled-content style=\"fixed-case\">OCM<\/jats:styled-content>. During the extraperitoneal growth of <jats:styled-content style=\"fixed-case\">OCM<\/jats:styled-content>, podoplanin\u2010positive and \u03b1 smooth muscle actin (\u03b1<jats:styled-content style=\"fixed-case\">SMA)<\/jats:styled-content>\u2010positive cancer\u2010associated fibroblasts (<jats:styled-content style=\"fixed-case\">CAF<\/jats:styled-content>) appears. In more advanced lesions, the boundary line of mesothelial cells disappears around the insertion areas of feeding vessels and then extraperitoneal and intraperitoneal stroma are integrated, enabling the <jats:styled-content style=\"fixed-case\">OCM<\/jats:styled-content> to invade the host stroma, being associated with <jats:styled-content style=\"fixed-case\">CAF<\/jats:styled-content>. In addition, tissue factors (<jats:styled-content style=\"fixed-case\">TF<\/jats:styled-content>) are strongly detected around these peritoneal implantation sites and their levels in ascites were higher than that in blood. These findings demonstrate the presence of neovascularization around fibrin net\u2010anchored <jats:styled-content style=\"fixed-case\">OCMs<\/jats:styled-content> on the outer side of the intact peritoneal surface, suggesting a novel strategy for peritoneal invasion of ovarian cancer and <jats:styled-content style=\"fixed-case\">TF<\/jats:styled-content>\u2010targeted intraperitoneal anti\u2010cancer treatment. We observed and propose a novel strategy for peritoneal implantation of ovarian cancer. The strategy includes the preinvasive growth of fibrin\u2010anchored cancer cells along with neovascularization on the outer side of the intact peritoneal surface.<\/jats:p>","DOI":"10.1111\/cas.14098","type":"journal-article","created":{"date-parts":[[2019,6,14]],"date-time":"2019-06-14T09:51:41Z","timestamp":1560505901000},"page":"2658-2666","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Novel strategy of ovarian cancer implantation: Pre\u2010invasive growth of fibrin\u2010anchored cells with neovascularization"],"prefix":"10.1111","volume":"110","author":[{"given":"Ayumi","family":"Matsuoka","sequence":"first","affiliation":[{"name":"Department of Obstetrics and Gynecology Graduate School of Medical Sciences Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8648-3696","authenticated-orcid":false,"given":"Yasunari","family":"Mizumoto","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology Graduate School of Medical Sciences Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masanori","family":"Ono","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology Graduate School of Medical Sciences Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kyosuke","family":"Kagami","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology Graduate School of Medical Sciences Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takeshi","family":"Obata","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology Graduate School of Medical Sciences Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junpei","family":"Terakawa","sequence":"additional","affiliation":[{"name":"Institute for Experimental Animals Advanced Science Research Center Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshiko","family":"Maida","sequence":"additional","affiliation":[{"name":"Department of Nursing College of Medical, Pharmaceutical, and Health Sciences Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mitsuhiro","family":"Nakamura","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology Graduate School of Medical Sciences Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takiko","family":"Daikoku","sequence":"additional","affiliation":[{"name":"Institute for Experimental Animals Advanced Science Research Center Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hiroshi","family":"Fujiwara","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology Graduate School of Medical Sciences Kanazawa University Kanazawa Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2019,7,9]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"publisher","DOI":"10.3322\/canjclin.49.5.297"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1535-6108(04)00002-9"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1186\/1479-5876-3-25"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ygyno.2008.11.032"},{"key":"e_1_2_8_6_1","first-page":"829","article-title":"Mesothelial cells interact with tumor cells for the formation of ovarian cancer multicellular spheroids in peritoneal effusions","volume":"33","author":"Matte I","year":"2006","journal-title":"Clin Exp Metastasis"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.1172\/JCI87252"},{"key":"e_1_2_8_8_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10555-011-9337-5"},{"key":"e_1_2_8_9_1","doi-asserted-by":"publisher","DOI":"10.1002\/jcp.21240"},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.18632\/oncotarget.3746"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2009.11.007"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0188641"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.thromres.2003.11.001"},{"key":"e_1_2_8_14_1","first-page":"369","article-title":"Pathogenesis of ascites tumor growth: fibrinogen influx and fibrin accumulation in tissues lining the peritoneal cavity","volume":"55","author":"Nagy JA","year":"1995","journal-title":"Cancer Res"},{"key":"e_1_2_8_15_1","first-page":"376","article-title":"Pathogenesis of ascites tumor growth: angiogenesis, vascular remodeling, and stroma formation in the peritoneal lining","volume":"55","author":"Nagy JA","year":"1995","journal-title":"Cancer Res"},{"key":"e_1_2_8_16_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms15208"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1038\/onc.2015.139"},{"key":"e_1_2_8_18_1","doi-asserted-by":"publisher","DOI":"10.18632\/oncotarget.11729"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2005.02.034"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/nm1037"},{"key":"e_1_2_8_21_1","doi-asserted-by":"publisher","DOI":"10.1111\/cas.12645"},{"key":"e_1_2_8_22_1","doi-asserted-by":"publisher","DOI":"10.1002\/ijc.29492"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1111\/cas.12863"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1093\/annonc\/mdx011"}],"container-title":["Cancer Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1111%2Fcas.14098","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/cas.14098","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/cas.14098","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/cas.14098","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,3]],"date-time":"2023-09-03T04:20:45Z","timestamp":1693714845000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/cas.14098"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,7,9]]},"references-count":23,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2019,8]]}},"alternative-id":["10.1111\/cas.14098"],"URL":"https:\/\/doi.org\/10.1111\/cas.14098","archive":["Portico"],"relation":{},"ISSN":["1347-9032","1349-7006"],"issn-type":[{"value":"1347-9032","type":"print"},{"value":"1349-7006","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,7,9]]},"assertion":[{"value":"2019-02-24","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2019-05-27","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2019-07-09","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}