{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T10:38:41Z","timestamp":1790937521891,"version":"4.1.0"},"reference-count":26,"publisher":"Wiley","issue":"2","license":[{"start":{"date-parts":[[2003,4,14]],"date-time":"2003-04-14T00:00:00Z","timestamp":1050278400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Developmental Dynamics"],"published-print":{"date-parts":[[2003,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The uterine bed undergoes remarkable changes during pregnancy, including proliferation and decidualization of the uterine stroma and remodeling and angiogenesis of the maternal vasculature. Fetal\u2010derived trophoblast giant cells invade into the uterus where they gain access to the maternal blood circulation to ensure sufficient nutrient supply of the embryo. In serial sections through early\u2010 to mid\u2010gestation conceptuses, we have determined the exact distance of trophoblast invasion and the expression of angiogenic, vasodilatory, and anticoagulative factors that are likely to influence remodeling and redirection of the maternal circulatory system. Trophoblast derivatives were detected at a distance as far as \u223c300 \u03bcm from the placental border, where they are allocated exclusively along the mid\u2010line of the decidua. The farthest invading cells characteristically expressed proliferin and proliferin\u2010related protein, hormones that affect endothelial cell migration and vascularization. Occasionally, these cells replaced the normal vascular endothelium and acquired a \u201cpseudo\u2010endothelial\u201d shape. Complete vascular disintegration was observed 50\u201380 \u03bcm outside of the placental border where maternal blood was entirely lined by a trophoblast giant cell\u2010derived network of blood sinuses. This transition in blood space lining correlated with trophoblast expression of various vasodilatory and anticoagulative factors that are likely to promote blood flow toward the placenta. Analysis of teratocarcinoma\u2010like tumors demonstrated that trophoblast giant cell\u2010induced promotion and redirection of blood flow is not restricted to the uterine environment. These results show that trophoblast giant cells have the intrinsic capacity to attract and increase blood flow and to gradually displace the vascular endothelium resulting in the formation of canals entirely lined by trophoblast cells. Developmental Dynamics 227:185\u2013191, 2003. \u00a9 2003 Wiley\u2010Liss, Inc.<\/jats:p>","DOI":"10.1002\/dvdy.10291","type":"journal-article","created":{"date-parts":[[2003,5,19]],"date-time":"2003-05-19T07:34:22Z","timestamp":1053329662000},"page":"185-191","source":"Crossref","is-referenced-by-count":87,"title":["Differential expression of angiogenic and vasodilatory factors by invasive trophoblast giant cells depending on depth of invasion"],"prefix":"10.1002","volume":"227","author":[{"given":"Myriam","family":"Hemberger","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tadashige","family":"Nozaki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mitsuko","family":"Masutani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James C.","family":"Cross","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2003,4,14]]},"reference":[{"key":"e_1_2_5_2_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.2002.0773"},{"key":"e_1_2_5_3_1","doi-asserted-by":"publisher","DOI":"10.1016\/0014-4827(72)90474-0"},{"key":"e_1_2_5_4_1","first-page":"775","article-title":"DNA ploidy of hydatidiform moles and nonmolar conceptuses: a study using flow and tissue section image cytometry","volume":"8","author":"Berezowsky J","year":"1995","journal-title":"Mod Pathol"},{"key":"e_1_2_5_5_1","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1051980308"},{"key":"e_1_2_5_6_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.114.2.521"},{"key":"e_1_2_5_7_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.77.7.4113"},{"key":"e_1_2_5_8_1","doi-asserted-by":"publisher","DOI":"10.1002\/mrd.1080340403"},{"key":"e_1_2_5_9_1","doi-asserted-by":"publisher","DOI":"10.1210\/rp.57.1.221"},{"key":"e_1_2_5_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0303-7207(01)00703-1"},{"key":"e_1_2_5_11_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.7985020"},{"key":"e_1_2_5_12_1","doi-asserted-by":"publisher","DOI":"10.1210\/endo-73-4-488"},{"key":"e_1_2_5_13_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod62.2.260"},{"key":"e_1_2_5_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1043-2760(01)00375-7"},{"key":"e_1_2_5_15_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0012-1606(03)00097-6"},{"key":"e_1_2_5_16_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.128.6.827"},{"key":"e_1_2_5_17_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.7527157"},{"key":"e_1_2_5_18_1","doi-asserted-by":"publisher","DOI":"10.1210\/endo-122-5-1761"},{"key":"e_1_2_5_19_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.82.13.4356"},{"key":"e_1_2_5_20_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.124.4.907"},{"key":"e_1_2_5_21_1","doi-asserted-by":"publisher","DOI":"10.1159\/000144801"},{"key":"e_1_2_5_22_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.23.13345"},{"key":"e_1_2_5_23_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.127.1.1"},{"key":"e_1_2_5_24_1","doi-asserted-by":"crossref","first-page":"2271","DOI":"10.1242\/dev.122.7.2271","article-title":"Developmentally regulated gene expression of thrombomodulin in postimplantation mouse embryos","volume":"122","author":"Weiler\u2010Guettler H","year":"1996","journal-title":"Development"},{"key":"e_1_2_5_25_1","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001920404"},{"key":"e_1_2_5_26_1","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.1998.9073"},{"key":"e_1_2_5_27_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0074-7696(08)62220-2"}],"container-title":["Developmental Dynamics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fdvdy.10291","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/anatomypubs.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/dvdy.10291","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T11:07:38Z","timestamp":1760353658000},"score":1,"resource":{"primary":{"URL":"https:\/\/anatomypubs.onlinelibrary.wiley.com\/doi\/10.1002\/dvdy.10291"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,4,14]]},"references-count":26,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2003,6]]}},"alternative-id":["10.1002\/dvdy.10291"],"URL":"https:\/\/doi.org\/10.1002\/dvdy.10291","archive":["Portico"],"relation":{},"ISSN":["1058-8388","1097-0177"],"issn-type":[{"value":"1058-8388","type":"print"},{"value":"1097-0177","type":"electronic"}],"subject":[],"published":{"date-parts":[[2003,4,14]]}}}