{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,25]],"date-time":"2026-08-25T13:01:54Z","timestamp":1787662914573,"version":"build-2736575974"},"reference-count":49,"publisher":"Elsevier BV","issue":"4","license":[{"start":{"date-parts":[[2013,11,1]],"date-time":"2013-11-01T00:00:00Z","timestamp":1383264000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2014,11,25]],"date-time":"2014-11-25T00:00:00Z","timestamp":1416873600000},"content-version":"vor","delay-in-days":389,"URL":"https:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Developmental Cell"],"published-print":{"date-parts":[[2013,11]]},"DOI":"10.1016\/j.devcel.2013.10.019","type":"journal-article","created":{"date-parts":[[2013,11,25]],"date-time":"2013-11-25T10:33:51Z","timestamp":1385375631000},"page":"373-386","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":93,"title":["c-Met-Dependent Multipotent Labyrinth Trophoblast Progenitors Establish Placental Exchange Interface"],"prefix":"10.1016","volume":"27","author":[{"given":"Masaya","family":"Ueno","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lydia\u00a0K.","family":"Lee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Akanksha","family":"Chhabra","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yeon\u00a0Joo","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rajkumar","family":"Sasidharan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ben","family":"Van\u00a0Handel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masakazu","family":"Kamata","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paniz","family":"Kamran","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Konstantina-Ioanna","family":"Sereti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Reza","family":"Ardehali","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meisheng","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hanna\u00a0K.A.","family":"Mikkola","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.devcel.2013.10.019_bib1","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1038\/77076","article-title":"The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta","volume":"25","author":"Anson-Cartwright","year":"2000","journal-title":"Nat. Genet."},{"key":"10.1016\/j.devcel.2013.10.019_bib2","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1002\/(SICI)1097-0177(199904)214:4<303::AID-AJA3>3.0.CO;2-B","article-title":"Murine Gcm1 gene is expressed in a subset of placental trophoblast cells","volume":"214","author":"Basyuk","year":"1999","journal-title":"Dev. Dyn."},{"key":"10.1016\/j.devcel.2013.10.019_bib3","doi-asserted-by":"crossref","first-page":"768","DOI":"10.1038\/376768a0","article-title":"Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud","volume":"376","author":"Bladt","year":"1995","journal-title":"Nature"},{"key":"10.1016\/j.devcel.2013.10.019_bib4","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1038\/nrc1912","article-title":"Invasive growth: a MET-driven genetic programme for cancer and stem cells","volume":"6","author":"Boccaccio","year":"2006","journal-title":"Nat. Rev. Cancer"},{"key":"10.1016\/j.devcel.2013.10.019_bib5","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1016\/j.devcel.2011.12.022","article-title":"Trophoblasts regulate the placental hematopoietic niche through PDGF-B signaling","volume":"22","author":"Chhabra","year":"2012","journal-title":"Dev. Cell"},{"key":"10.1016\/j.devcel.2013.10.019_bib6","first-page":"7345","article-title":"A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes in\u00a0vitro and exhibits cytoreductive antitumor activity in\u00a0vivo","volume":"63","author":"Christensen","year":"2003","journal-title":"Cancer Res."},{"key":"10.1016\/j.devcel.2013.10.019_bib7","first-page":"2726","article-title":"Levels of hepatocyte growth factor and its messenger ribonucleic acid in uncomplicated pregnancies and those complicated by preeclampsia","volume":"82","author":"Furugori","year":"1997","journal-title":"J.\u00a0Clin. Endocrinol. Metab."},{"key":"10.1016\/j.devcel.2013.10.019_bib8","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1083\/jcb.140.6.1453","article-title":"Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice","volume":"140","author":"Gabriel","year":"1998","journal-title":"J.\u00a0Cell Biol."},{"key":"10.1016\/j.devcel.2013.10.019_bib9","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1016\/j.devcel.2004.12.016","article-title":"The placenta is a niche for hematopoietic stem cells","volume":"8","author":"Gekas","year":"2005","journal-title":"Dev. Cell"},{"key":"10.1016\/j.devcel.2013.10.019_bib10","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.1002\/stem.686","article-title":"Establishment of human trophoblast progenitor cell lines from the chorion","volume":"29","author":"Genbacev","year":"2011","journal-title":"Stem Cells"},{"key":"10.1016\/j.devcel.2013.10.019_bib11","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1053\/plac.2001.0738","article-title":"Comparative developmental anatomy of the murine and human definitive placentae","volume":"23","author":"Georgiades","year":"2002","journal-title":"Placenta"},{"key":"10.1016\/j.devcel.2013.10.019_bib12","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1016\/j.tcb.2010.08.004","article-title":"Recycling endosomes in apical plasma membrane domain formation and epithelial cell polarity","volume":"20","author":"Golachowska","year":"2010","journal-title":"Trends Cell Biol."},{"key":"10.1016\/j.devcel.2013.10.019_bib13","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1038\/nrm2755","article-title":"Pathways and mechanisms of endocytic recycling","volume":"10","author":"Grant","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.devcel.2013.10.019_bib14","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.ydbio.2004.03.029","article-title":"The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells","volume":"271","author":"Hughes","year":"2004","journal-title":"Dev. Biol."},{"key":"10.1016\/j.devcel.2013.10.019_bib15","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1242\/dev.126.6.1247","article-title":"Mrj encodes a DnaJ-related co-chaperone that is essential for murine placental development","volume":"126","author":"Hunter","year":"1999","journal-title":"Development"},{"key":"10.1016\/j.devcel.2013.10.019_bib16","doi-asserted-by":"crossref","first-page":"4477","DOI":"10.1073\/pnas.0306068101","article-title":"Hepatocyte growth factor\/c-met signaling pathway is required for efficient liver regeneration and repair","volume":"101","author":"Huh","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.devcel.2013.10.019_bib17","first-page":"4092","article-title":"Hepatocyte growth factor stimulates trophoblast invasion: a potential mechanism for abnormal placentation in preeclampsia","volume":"84","author":"Kauma","year":"1999","journal-title":"J.\u00a0Clin. Endocrinol. Metab."},{"key":"10.1016\/j.devcel.2013.10.019_bib18","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/j.placenta.2010.06.017","article-title":"Cadherins in the human placenta\u2014epithelial-mesenchymal transition (EMT) and placental development","volume":"31","author":"Kokkinos","year":"2010","journal-title":"Placenta"},{"key":"10.1016\/j.devcel.2013.10.019_bib19","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1038\/7727","article-title":"Transferrin receptor is necessary for development of erythrocytes and the nervous system","volume":"21","author":"Levy","year":"1999","journal-title":"Nat. Genet."},{"key":"10.1016\/j.devcel.2013.10.019_bib20","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.exphem.2008.08.008","article-title":"Canonical Wnt pathway signaling suppresses VCAM-1 expression by marrow stromal and hematopoietic cells","volume":"37","author":"Malhotra","year":"2009","journal-title":"Exp. Hematol."},{"key":"10.1016\/j.devcel.2013.10.019_bib21","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1172\/JCI41211","article-title":"The placenta: transcriptional, epigenetic, and physiological integration during development","volume":"120","author":"Maltepe","year":"2010","journal-title":"J.\u00a0Clin. Invest."},{"key":"10.1016\/j.devcel.2013.10.019_bib22","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1038\/nrc3169","article-title":"Epithelial cell polarity, stem cells and cancer","volume":"12","author":"Martin-Belmonte","year":"2012","journal-title":"Nat. Rev. Cancer"},{"key":"10.1016\/j.devcel.2013.10.019_bib23","doi-asserted-by":"crossref","first-page":"1414","DOI":"10.1073\/pnas.0909207107","article-title":"Evidence of an epithelial stem\/progenitor cell hierarchy in the adult mouse lung","volume":"107","author":"McQualter","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.devcel.2013.10.019_bib24","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1073\/pnas.96.1.162","article-title":"Placental failure in mice lacking the homeobox gene Dlx3","volume":"96","author":"Morasso","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.devcel.2013.10.019_bib25","doi-asserted-by":"crossref","first-page":"2063","DOI":"10.1101\/gad.199828.112","article-title":"Blimp1\/Prdm1 governs terminal differentiation of endovascular trophoblast giant cells and defines multipotent progenitors in the developing placenta","volume":"26","author":"Mould","year":"2012","journal-title":"Genes Dev."},{"key":"10.1016\/j.devcel.2013.10.019_bib26","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.placenta.2009.11.013","article-title":"Cellular expression of the monocarboxylate transporter (MCT) family in the placenta of mice","volume":"31","author":"Nagai","year":"2010","journal-title":"Placenta"},{"key":"10.1016\/j.devcel.2013.10.019_bib27","first-page":"73","article-title":"Upregulation of human cytotrophoblast invasion by hepatocyte growth factor","volume":"55","author":"Nasu","year":"2000","journal-title":"J.\u00a0Reprod. Fertil. Suppl."},{"key":"10.1016\/j.devcel.2013.10.019_bib28","first-page":"275","article-title":"Phenotypic analysis of the mouse placenta","volume":"121","author":"Natale","year":"2006","journal-title":"Methods Mol. Med."},{"key":"10.1016\/j.devcel.2013.10.019_bib29","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1006\/dbio.2000.0148","article-title":"Connexin31-deficiency in mice causes transient placental dysmorphogenesis but does not impair hearing and skin differentiation","volume":"231","author":"Plum","year":"2001","journal-title":"Dev. Biol."},{"key":"10.1016\/j.devcel.2013.10.019_bib30","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.stem.2008.01.001","article-title":"The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation","volume":"2","author":"Rhodes","year":"2008","journal-title":"Cell Stem Cell"},{"key":"10.1016\/j.devcel.2013.10.019_bib31","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1038\/nature10346","article-title":"Germ-layer and lineage-restricted stem\/progenitors regenerate the mouse digit tip","volume":"476","author":"Rinkevich","year":"2011","journal-title":"Nature"},{"key":"10.1016\/j.devcel.2013.10.019_bib32","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1038\/35080570","article-title":"Placental development: lessons from mouse mutants","volume":"2","author":"Rossant","year":"2001","journal-title":"Nat. Rev. Genet."},{"key":"10.1016\/j.devcel.2013.10.019_bib33","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1093\/oxfordjournals.jbchem.a124761","article-title":"Hepatocyte growth factor promotes the growth of cytotrophoblasts by the paracrine mechanism","volume":"117","author":"Saito","year":"1995","journal-title":"J.\u00a0Biochem."},{"key":"10.1016\/j.devcel.2013.10.019_bib34","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1038\/373699a0","article-title":"Scatter factor\/hepatocyte growth factor is essential for liver development","volume":"373","author":"Schmidt","year":"1995","journal-title":"Nature"},{"key":"10.1016\/j.devcel.2013.10.019_bib35","doi-asserted-by":"crossref","first-page":"3453","DOI":"10.1113\/jphysiol.2009.173252","article-title":"Intrauterine growth restriction, human placental development and trophoblast cell death","volume":"587","author":"Scifres","year":"2009","journal-title":"J.\u00a0Physiol."},{"key":"10.1016\/j.devcel.2013.10.019_bib36","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.ydbio.2005.05.010","article-title":"Determinants of trophoblast lineage and cell subtype specification in the mouse placenta","volume":"284","author":"Simmons","year":"2005","journal-title":"Dev. Biol."},{"key":"10.1016\/j.devcel.2013.10.019_bib37","doi-asserted-by":"crossref","first-page":"2083","DOI":"10.1242\/dev.020099","article-title":"Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth","volume":"135","author":"Simmons","year":"2008","journal-title":"Development"},{"key":"10.1016\/j.devcel.2013.10.019_bib38","doi-asserted-by":"crossref","first-page":"1296","DOI":"10.1210\/en.2012-1823","article-title":"Where polarity meets fusion: role of Par6 in trophoblast differentiation during placental development and preeclampsia","volume":"154","author":"Sivasubramaniyam","year":"2013","journal-title":"Endocrinology"},{"key":"10.1016\/j.devcel.2013.10.019_bib39","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1016\/S0002-9440(10)65658-1","article-title":"Ontogeny of hepatocyte growth factor (HGF) and its receptor (c-met) in human placenta: reduced HGF expression in intrauterine growth restriction","volume":"153","author":"Somerset","year":"1998","journal-title":"Am. J. Pathol."},{"key":"10.1016\/j.devcel.2013.10.019_bib40","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/S0925-4773(02)00095-3","article-title":"Gcm1 expression defines three stages of chorio-allantoic interaction during placental development","volume":"115","author":"Stecca","year":"2002","journal-title":"Mech. Dev."},{"key":"10.1016\/j.devcel.2013.10.019_bib41","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1159\/000010310","article-title":"Expression of constitutively active c-MET receptor in human choriocarcinoma","volume":"50","author":"Takayanagi","year":"2000","journal-title":"Gynecol. Obstet. Invest."},{"key":"10.1016\/j.devcel.2013.10.019_bib42","doi-asserted-by":"crossref","first-page":"2072","DOI":"10.1126\/science.282.5396.2072","article-title":"Promotion of trophoblast stem cell proliferation by FGF4","volume":"282","author":"Tanaka","year":"1998","journal-title":"Science"},{"key":"10.1016\/j.devcel.2013.10.019_bib43","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1038\/373702a0","article-title":"Placental defect and embryonic lethality in mice lacking hepatocyte growth factor\/scatter factor","volume":"373","author":"Uehara","year":"1995","journal-title":"Nature"},{"key":"10.1016\/j.devcel.2013.10.019_bib44","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1111\/j.1365-2443.2007.01084.x","article-title":"Ovol2\/Movo, a homologue of Drosophila ovo, is required for angiogenesis, heart formation and placental development in mice","volume":"12","author":"Unezaki","year":"2007","journal-title":"Genes Cells"},{"key":"10.1016\/j.devcel.2013.10.019_bib45","doi-asserted-by":"crossref","first-page":"3913","DOI":"10.1242\/dev.129.16.3913","article-title":"Inhibition of trophoblast stem cell potential in chorionic ectoderm coincides with occlusion of the ectoplacental cavity in the mouse","volume":"129","author":"Uy","year":"2002","journal-title":"Development"},{"key":"10.1016\/j.devcel.2013.10.019_bib46","doi-asserted-by":"crossref","first-page":"3321","DOI":"10.1182\/blood-2010-04-279489","article-title":"The first trimester human placenta is a site for terminal maturation of primitive erythroid cells","volume":"116","author":"Van Handel","year":"2010","journal-title":"Blood"},{"key":"10.1016\/j.devcel.2013.10.019_bib47","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1152\/physiol.00001.2005","article-title":"Development of structures and transport functions in the mouse placenta","volume":"20","author":"Watson","year":"2005","journal-title":"Physiology (Bethesda)"},{"key":"10.1016\/j.devcel.2013.10.019_bib48","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1530\/rep.1.00869","article-title":"Mouse pregnancy-specific glycoproteins: tissue-specific expression and evidence of association with maternal vasculature","volume":"131","author":"Wynne","year":"2006","journal-title":"Reproduction"},{"key":"10.1016\/j.devcel.2013.10.019_bib49","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1146\/annurev-pathol-121808-102149","article-title":"Pathogenesis of preeclampsia","volume":"5","author":"Young","year":"2010","journal-title":"Annu. Rev. Pathol."}],"container-title":["Developmental Cell"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1534580713006369?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1534580713006369?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2024,5,20]],"date-time":"2024-05-20T06:02:30Z","timestamp":1716184950000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1534580713006369"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,11]]},"references-count":49,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2013,11]]}},"alternative-id":["S1534580713006369"],"URL":"https:\/\/doi.org\/10.1016\/j.devcel.2013.10.019","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.718190882.793536741","asserted-by":"object"}]},"ISSN":["1534-5807"],"issn-type":[{"value":"1534-5807","type":"print"}],"subject":[],"published":{"date-parts":[[2013,11]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"c-Met-Dependent Multipotent Labyrinth Trophoblast Progenitors Establish Placental Exchange Interface","name":"articletitle","label":"Article Title"},{"value":"Developmental Cell","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.devcel.2013.10.019","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2013 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}]}}