{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T23:06:03Z","timestamp":1791846363896,"version":"4.3.4"},"reference-count":87,"publisher":"The Company of Biologists","issue":"22","license":[{"start":{"date-parts":[[2023,11,15]],"date-time":"2023-11-15T00:00:00Z","timestamp":1700006400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"funder":[{"name":"Austrian Science Fund","award":["P31470-B30"],"award-info":[{"award-number":["P31470-B30"]}]},{"name":"Austrian Science Fund","award":["P36159-B"],"award-info":[{"award-number":["P36159-B"]}]},{"name":"Austrian Science Fund","award":["P34588-B"],"award-info":[{"award-number":["P34588-B"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,11,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Failures in growth and differentiation of the early human placenta are associated with severe pregnancy disorders such as pre-eclampsia and fetal growth restriction. However, regulatory mechanisms controlling development of placental epithelial cells, the trophoblasts, remain poorly elucidated. Using trophoblast stem cells (TSCs), trophoblast organoids (TB-ORGs) and primary cytotrophoblasts (CTBs) of early pregnancy, we herein show that autocrine NOTCH3 signalling controls human placental expansion and differentiation. The NOTCH3 receptor was specifically expressed in proliferative CTB progenitors and its active form, the nuclear NOTCH3 intracellular domain (NOTCH3-ICD), interacted with the transcriptional co-activator mastermind-like 1 (MAML1). Doxycycline-inducible expression of dominant-negative MAML1 in TSC lines provoked cell fusion and upregulation of genes specific for multinucleated syncytiotrophoblasts, which are the differentiated hormone-producing cells of the placenta. However, progenitor expansion and markers of trophoblast stemness and proliferation were suppressed. Accordingly, inhibition of NOTCH3 signalling diminished growth of TB-ORGs, whereas overexpression of NOTCH3-ICD in primary CTBs and TSCs showed opposite effects. In conclusion, the data suggest that canonical NOTCH3 signalling plays a key role in human placental development by promoting self-renewal of CTB progenitors.<\/jats:p>","DOI":"10.1242\/dev.202152","type":"journal-article","created":{"date-parts":[[2023,10,31]],"date-time":"2023-10-31T05:03:07Z","timestamp":1698728587000},"source":"Crossref","is-referenced-by-count":26,"title":["NOTCH3 signalling controls human trophoblast stem cell expansion and differentiation"],"prefix":"10.1242","volume":"150","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4640-0301","authenticated-orcid":false,"given":"Bianca","family":"Dietrich","sequence":"first","affiliation":[{"name":"Medical University of Vienna 1 Placental Development Group , , A-1090 Vienna , Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2575-8219","authenticated-orcid":false,"given":"Victoria","family":"Kunihs","sequence":"additional","affiliation":[{"name":"Medical University of Vienna 1 Placental Development Group , , A-1090 Vienna , Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8034-0181","authenticated-orcid":false,"given":"Andreas I.","family":"Lackner","sequence":"additional","affiliation":[{"name":"Medical University of Vienna 2 Maternal-Fetal Immunology Group, Department of Obstetrics and Gynecology, Reproductive Biology Unit , , A-1090 Vienna , Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8115-8867","authenticated-orcid":false,"given":"Gudrun","family":"Meinhardt","sequence":"additional","affiliation":[{"name":"Medical University of Vienna 1 Placental Development Group , , A-1090 Vienna , Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4134-8033","authenticated-orcid":false,"given":"Bon-Kyoung","family":"Koo","sequence":"additional","affiliation":[{"name":"Center for Genome Engineering, Institute for Basic Science 3 , Yuseong-Gu, Daejeon 34126 , Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8440-5221","authenticated-orcid":false,"given":"J\u00fcrgen","family":"Pollheimer","sequence":"additional","affiliation":[{"name":"Medical University of Vienna 2 Maternal-Fetal Immunology Group, Department of Obstetrics and Gynecology, Reproductive Biology Unit , , A-1090 Vienna , Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2409-1317","authenticated-orcid":false,"given":"Sandra","family":"Haider","sequence":"additional","affiliation":[{"name":"Medical University of Vienna 1 Placental Development Group , , A-1090 Vienna , Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6625-8950","authenticated-orcid":false,"given":"Martin","family":"Kn\u00f6fler","sequence":"additional","affiliation":[{"name":"Medical University of Vienna 1 Placental Development Group , , A-1090 Vienna , Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2023,11,16]]},"reference":[{"key":"2023111612421566800_DEV202152C1","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1038\/s41586-023-05869-0","article-title":"Spatial multiomics map of trophoblast development in early pregnancy","volume":"616","author":"Arutyunyan","year":"2023","journal-title":"Nature"},{"key":"2023111612421566800_DEV202152C2","author":"Blighe","year":"2023"},{"key":"2023111612421566800_DEV202152C3","doi-asserted-by":"publisher","first-page":"1631","DOI":"10.1007\/s00018-009-8668-7","article-title":"The Notch signaling pathway: transcriptional regulation at Notch target genes","volume":"66","author":"Borggrefe","year":"2009","journal-title":"Cell. Mol. Life Sci."},{"key":"2023111612421566800_DEV202152C4","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.ajog.2010.08.009","article-title":"The \u201cGreat Obstetrical Syndromes\u201d are associated with disorders of deep placentation","volume":"204","author":"Brosens","year":"2011","journal-title":"Am. J. Obstet. Gynecol."},{"key":"2023111612421566800_DEV202152C5","doi-asserted-by":"publisher","first-page":"20140066","DOI":"10.1098\/rstb.2014.0066","article-title":"The placenta: a multifaceted, transient organ","volume":"370","author":"Burton","year":"2015","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"2023111612421566800_DEV202152C6","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1387\/ijdb.082764gb","article-title":"The influence of the intrauterine environment on human placental development","volume":"54","author":"Burton","year":"2010","journal-title":"Int. J. Dev. Biol."},{"key":"2023111612421566800_DEV202152C7","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.placenta.2020.02.008","article-title":"Review: Histotrophic nutrition and the placental-endometrial dialogue during human early pregnancy","volume":"102","author":"Burton","year":"2020","journal-title":"Placenta"},{"key":"2023111612421566800_DEV202152C8","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1093\/molehr\/gat050","article-title":"Involvement of Epac1\/Rap1\/CaMKI\/HDAC5 signaling cascade in the regulation of placental cell fusion","volume":"19","author":"Chang","year":"2013","journal-title":"Mol. Hum. Reprod."},{"key":"2023111612421566800_DEV202152C9","doi-asserted-by":"publisher","first-page":"dev200171","DOI":"10.1242\/dev.200171","article-title":"An integrated atlas of human placental development delineates essential regulators of trophoblast stem cells","volume":"149","author":"Chen","year":"2022","journal-title":"Development"},{"key":"2023111612421566800_DEV202152C10","doi-asserted-by":"publisher","first-page":"1439","DOI":"10.1158\/0008-5472.CAN-16-1022","article-title":"Constitutive NOTCH3 signaling promotes the growth of basal breast cancers","volume":"77","author":"Choy","year":"2017","journal-title":"Cancer Res."},{"key":"2023111612421566800_DEV202152C11","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1007\/s00018-022-04589-4","article-title":"Here and there a trophoblast, a transcriptional evaluation of trophoblast cell models","volume":"79","author":"Cox","year":"2022","journal-title":"Cell. Mol. Life Sci."},{"key":"2023111612421566800_DEV202152C12","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1007\/s00018-022-04285-3","article-title":"WNT and NOTCH signaling in human trophoblast development and differentiation","volume":"79","author":"Dietrich","year":"2022","journal-title":"Cell. Mol. Life Sci."},{"key":"2023111612421566800_DEV202152C13","doi-asserted-by":"publisher","first-page":"5148","DOI":"10.1038\/onc.2008.229","article-title":"The many facets of Notch ligands","volume":"27","author":"D'Souza","year":"2008","journal-title":"Oncogene"},{"key":"2023111612421566800_DEV202152C14","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1146\/annurev-immunol-032712-100003","article-title":"Immunology of the maternal-fetal interface","volume":"31","author":"Erlebacher","year":"2013","journal-title":"Annu. Rev. Immunol."},{"key":"2023111612421566800_DEV202152C15","doi-asserted-by":"publisher","first-page":"S34","DOI":"10.1016\/S1096-6374(03)00053-4","article-title":"Human placenta as an endocrine organ","volume":"13","author":"Evain-Brion","year":"2003","journal-title":"Growth Horm. IGF Res."},{"key":"2023111612421566800_DEV202152C16","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1016\/j.placenta.2020.02.007","article-title":"Trophoblast lineage-specific differentiation and associated alterations in preeclampsia and fetal growth restriction","volume":"102","author":"Farah","year":"2020","journal-title":"Placenta"},{"key":"2023111612421566800_DEV202152C17","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1016\/j.devcel.2009.03.010","article-title":"Notch signaling: the core pathway and its posttranslational regulation","volume":"16","author":"Fortini","year":"2009","journal-title":"Dev. Cell"},{"key":"2023111612421566800_DEV202152C18","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1038\/s41594-023-00960-6","article-title":"Regulation of human trophoblast gene expression by endogenous retroviruses","volume":"30","author":"Frost","year":"2023","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2023111612421566800_DEV202152C19","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1016\/j.molcel.2004.10.014","article-title":"Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover","volume":"16","author":"Fryer","year":"2004","journal-title":"Mol. Cell"},{"key":"2023111612421566800_DEV202152C20","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1210\/en.2013-1455","article-title":"Notch signaling plays a critical role in motility and differentiation of human first-trimester cytotrophoblasts","volume":"155","author":"Haider","year":"2014","journal-title":"Endocrinology"},{"key":"2023111612421566800_DEV202152C21","doi-asserted-by":"publisher","first-page":"E7710","DOI":"10.1073\/pnas.1612335113","article-title":"Notch1 controls development of the extravillous trophoblast lineage in the human placenta","volume":"113","author":"Haider","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023111612421566800_DEV202152C22","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.placenta.2017.01.117","article-title":"Notch signalling in placental development and gestational diseases","volume":"56","author":"Haider","year":"2017","journal-title":"Placenta"},{"key":"2023111612421566800_DEV202152C23","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1016\/j.stemcr.2018.07.004","article-title":"Self-renewing trophoblast organoids recapitulate the developmental program of the early human placenta","volume":"11","author":"Haider","year":"2018","journal-title":"Stem Cell Rep."},{"key":"2023111612421566800_DEV202152C24","doi-asserted-by":"publisher","first-page":"e2120667119","DOI":"10.1073\/pnas.2120667119","article-title":"Transforming growth factor-beta signaling governs the differentiation program of extravillous trophoblasts in the developing human placenta","volume":"119","author":"Haider","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023111612421566800_DEV202152C25","first-page":"297","article-title":"Development of the human placenta in the first three months of gestation","volume":"94","author":"Hamilton","year":"1960","journal-title":"J. Anat."},{"key":"2023111612421566800_DEV202152C26","doi-asserted-by":"publisher","first-page":"ra30","DOI":"10.1126\/scisignal.2005892","article-title":"Site-specific methylation of Notch1 controls the amplitude and duration of the Notch1 response","volume":"8","author":"Hein","year":"2015","journal-title":"Sci. Signal."},{"key":"2023111612421566800_DEV202152C27","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1038\/s41576-019-0169-4","article-title":"Mechanisms of early placental development in mouse and humans","volume":"21","author":"Hemberger","year":"2020","journal-title":"Nat. Rev. Genet."},{"key":"2023111612421566800_DEV202152C28","doi-asserted-by":"publisher","first-page":"e2105130118","DOI":"10.1073\/pnas.2105130118","article-title":"MSX2 safeguards syncytiotrophoblast fate of human trophoblast stem cells","volume":"118","author":"Hornbachner","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023111612421566800_DEV202152C29","doi-asserted-by":"publisher","first-page":"3187","DOI":"10.1007\/s00018-010-0378-7","article-title":"Notch1 signaling is mediated by importins alpha 3, 4, and 7","volume":"67","author":"Huenniger","year":"2010","journal-title":"Cell. Mol. Life Sci."},{"key":"2023111612421566800_DEV202152C30","doi-asserted-by":"publisher","first-page":"2987","DOI":"10.1242\/dev.066589","article-title":"A role for Notch signaling in trophoblast endovascular invasion and in the pathogenesis of pre-eclampsia","volume":"138","author":"Hunkapiller","year":"2011","journal-title":"Development"},{"key":"2023111612421566800_DEV202152C31","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/j.placenta.2012.01.020","article-title":"Human placentation from nidation to 5 weeks of gestation. Part I: What do we know about formative placental development following implantation?","volume":"33","author":"James","year":"2012","journal-title":"Placenta"},{"key":"2023111612421566800_DEV202152C32","doi-asserted-by":"publisher","first-page":"e2203071119","DOI":"10.1073\/pnas.2203071119","article-title":"The multifaceted role of GCM1 during trophoblast differentiation in the human placenta","volume":"119","author":"Jeyarajah","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023111612421566800_DEV202152C33","doi-asserted-by":"publisher","first-page":"1049","DOI":"10.1111\/j.1471-0528.1986.tb07830.x","article-title":"Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants","volume":"93","author":"Khong","year":"1986","journal-title":"Br. J. Obstet. Gynaecol."},{"key":"2023111612421566800_DEV202152C34","doi-asserted-by":"publisher","first-page":"3806","DOI":"10.1093\/nar\/gkad215","article-title":"Super-enhancer-associated transcription factors collaboratively regulate trophoblast-active gene expression programs in human trophoblast stem cells","volume":"51","author":"Kim","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"2023111612421566800_DEV202152C35","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1093\/jb\/mvv123","article-title":"Notch signalling in the nucleus: roles of Mastermind-like (MAML) transcriptional coactivators","volume":"159","author":"Kitagawa","year":"2016","journal-title":"J. Biochem."},{"key":"2023111612421566800_DEV202152C36","doi-asserted-by":"publisher","first-page":"1685","DOI":"10.1210\/en.2003-0954","article-title":"Transcriptional regulation of the human chorionic gonadotropin \u03b2 gene during villous trophoblast differentiation","volume":"145","author":"Kn\u00f6fler","year":"2004","journal-title":"Endocrinology"},{"key":"2023111612421566800_DEV202152C37","doi-asserted-by":"publisher","first-page":"3479","DOI":"10.1007\/s00018-019-03104-6","article-title":"Human placenta and trophoblast development: key molecular mechanisms and model systems","volume":"76","author":"Kn\u00f6fler","year":"2019","journal-title":"Cell. Mol. Life Sci."},{"key":"2023111612421566800_DEV202152C38","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1016\/j.cell.2009.03.045","article-title":"The canonical Notch signaling pathway: unfolding the activation mechanism","volume":"137","author":"Kopan","year":"2009","journal-title":"Cell"},{"key":"2023111612421566800_DEV202152C39","doi-asserted-by":"publisher","first-page":"179827","DOI":"10.1155\/2012\/179827","article-title":"Regulation of nutrient transport across the placenta","volume":"2012","author":"Lager","year":"2012","journal-title":"J. Pregnancy"},{"key":"2023111612421566800_DEV202152C40","doi-asserted-by":"publisher","first-page":"dev162305","DOI":"10.1242\/dev.162305","article-title":"Integrin alpha2 marks a niche of trophoblast progenitor cells in first trimester human placenta","volume":"145","author":"Lee","year":"2018","journal-title":"Development"},{"key":"2023111612421566800_DEV202152C41","first-page":"1809","article-title":"Human cytotrophoblast differentiation\/invasion is abnormal in pre-eclampsia","volume":"151","author":"Lim","year":"1997","journal-title":"Am. J. Pathol."},{"key":"2023111612421566800_DEV202152C42","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1161\/CIRCRESAHA.108.184846","article-title":"NOTCH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1","volume":"104","author":"Liu","year":"2009","journal-title":"Circ. Res."},{"key":"2023111612421566800_DEV202152C43","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1038\/s41422-018-0066-y","article-title":"Single-cell RNA-seq reveals the diversity of trophoblast subtypes and patterns of differentiation in the human placenta","volume":"28","author":"Liu","year":"2018","journal-title":"Cell Res."},{"key":"2023111612421566800_DEV202152C44","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"2023111612421566800_DEV202152C45","doi-asserted-by":"publisher","first-page":"1150","DOI":"10.1016\/j.celrep.2017.10.019","article-title":"Fine-tuned and cell-cycle-restricted expression of fusogenic protein syncytin-2 maintains functional placental syncytia","volume":"21","author":"Lu","year":"2017","journal-title":"Cell Rep."},{"key":"2023111612421566800_DEV202152C46","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1146\/annurev-cellbio-100814-125620","article-title":"Placenta: the forgotten organ","volume":"31","author":"Maltepe","year":"2015","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"2023111612421566800_DEV202152C47","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1002\/path.2997","article-title":"Inhibition of NOTCH3 signalling significantly enhances sensitivity to cisplatin in EBV-associated nasopharyngeal carcinoma","volume":"226","author":"Man","year":"2012","journal-title":"J. Pathol."},{"key":"2023111612421566800_DEV202152C48","doi-asserted-by":"publisher","first-page":"5138","DOI":"10.1038\/onc.2008.228","article-title":"Mastermind-like transcriptional co-activators: emerging roles in regulating cross talk among multiple signaling pathways","volume":"27","author":"McElhinny","year":"2008","journal-title":"Oncogene"},{"key":"2023111612421566800_DEV202152C49","doi-asserted-by":"publisher","first-page":"1908","DOI":"10.1210\/en.2013-2042","article-title":"Wnt-dependent T-cell factor-4 controls human etravillous trophoblast motility","volume":"155","author":"Meinhardt","year":"2014","journal-title":"Endocrinology"},{"key":"2023111612421566800_DEV202152C50","doi-asserted-by":"publisher","first-page":"13562","DOI":"10.1073\/pnas.2002630117","article-title":"Pivotal role of the transcriptional co-activator YAP in trophoblast stemness of the developing human placenta","volume":"117","author":"Meinhardt","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023111612421566800_DEV202152C51","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1038\/s41577-022-00777-2","article-title":"Local immune recognition of trophoblast in early human pregnancy: controversies and questions","volume":"23","author":"Moffett","year":"2023","journal-title":"Nat. Rev. Immunol."},{"key":"2023111612421566800_DEV202152C52","doi-asserted-by":"publisher","first-page":"21232","DOI":"10.1074\/jbc.M301567200","article-title":"Structural requirements for assembly of the CSL intracellular Notch1 Mastermind-like 1 transcriptional activation complex","volume":"278","author":"Nam","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2023111612421566800_DEV202152C53","doi-asserted-by":"publisher","first-page":"1091","DOI":"10.3389\/fphys.2018.01091","article-title":"The role of placental hormones in mediating maternal adaptations to support pregnancy and lactation","volume":"9","author":"Napso","year":"2018","journal-title":"Front. Physiol."},{"key":"2023111612421566800_DEV202152C54","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1016\/j.stem.2017.11.004","article-title":"Derivation of human trophoblast stem cells","volume":"22","author":"Okae","year":"2018","journal-title":"Cell Stem Cell"},{"key":"2023111612421566800_DEV202152C55","doi-asserted-by":"publisher","first-page":"1007","DOI":"10.1016\/j.neo.2014.10.004","article-title":"Notch3\/Jagged1 circuitry reinforces notch signaling and sustains T-ALL","volume":"16","author":"Pelullo","year":"2014","journal-title":"Neoplasia"},{"key":"2023111612421566800_DEV202152C56","doi-asserted-by":"publisher","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT-PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"2023111612421566800_DEV202152C57","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/S0143-4004(80)80012-9","article-title":"Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy","volume":"1","author":"Pijnenborg","year":"1980","journal-title":"Placenta"},{"key":"2023111612421566800_DEV202152C58","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1016\/S0143-4004(83)80043-5","article-title":"Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy","volume":"4","author":"Pijnenborg","year":"1983","journal-title":"Placenta"},{"key":"2023111612421566800_DEV202152C59","doi-asserted-by":"publisher","first-page":"648","DOI":"10.1111\/j.1471-0528.1991.tb13450.x","article-title":"Placental bed spiral arteries in the hypertensive disorders of pregnancy","volume":"98","author":"Pijnenborg","year":"1991","journal-title":"Br. J. Obstet. Gynaecol."},{"key":"2023111612421566800_DEV202152C60","doi-asserted-by":"publisher","first-page":"939","DOI":"10.1016\/j.placenta.2005.12.006","article-title":"The uterine spiral arteries in human pregnancy: facts and controversies","volume":"27","author":"Pijnenborg","year":"2006","journal-title":"Placenta"},{"key":"2023111612421566800_DEV202152C61","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1016\/j.placenta.2015.01.009","article-title":"Expression pattern and function of Notch2 in different subtypes of first trimester cytotrophoblast","volume":"36","author":"Plessl","year":"2015","journal-title":"Placenta"},{"key":"2023111612421566800_DEV202152C62","doi-asserted-by":"publisher","first-page":"2597","DOI":"10.3389\/fimmu.2018.02597","article-title":"Regulation of placental extravillous trophoblasts by the maternal uterine environment","volume":"9","author":"Pollheimer","year":"2018","journal-title":"Front. Immunol."},{"key":"2023111612421566800_DEV202152C63","doi-asserted-by":"publisher","first-page":"1825","DOI":"10.1128\/MCB.20.5.1825-1835.2000","article-title":"Calcium depletion dissociates and activates heterodimeric notch receptors","volume":"20","author":"Rand","year":"2000","journal-title":"Mol. Cell. Biol."},{"key":"2023111612421566800_DEV202152C64","doi-asserted-by":"publisher","first-page":"e2204069119","DOI":"10.1073\/pnas.2204069119","article-title":"Hippo signaling cofactor, WWTR1, at the crossroads of human trophoblast progenitor self-renewal and differentiation","volume":"119","author":"Ray","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023111612421566800_DEV202152C65","doi-asserted-by":"publisher","first-page":"594","DOI":"10.1016\/0046-8177(95)90162-0","article-title":"Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast","volume":"26","author":"Redline","year":"1995","journal-title":"Hum. Pathol."},{"key":"2023111612421566800_DEV202152C66","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1007\/s00018-022-04475-z","article-title":"How trophoblasts fuse: an in-depth look into placental syncytiotrophoblast formation","volume":"79","author":"Renaud","year":"2022","journal-title":"Cell. Mol. Life Sci."},{"key":"2023111612421566800_DEV202152C67","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/j.bpobgyn.2011.02.006","article-title":"Placental bed disorders in preterm labor, preterm PROM, spontaneous abortion and abruptio placentae","volume":"25","author":"Romero","year":"2011","journal-title":"Best Pract. Res. Clin. Obstet. Gynaecol."},{"key":"2023111612421566800_DEV202152C68","doi-asserted-by":"publisher","first-page":"17864","DOI":"10.1073\/pnas.2002449117","article-title":"TEAD4 ensures postimplantation development by promoting trophoblast self-renewal: An implication in early human pregnancy loss","volume":"117","author":"Saha","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023111612421566800_DEV202152C69","doi-asserted-by":"publisher","first-page":"dev199840","DOI":"10.1242\/dev.199840","article-title":"Cell trajectory modeling identifies a primitive trophoblast state defined by BCAM enrichment","volume":"149","author":"Shannon","year":"2022","journal-title":"Development"},{"key":"2023111612421566800_DEV202152C70","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1101\/gad.1383706","article-title":"The Notch coactivator, MAML1, functions as a novel coactivator for MEF2C-mediated transcription and is required for normal myogenesis","volume":"20","author":"Shen","year":"2006","journal-title":"Genes Dev."},{"key":"2023111612421566800_DEV202152C71","doi-asserted-by":"publisher","first-page":"dev199749","DOI":"10.1242\/dev.199749","article-title":"Characterization of primary models of human trophoblast","volume":"148","author":"Sheridan","year":"2021","journal-title":"Development"},{"key":"2023111612421566800_DEV202152C72","doi-asserted-by":"publisher","first-page":"1235","DOI":"10.1152\/physrev.00005.2017","article-title":"Notch signaling in development, tissue homeostasis, and disease","volume":"97","author":"Siebel","year":"2017","journal-title":"Physiol. Rev."},{"key":"2023111612421566800_DEV202152C73","doi-asserted-by":"publisher","first-page":"dev163428","DOI":"10.1242\/dev.163428","article-title":"Development of the human placenta","volume":"146","author":"Turco","year":"2019","journal-title":"Development"},{"key":"2023111612421566800_DEV202152C74","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1038\/s41586-018-0753-3","article-title":"Trophoblast organoids as a model for maternal-fetal interactions during human placentation","volume":"564","author":"Turco","year":"2018","journal-title":"Nature"},{"key":"2023111612421566800_DEV202152C75","doi-asserted-by":"publisher","first-page":"e2016517118","DOI":"10.1073\/pnas.2016517118","article-title":"ASCL2 reciprocally controls key trophoblast lineage decisions during hemochorial placenta development","volume":"118","author":"Varberg","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023111612421566800_DEV202152C76","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1038\/s41586-018-0698-6","article-title":"Single-cell reconstruction of the early maternal-fetal interface in humans","volume":"563","author":"Vento-Tormo","year":"2018","journal-title":"Nature"},{"key":"2023111612421566800_DEV202152C77","doi-asserted-by":"publisher","first-page":"767","DOI":"10.1016\/j.ajpath.2016.11.018","article-title":"Hypoxia Directs Human Extravillous Trophoblast Differentiation in a Hypoxia-Inducible Factor-Dependent Manner","volume":"187","author":"Wakeland","year":"2017","journal-title":"Am. J. Pathol."},{"key":"2023111612421566800_DEV202152C78","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1016\/B978-0-12-405943-6.00008-7","article-title":"Hey bHLH transcription factors","volume":"110","author":"Weber","year":"2014","journal-title":"Curr. Top. Dev. Biol."},{"key":"2023111612421566800_DEV202152C79","doi-asserted-by":"publisher","first-page":"2096","DOI":"10.1101\/gad.1450406","article-title":"c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia\/lymphoma","volume":"20","author":"Weng","year":"2006","journal-title":"Genes Dev."},{"key":"2023111612421566800_DEV202152C80","doi-asserted-by":"publisher","first-page":"1119","DOI":"10.1126\/science.1096187","article-title":"Intramembrane proteolysis: theme and variations","volume":"305","author":"Wolfe","year":"2004","journal-title":"Science"},{"key":"2023111612421566800_DEV202152C81","doi-asserted-by":"publisher","first-page":"7688","DOI":"10.1128\/MCB.22.21.7688-7700.2002","article-title":"Identification of a family of mastermind-like transcriptional coactivators for mammalian notch receptors","volume":"22","author":"Wu","year":"2002","journal-title":"Mol. Cell. Biol."},{"key":"2023111612421566800_DEV202152C82","doi-asserted-by":"publisher","first-page":"1227","DOI":"10.1016\/j.str.2015.05.001","article-title":"Insights into autoregulation of Notch3 from structural and functional studies of its negative regulatory region","volume":"23","author":"Xu","year":"2015","journal-title":"Structure"},{"key":"2023111612421566800_DEV202152C83","doi-asserted-by":"publisher","first-page":"613557","DOI":"10.3389\/fcell.2020.613557","article-title":"A dynamic role of mastermind-like 1: a journey through the main (path)ways between development and cancer","volume":"8","author":"Zema","year":"2020","journal-title":"Front. Cell Dev. Biol."},{"key":"2023111612421566800_DEV202152C84","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1016\/j.ccell.2016.07.005","article-title":"A critical role for Notch signaling in the formation of cholangiocellular carcinomas","volume":"30","author":"Zender","year":"2016","journal-title":"Cancer Cell"},{"key":"2023111612421566800_DEV202152C85","doi-asserted-by":"publisher","first-page":"16111","DOI":"10.1074\/jbc.M111.322107","article-title":"Reciprocal regulation of syndecan-2 and Notch signaling in vascular smooth muscle cells","volume":"287","author":"Zhao","year":"2012","journal-title":"J. Biol. Chem."},{"key":"2023111612421566800_DEV202152C86","doi-asserted-by":"publisher","first-page":"2152","DOI":"10.1172\/JCI119388","article-title":"Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome?","volume":"99","author":"Zhou","year":"1997","journal-title":"J. Clin. Invest."},{"key":"2023111612421566800_DEV202152C87","doi-asserted-by":"publisher","first-page":"2084","DOI":"10.1093\/bioinformatics\/bty895","article-title":"Heavy-tailed prior distributions for sequence count data: removing the noise and preserving large differences","volume":"35","author":"Zhu","year":"2019","journal-title":"Bioinformatics"}],"container-title":["Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202152\/3243564\/dev202152.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202152\/3246819\/dev202152.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/journals.biologists.com\/dev\/article-pdf\/doi\/10.1242\/dev.202152\/3246819\/dev202152.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,16]],"date-time":"2023-11-16T07:42:30Z","timestamp":1700120550000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dev\/article\/150\/22\/dev202152\/334740\/NOTCH3-signalling-controls-human-trophoblast-stem"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,11,15]]},"references-count":87,"journal-issue":{"issue":"22","published-print":{"date-parts":[[2023,11,15]]}},"URL":"https:\/\/doi.org\/10.1242\/dev.202152","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.07.03.547490","asserted-by":"object"}]},"ISSN":["0950-1991","1477-9129"],"issn-type":[{"value":"0950-1991","type":"print"},{"value":"1477-9129","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,15]]},"article-number":"dev202152"}}