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Citations to this article

Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?
Y Zhou, … , M Wheelock, C H Damsky
Y Zhou, … , M Wheelock, C H Damsky
Published May 1, 1997
Citation Information: J Clin Invest. 1997;99(9):2139-2151. https://doi.org/10.1172/JCI119387.
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Research Article Article has an altmetric score of 15

Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?

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Abstract

Establishment of the human placenta requires that fetal cytotrophoblast stem cells in anchoring chorionic villi become invasive. These cytotrophoblasts aggregate into cell columns and invade both the uterine interstitium and vasculature, anchoring the fetus to the mother and establishing blood flow to the placenta. Cytotrophoblasts colonizing spiral arterioles replace maternal endothelium as far as the first third of the myometrium. We show here that differentiating cytotrophoblasts transform their adhesion receptor phenotype so as to resemble the endothelial cells they replace. Cytotrophoblasts in cell columns show reduced E-cadherin staining and express VE-(endothelial) cadherin, platelet-endothelial adhesion molecule-1, vascular endothelial adhesion molecule-1, and alpha-4-integrins. Cytotrophoblasts in the uterine interstitium and maternal vasculature continue to express these receptors, and, like endothelial cells during angiogenesis, also stain for alphaVbeta3. In functional studies, alphaVbeta3 and VE-cadherin enhance, while E-cadherin restrains, cytotrophoblast invasiveness. Cytotrophoblasts expressing alpha4 integrins bound immobilized VCAM-1 in vitro, suggesting that this receptor-pair could mediate cytotrophoblast-endothelium or cytotrophoblast-cytotrophoblast interactions in vivo, during endovascular invasion. In the pregnancy disorder preeclampsia, in which endovascular invasion remains superficial, cytotrophoblasts fail to express most of these endothelial markers (Zhou et al., 1997. J. Clin. Invest. 99:2152-2164.), suggesting that this adhesion phenotype switch is required for successful endovascular invasion and normal placentation.

Authors

Y Zhou, S J Fisher, M Janatpour, O Genbacev, E Dejana, M Wheelock, C H Damsky

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Total citations by year

Year: 2025 2024 2023 2022 2021 2020 2019 2018 2017 2016 2015 2014 2013 2012 2011 2010 2009 2008 2007 2006 2005 2004 2003 2002 2001 2000 1999 1998 1997 1995 1994 1991 Total
Citations: 3 7 11 14 15 24 22 22 29 23 26 28 36 20 25 24 30 35 31 34 35 32 34 24 23 30 23 16 4 1 1 1 683
Citation information
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Citations to this article in year 2014 (28)

Title and authors Publication Year
The Ubiquitin Ligase ASB4 Promotes Trophoblast Differentiation through the Degradation of ID2
WH Townley-Tilson, Y Wu, JE Ferguson, C Patterson, C Oudejans
PloS one 2014
LIMK1 Regulates Human Trophoblast Invasion/Differentiation and Is Down-Regulated in Preeclampsia
Y Zhou, A Yuge, AM Rajah, G Unek, PF Rinaudo, E Maltepe
The American Journal of Pathology 2014
Elastin-derived peptides stimulate trophoblast migration and invasion: a positive feedback loop to enhance spiral artery remodelling
M Desforges, LK Harris, JD Aplin
Molecular Human Reproduction 2014
Wnt-Dependent T-Cell Factor-4 Controls Human Etravillous Trophoblast Motility
G Meinhardt, S Haider, P Haslinger, K Proestling, C Fiala, J Pollheimer, M Knöfler
Endocrinology 2014
Decidual natural killer cell receptor expression is altered in pregnancies with impaired vascular remodeling and a higher risk of pre-eclampsia
AE Wallace, GS Whitley, B Thilaganathan, JE Cartwright
Journal of leukocyte biology 2014
Oxygen Modulates Human Decidual Natural Killer Cell Surface Receptor Expression and Interactions with Trophoblasts
AE Wallace, SS Goulwara, GS Whitley, JE Cartwright
Biology of reproduction 2014
Antiphospholipid antibodies and the placenta: a systematic review of their in vitro effects and modulation by treatment
M Tong, CA Viall, LW Chamley
Human Reproduction Update 2014
HCMV Infection of Human Trophoblast Progenitor Cells of the Placenta Is Neutralized by a Human Monoclonal Antibody to Glycoprotein B and Not by Antibodies to the Pentamer Complex
M Zydek, M Petitt, J Fang-Hoover, B Adler, L Kauvar, L Pereira, T Tabata
Viruses 2014
Trophoblast retrieval and isolation from the cervix (TRIC) for noninvasive prenatal screening at 5 to 20 weeks of gestation
JM Bolnick, BA Kilburn, S Bajpayee, N Reddy, R Jeelani, B Crone, N Simmerman, M Singh, MP Diamond, DR Armant
Fertility and Sterility 2014
Increased angiogenic factor secretion by decidual natural killer cells from pregnancies with high uterine artery resistance alters trophoblast function
AE Wallace, R Fraser, S Gurung, SS Goulwara, GS Whitley, AP Johnstone, JE Cartwright
Human Reproduction 2014
The multidrug-resistance transporter ABCB5 is expressed in human placenta
ER Volpicelli, C Lezcano, Q Zhan, SD Girouard, DW Kindelberger, MH Frank, NY Frank, CP Crum, GF Murphy
International Journal of Gynecological Pathology 2014
Noninvasive and Quantitative Assessment of In Vivo Fetomaternal Interface Angiogenesis Using RGD-Based Fluorescence
M Keramidas, J Lavaud, F Sergent, P Hoffmann, S Brouillet, JJ Feige, JL Coll, N Alfaidy
BioMed Research International 2014
Angiogenin Expression during Early Human Placental Development; Association with Blood Vessel Formation
N Pavlov, JL Frendo, J Guibourdenche, SA Degrelle, D Evain-Brion, J Badet
BioMed Research International 2014
Signaling pathways in mouse and human trophoblast differentiation: a comparative review
F Soncin, D Natale, MM Parast
Cellular and Molecular Life Sciences 2014
Oxygen regulates human cytotrophoblast migration by controlling chemokine and receptor expression
A Schanz, K Red-Horse, AP Hess, DM Baston-Büst, C Heiss, JS Krüssel
Placenta 2014
p63 Inhibits Extravillous Trophoblast Migration and Maintains Cells in a Cytotrophoblast Stem Cell-Like State
Y Li, M Moretto-Zita, S Leon-Garcia, MM Parast
The American Journal of Pathology 2014
Review: The ADAM metalloproteinases – Novel regulators of trophoblast invasion?
J Pollheimer, V Fock, M Knöfler
Placenta 2014
Expression of Gadd45α in human early placenta and its role in trophoblast invasion
X Liu, H Mu, X Luo, X Xiao, Y Ding, N Yin, Q Deng, H Qi
Placenta 2014
Development of the hemochorial maternal vascular spaces in the placenta through endothelial and vasculogenic mimicry
A Rai, JC Cross
Developmental Biology 2014
An integrative view on the physiology of human early placental villi
B Huppertz, D Ghosh, J Sengupta
Progress in Biophysics and Molecular Biology 2014
Tetrabromobisphenol A activates inflammatory pathways in human first trimester extravillous trophoblasts in vitro
HR Park, PW Kamau, C Korte, R Loch-Caruso
Reproductive Toxicology 2014
Evaluation of inflammatory mediators in the deciduas of pregnant women with pre-eclampsia/eclampsia
AB Peixoto, EA Júnior, JU Ribeiro, DB Rodrigues, EC Castro, TM Caldas, VR Júnior
Journal of Maternal-Fetal and Neonatal Medicine 2014
Discovery of a Cell: Reflections on the Checkered History of Intermediate Trophoblast and Update on its Nature and Pathologic Manifestations
RJ Kurman, IM Shih
International Journal of Gynecological Pathology 2014
Hyperglycemia impairs cytotrophoblast function via stress signaling
C Cawyer, D Horvat, D Leonard, SR Allen, RO Jones, DC Zawieja, TJ Kuehl, MN Uddin
American Journal of Obstetrics and Gynecology 2014
Calcitonin gene- and parathyroid hormone-related peptides in normotensive and preeclamptic pregnancies: a nested case–control study
S Yadav, YS Yadav, MM Goel, U Singh, SM Natu, MP Negi
Archives of Gynecology and Obstetrics 2014
Pathobiology of Human Disease
S Akilesh
Pathobiology of Human Disease 2014
A new marker set that identifies fetal cells in maternal circulation with high specificity: Fetal cell identification in maternal blood
L Hatt, M Brinch, R Singh, K Møller, RH Lauridsen, JM Schlütter, N Uldbjerg, B Christensen, S Kølvraa
Prenatal Diagnosis 2014
Differential Methylation of Genes Associated with Cell Adhesion in Preeclamptic Placentas
L Anton, AG Brown, MS Bartolomei, MA Elovitz, C Oudejans
PloS one 2014

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