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Frontiers in Biology

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CN 11-5892/Q

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Front Biol    2011, Vol. 6 Issue (4) : 300-311    https://doi.org/10.1007/s11515-011-1120-z
REVIEW
Developmental genes during placentation: insights from mouse mutants
Jinhua LU1,2, Qiang WANG1,2, Bingyan WANG1, Fengchao WANG1, Haibin WANG1()
1. State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; 2. Graduate University of the Chinese Academy of Sciences, Beijing 100039, China
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Abstract

Placenta, a temporary organ first formed during the development of a new life is essential for the survival and growth of the fetus in eutherian mammals. It serves as an interface for the exchange of nutrients, gases and wastes between the maternal and fetal compartments. During the past decades, studies employing gene-engineered mouse mutants have revealed a wide range of signaling molecules governing the trophoblast development and function during placentation under various pathophysiological conditions. Here, we summarize the recent progress with particular respect to the involvement of developmental genes during placentation.
Keywords developmental gene      placentation      mouse mutant     
Corresponding Author(s): WANG Haibin,Email:hbwang@ioz.ac.cn   
Issue Date: 01 August 2011
 Cite this article:   
Jinhua LU,Qiang WANG,Bingyan WANG, et al. Developmental genes during placentation: insights from mouse mutants[J]. Front Biol, 2011, 6(4): 300-311.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-011-1120-z
https://academic.hep.com.cn/fib/EN/Y2011/V6/I4/300
Fig.1  A diagram showing the development of mouse placenta. The development of placenta from embryonic day (E) 4.0-E12.5, showing the origin of the trophoblast, primitive endoderm, ICM and extra-embryonic mesoderm lineages and derivatives.
GeneExpression in placentasPlacenta phenotype of mutant miceReference
Fgfr2Trophectoderm and its derived extraembryonic ectodermFailure of chorioallantoic fusion; Defect of fetal vascular invasion into chorionArman et al., 1998; Xu et al., 1998
PLCδ1/PLCδ3Placenta trophoblastReduced vascularization, proliferation and aberrant apoptosis in labyrinth areaNakamura et al., 2005
Pkbα (Akt1)Trophoblast giant cell, spongiotrophoblast, labyrinth, the endothelium of fetal capillariesSmall layer of labyrinth and spongiotrophoblast; marked reduction of glycogen-containing cells in spongiotrophoblast; disordered fetal vasculature with fewer vesselsYang et al., 2003
Gab1Labyrinth trophoblast cells and spongiotrophoblast CellsSeverely reduced number of trophoblast cells in the labyrinth regionItoh et al., 2000
Grb2UnknownDefects in chorioallantoic fusion, smaller labyrinth structuresSaxton et al., 2001
Sos1Trophoblast giant cell, spongiotrophoblast, labyrinth layerDisorganized spongiotrophoblastand labyrinth trophoblast layers, incomplete embryonic vasculature in labyrinthQian et al., 2000
B-RafUnknownDiscontinuous spongiotrophoblast and giant trophoblast layers, underdeveloped labyrinth layer (hypocellular areas filled with stroma in labyrinth)Galabova-Kovacs et al., 2006
C-raf-1UnknownReduced size of spongiotrophoblast and the labyrinth layer, poorly vascularized and abundant mesenchymal cells-contained labyrinth layerMikula et al., 2001
Mekk3 (Map3k3)UnknownReduced embryonic blood vessels in the labyrinth layerYang et al., 2000
Mekk4 (Map3k4)Labyrinth, spongiotrophoblast, and giant cell layersA point mutation exhibited dysregulated placental development with increased trophoblast invasion.Abell et al., 2009
Mek1 (Map2k1)Labyrinth layerLess defined spongiotrophoblast layer, more compact labyrinthine region with fewer blood vesselsGiroux et al., 1999; Bissonauth et al., 2006; Nadeau et al., 2009
Erk2 (Mapk1)Trophoectoderm and its derivatives including ectoplacental cone, extraembryonic ectoderm and giant cellsFailure to form the ectoplacental cone and extraembryonic ectoderm in ERK2 (Ex3) mutants; Thinner labyrinthine layers, few fetal blood vessels penetrating into the labyrinthine layer in Erk2 (Ex2) mutants.Hatano et al., 2003; Saba-El-Leil et al., 2003
Erk5 (Mapk7)Labyrinth layerThinner labyrinth layer, less intermixing between embryonic and maternal blood vessels in the labyrinthine region, more apoptosis.Regan et al., 2002; Sohn et al., 2002; Yan et al., 2003
FRS2αExtraembryonic ectodermTrophoblast stem cells failed to maintenance of self-renewing.Melillo et al., 2001; Gotoh et al., 2005
p38α (Mapk14)Diploid trophoblast of the placenta, including the labyrinth, yolk sacThinner labyrinth layer, greatly reduced spongiotrophoblast,decreased vascular network within the labyrinth layerAdams et al., 2000; Mudgett et al., 2000
Shp2 (Ptpn11)Spongiotrophoblast and labyrinth trophoblast (unpublished data)Diminished numbers of trophoblast giant cells, and failure to yield trophoblast stem (TS) cell lines.Yang et al., 2006
Tab.1  The placenta phenotype of FGF family mutant mice
Fig.2  The regulation of developmental genes during trophoblast development and cell lineage specification.
GeneExpression in placentasPlacenta phenotype of mutant miceReference
Wnt2Allantois, fetal blood vessels in the labyrinth (unpublished data)Defects of vascularization in placentaMonkley et al., 1996
Wnt7bChorionic trophoblastDefects in chorioallantoic attachment and cell organization in chorionic plateParr et al., 2001
Fzd5Labyrinth trophoblast, yolk sacSmall labyrinth, failure of fetal vascular invasion into the chorion, defects in yolk sac angiogenesisIshikawa et al., 2001
Tcf1/Lef1Placenta trophoblast (unpublished data)Unknown defect in placentaGalceran et al., 1999
Tab.2  The placenta phenotype of Wnt family mutant mice.
GeneExpression in placentasPlacenta phenotype of mutant miceReference
Jagged 1UnknownDied at E10.0 due to the vascular defects.Large blood vessels were not present in the yolk sac.Xue et al., 1999
Delta-like 4Trophoblast giant cells, umbilical and vitelline arteriesAt E10.5 no viable null embryos were found. Yolk sac defects. Haploid insufficiency leads embryonic lethality. Vascular remodeling defects in the yolk sacs and the major central placenta arteries undergo degeneration and regression.Duarte et al., 2004; Gale et al., 2004
Notch 1Vascular endothelial cells in labyrinth, maternal blood sinus (unpublished data)Single knockout null embryos died before E11.5, but had no placenta defects. Conditional knockout (with tie2-cre) had yolk sac vascular remodeling failure and placenta blood vessels labyrinth invasion defects.Swiatek et al., 1994; Limbourg et al., 2005
Notch 2Allantois, spongiotrophoblast, giant cells, endovascular trophoblasts and mesenchymal derivatives in labyrinthDelayed entry of maternal blood into the mutant placenta and poor blood sinus formation at later stages.Nakayama et al., 1997; Hamada et al., 1999; Hamada et al., 2007
Notch 4Vascular endothelial cells in labyrinthSingle knockout exhibited no obvious mutant phenotype. Notch 1 and Notch 4 double knockout had pale yolk sacs, lacking obvious blood vessels and failture of mutant endothelial cells to invade the labyrinth.Krebs et al., 2000
RBP-J kappaMesodermal derivatives in labyrinthDied before E10.0 due to the deficiency of chorioallantoic fusion.Oka et al., 1995; Krebs et al., 2004
Hey1 and Hey2Blood vessels of the allantois and chorionic plateComplete lack of embryonic blood vessels in the placental labyrinth.Fischer et al., 2004
Mash2Ectoplacental cone, chorion and their derivatives in the placentaDied at E10.0 because of the placental defects. No spongiotrophoblast cells and their precursors, more trophoblast giant cells.Guillemot et al., 1994; Tanaka et al., 1997
Tab.3  The placenta phenotype of Notch family mutant mice
GeneExpression in placentasPlacenta phenotype of mutant miceReference
TGF-β1Extraembryonic blood islands of the yolk sac, mesodermal cells of the allantoisAbout 50% homozygous and 25% heterozygous embryos died around E10.5. The yolk sac vasculature defects.Akhurst et al., 1990; Dickson et al., 1995
NodalSpongiotrophoblastsInsertional null mutant loss of the diploid spongiotrophoblasts and labyrinth, and had more giant cells. Hypomorphic mutation results in an expansion of the giant cell and spongiotrophoblast layers, and a decrease in labyrinthine development.Iannaccone et al., 1992; Ma et al., 2001
Bmp2Extraembryonic mesoderm, allantois.Died at midgestation. Allantois had delayed development.Winnier et al., 1995
Bmp4AllantoisDied between E6.5-E9.5. Yolk sac defects, reduced blood islands and no allantois.Zhang and Bradley, 1996; Lawson et al., 1999
Bmp5and 7Allantois, endoderm of the visceral yolk sac.Died at E10.5. Allantois developed abnormal. Failure of chorioallantoic fusion.Solloway and Robertson, 1999
Bmp8bExtraembryonic ectoderm.Short allantois, no allantois in some more severe mutant.Lawler et al., 1994; Oshima et al., 1996
TGF-β receptorType IIExtraembryonic blood islands of the yolk sac, mesodermal cells of the allantoisHomozygous embryos died around E10.5. Yolk sac hematopoiesis and vasculogenesis.Ying et al., 2000
Alk1endothelial cells of fetal vesselsDilated and fused chorioallantoic vessels.Lechleider et al., 2001; Tremblay et al., 2001
Smad 1Yolk sac, allantoisMutant embryos died around E9.5 due to the defects of allantois formation. The abnormal allantois failed to fuse to the chorion.Hong et al., 2007
Smad 5Allantois, yolk sacHomozygous mutant died between E9.5 and E11.5. Allantois lacked a well-organized vasculature. Allantois could fuse to the chorion, but was not well-elongated.Chang et al., 1999
P300UnknownNull embryos died between E9.0 and E11.5. The yolk sac was poorly vascularized.Yao et al., 1998
CBPUnknownHomozygous embryos died between E9.5 and E10.5. Decreased in erythroid cells and colony-forming cells in the yolk sac.Oike et al., 1999
Tab.4  The placenta phenotype of TGF beta family mutant mice
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