Trophoblast Development in the Murine Preimplantation Embryo

Abstract

Trophoblast cells of the murine placenta are derived from the trophectoderm (TE) cells of the preimplantation embryo. Establishment of the TE cell lineage is the result of a cell segregation event early in blastomere division. Models of cell lineage segregation suggest it is driven by the internalization of spatial information which induce or inhibit specific signaling pathways. Once segregated, TE cells undergo a differentiation event, resulting in both proliferative and terminally differentiated trophoblast cells. Thus, the development of a healthy, functional placenta relies on the well-choreographed events of trophoblast segregation, proliferation and differentiation. The pre and peri-implantation events that contribute to the development of the four main types of placental trophoblasts are the subject of this review. Identifying the components and promotors of trophoblast development will lead to a more comprehensive understanding of diseases associated with abnormal placentation and recurrent pregnancy loss.

Keywords

trophoblast - preimplantation - differentiation - segregation

• References

• 1 Pedersen RA, Wu K, Bałakier H. Origin of the inner cell mass in mouse embryos: cell lineage analysis by microinjection. Dev Biol 1986; 117 (2) 581-595
• 2 Senner CE, Hemberger M. Regulation of early trophoblast differentiation - lessons from the mouse. Placenta 2010; 31 (11) 944-950
• 3 Tarkowski AK, Wróblewska J. Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J Embryol Exp Morphol 1967; 18 (1) 155-180
• 4 Shirayoshi Y, Okada TS, Takeichi M. The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. Cell 1983; 35 (3, Pt 2): 631-638
• 5 Reeve WJ, Kelly FP. Nuclear position in the cells of the mouse early embryo. J Embryol Exp Morphol 1983; 75: 117-139
• 6 Johnson MH, Ziomek CA. The foundation of two distinct cell lineages within the mouse morula. Cell 1981; 24 (1) 71-80
• 7 Wennekamp S, Mesecke S, Nédélec F, Hiiragi T. A self-organization framework for symmetry breaking in the mammalian embryo. Nat Rev Mol Cell Biol 2013; 14 (7) 452-459
• 8 Dard N, Le T, Maro B, Louvet-Vallée S. Inactivation of aPKClambda reveals a context dependent allocation of cell lineages in preimplantation mouse embryos. PLoS ONE 2009; 4 (9) e7117
• 9 Plusa B, Frankenberg S, Chalmers A , et al. Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. J Cell Sci 2005; 118 (Pt 3): 505-515
• 10 Alarcon VB. Cell polarity regulator PARD6B is essential for trophectoderm formation in the preimplantation mouse embryo. Biol Reprod 2010; 83 (3) 347-358
• 11 Nichols J, Zevnik B, Anastassiadis K , et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998; 95 (3) 379-391
• 12 Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17 (1) 126-140
• 13 Nishioka N, Yamamoto S, Kiyonari H , et al. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech Dev 2008; 125 (3–4) 270-283
• 14 Ralston A, Cox BJ, Nishioka N , et al. Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 2010; 137 (3) 395-403
• 15 Cockburn K, Rossant J. Making the blastocyst: lessons from the mouse. J Clin Invest 2010; 120 (4) 995-1003
• 16 Dietrich JE, Hiiragi T. Stochastic patterning in the mouse pre-implantation embryo. Development 2007; 134 (23) 4219-4231
• 17 Niwa H, Toyooka Y, Shimosato D , et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005; 123 (5) 917-929
• 18 Ralston A, Rossant J. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol 2008; 313 (2) 614-629
• 19 Stephenson RO, Yamanaka Y, Rossant J. Disorganized epithelial polarity and excess trophectoderm cell fate in preimplantation embryos lacking E-cadherin. Development 2010; 137 (20) 3383-3391
• 20 Hirate Y, Cockburn K, Rossant J, Sasaki H. Tead4 is constitutively nuclear, while nuclear vs. cytoplasmic Yap distribution is regulated in preimplantation mouse embryos. Proc Natl Acad Sci U S A 2012; 109 (50) E3389-E3390 , author reply E3391–E3392
• 21 Zhao B, Wei X, Li W , et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007; 21 (21) 2747-2761
• 22 Nishioka N, Inoue K, Adachi K , et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell 2009; 16 (3) 398-410
• 23 Lorthongpanich C, Issaragrisil S. Emerging role of the hippo signaling pathway in position sensing and lineage specification in mammalian embryos. Biol Reprod 2015; 92 (6) 143
• 24 Genevet A, Tapon N. The Hippo pathway and apico-basal cell polarity. Biochem J 2011; 436 (2) 213-224
• 25 Vinot S, Le T, Ohno S, Pawson T, Maro B, Louvet-Vallée S. Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. Dev Biol 2005; 282 (2) 307-319
• 26 Hirate Y, Hirahara S, Inoue K , et al. Polarity-dependent distribution of angiomotin localizes Hippo signaling in preimplantation embryos. Curr Biol 2013; 23 (13) 1181-1194
• 27 Sasaki H. Position- and polarity-dependent Hippo signaling regulates cell fates in preimplantation mouse embryos. Semin Cell Dev Biol 2015; 15: 100-107
• 28 Wells CD, Fawcett JP, Traweger A , et al. A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell 2006; 125 (3) 535-548
• 29 Sugihara-Mizuno Y, Adachi M, Kobayashi Y , et al. Molecular characterization of angiomotin/JEAP family proteins: interaction with MUPP1/Patj and their endogenous properties. Genes Cells 2007; 12 (4) 473-486
• 30 Wada K, Itoga K, Okano T, Yonemura S, Sasaki H. Hippo pathway regulation by cell morphology and stress fibers. Development 2011; 138 (18) 3907-3914
• 31 Hirate Y, Sasaki H. The role of angiomotin phosphorylation in the Hippo pathway during preimplantation mouse development. Tissue Barriers 2014; 2 (1) e28127
• 32 Cao Z, Carey TS, Ganguly A, Wilson CA, Paul S, Knott JG. Transcription factor AP-2γ induces early Cdx2 expression and represses HIPPO signaling to specify the trophectoderm lineage. Development 2015; 142 (9) 1606-1615
• 33 Rayon T, Menchero S, Nieto A , et al. Notch and hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev Cell 2014; 30 (4) 410-422
• 34 Rappolee DA, Basilico C, Patel Y, Werb Z. Expression and function of FGF-4 in peri-implantation development in mouse embryos. Development 1994; 120 (8) 2259-2269
• 35 Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998; 282 (5396) 2072-2075
• 36 Ornitz DM, Itoh N. Fibroblast growth factors. Genome Biol 2001; 2 (3) S3005
• 37 Itoh N, Ornitz DM. Evolution of the Fgf and Fgfr gene families. Trends Genet 2004; 20 (11) 563-569
• 38 Thisse B, Thisse C. Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 2005; 287 (2) 390-402
• 39 Gardner RL, Papaioannou VE, Barton SC. Origin of the ectoplacental cone and secondary giant cells in mouse blastocysts reconstituted from isolated trophoblast and inner cell mass. J Embryol Exp Morphol 1973; 30 (3) 561-572
• 40 Oda M, Shiota K, Tanaka S. Trophoblast stem cells. Methods Enzymol 2006; 419: 387-400
• 41 Tesser RB, Scherholz PL, do Nascimento L, Katz SG. Trophoblast glycogen cells differentiate early in the mouse ectoplacental cone: putative role during placentation. Histochem Cell Biol 2010; 134 (1) 83-92
• 42 Bruick RK, McKnight SL. Transcription. Oxygen sensing gets a second wind. Science 2002; 295 (5556) 807-808
• 43 Kallio PJ, Wilson WJ, O'Brien S, Makino Y, Poellinger L. Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J Biol Chem 1999; 274 (10) 6519-6525
• 44 De Marco CS, Caniggia I. Mechanisms of oxygen sensing in human trophoblast cells. Placenta 2002; 23 (Suppl A): S58-S68
• 45 Caniggia I, Winter JL. Adriana and Luisa Castellucci Award lecture 2001. Hypoxia inducible factor-1: oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies—a review. Placenta 2002; 23 (Suppl A): S47-S57
• 46 Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 1996; 97 (2) 540-550
• 47 Adelman DM, Maltepe E, Simon MC. HIF-1 is essential for multilineage hematopoiesis in the embryo. Adv Exp Med Biol 2000; 475: 275-284
• 48 Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 1997; 386 (6623) 403-407
• 49 Kozak KR, Abbott B, Hankinson O. ARNT-deficient mice and placental differentiation. Dev Biol 1997; 191 (2) 297-305
• 50 Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 2000; 14 (24) 3191-3203
• 51 Yung HW, Atkinson D, Campion-Smith T, Olovsson M, Charnock-Jones DS, Burton GJ. Differential activation of placental unfolded protein response pathways implies heterogeneity in causation of early- and late-onset pre-eclampsia. J Pathol 2014; 234 (2) 262-276
• 52 Fradet S, Pierredon S, Ribaux P , et al. Involvement of membrane GRP78 in trophoblastic cell fusion. PLoS ONE 2012; 7 (8) e40596
• 53 Rzymski T, Harris AL. The unfolded protein response and integrated stress response to anoxia. Clin Cancer Res 2007; 13 (9) 2537-2540
• 54 Oskolkova OV, Afonyushkin T, Leitner A , et al. ATF4-dependent transcription is a key mechanism in VEGF up-regulation by oxidized phospholipids: critical role of oxidized sn-2 residues in activation of unfolded protein response. Blood 2008; 112 (2) 330-339
• 55 Iwawaki T, Akai R, Yamanaka S, Kohno K. Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability. Proc Natl Acad Sci U S A 2009; 106 (39) 16657-16662
• 56 Ghosh R, Lipson KL, Sargent KE , et al. Transcriptional regulation of VEGF-A by the unfolded protein response pathway. PLoS ONE 2010; 5 (3) e9575