Transcription Factors That Regulate Trophoblast Development and Function

Progress in Molecular Biology and Translational Science

Volumn 145, Issue , 2017, Pages 39-88

  Baines, K J ^a   Renaud, S J ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Cell proliferation and differentiation; Placenta; Syncytialization; Transcription factors; Trophoblast; Trophoblast stem cells

Indexed keywords

ACHAETE SCUTE FAMILY BHLH TRANSCRIPTION FACTOR 2; AT RICH INTERACTIVE DOMAIN 3A PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DISTALLESS 3 PROTEIN; E74 LIKE FACTOR 5; EOMESODERMIN; ESTROGEN RELATED RECEPTOR BETA; FORKHEAD BOX D3 PROTEIN; IKAROS FAMILY ZINC FINGER PROTEIN 1; INHIBITOR OF DIFFERENTIATION PROTEIN; KRUPPEL LIKE FACTOR 6; MYC PROTEIN; OVO LIKE 1 PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PROTEIN FOS; PROTEIN P63; RETINOID X RECEPTOR ALPHA; TEA DOMAIN FAMILY MEMBER 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR ETS1; TRANSCRIPTION FACTOR ETS2; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR GCM1; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR TEAD3; TRANSCRIPTION FACTOR TFAP2; TRANSCRIPTION FACTOR TFAP2C; UNCLASSIFIED DRUG; WW DOMAIN CONTAINING TRANSCRIPTION REGULATOR 1; YES ASSOCIATED PROTEIN;

CELL FUNCTION; CELL MATURATION; CELL SELF-RENEWAL; CELL SPECIFICITY; CHORION VILLUS; CYTOTROPHOBLAST; DECIDUA; EMBRYO DEVELOPMENT; FETOMATERNAL TRANSFUSION; HUMAN; MATERNAL BLOOD; NONHUMAN; NUTRIENT UPTAKE; PLACENTA; PLACENTA CIRCULATION; PROTEIN FUNCTION; REGULATORY MECHANISM; STROMA; TROPHOBLAST; ANIMAL; BIOLOGICAL MODEL; CELL LINEAGE; CYTOLOGY; FETUS BLOOD; METABOLISM;

ANIMALS; CELL LINEAGE; FETAL BLOOD; HUMANS; MODELS, BIOLOGICAL; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 85009415806     PISSN: 18771173     EISSN: 18780814     Source Type: Book Series    
DOI: 10.1016/bs.pmbts.2016.12.003     Document Type: Chapter

References (254)

1. 1 Niakan, K.K., Han, J., Pedersen, R.A., Simon, C., Pera, R.A., Human pre-implantation embryo development. Development 139:5 (2012), 829–841.
2. 2 Rossant, J., Tam, P.P., Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136:5 (2009), 701–713.
3. 3 Genbacev, O.D., Prakobphol, A., Foulk, R.A., et al. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science 299:5605 (2003), 405–408.
4. 4 Benirschke, K., Burton, G.J., Baergen, R.N., Pathology of the Human Placenta. 6th ed., 2012, Springer, New York.
5. 5 Enders, A.C., Trophoblast differentiation during the transition from trophoblastic plate to lacunar stage of implantation in the rhesus monkey and human. Am J Anat 186:1 (1989), 85–98.
6. 6 Enders, A.C., King, B.F., Formation and differentiation of extraembryonic mesoderm in the rhesus monkey. Am J Anat 181:4 (1988), 327–340.
7. 7 Rossant, J., Cross, J.C., Placental development: lessons from mouse mutants. Nat Rev Genet 2:7 (2001), 538–548.
8. 8 Quinn, J., Kunath, T., Rossant, J., Mouse trophoblast stem cells. Methods Mol Med 121 (2006), 125–148.
9. 9 Tanaka, S., Kunath, T., Hadjantonakis, A.K., Nagy, A., Rossant, J., Promotion of trophoblast stem cell proliferation by FGF4. Science 282:5396 (1998), 2072–2075.
10. 10 Erlebacher, A., Price, K.A., Glimcher, L.H., Maintenance of mouse trophoblast stem cell proliferation by TGF-beta/activin. Dev Biol 275:1 (2004), 158–169.
11. 11 Carter, A.M., Enders, A.C., Comparative aspects of trophoblast development and placentation. Reprod Biol Endocrinol, 2, 2004, 46.
12. 12 Knight, M., Redman, C.W., Linton, E.A., Sargent, I.L., Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br J Obstet Gynaecol 105:6 (1998), 632–640.
13. 13 Simpson, R.A., Mayhew, T.M., Barnes, P.R., From 13 weeks to term, the trophoblast of human placenta grows by the continuous recruitment of new proliferative units: a study of nuclear number using the disector. Placenta 13:5 (1992), 501–512.
14. 14 Mi, S., Lee, X., Li, X., et al. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:6771 (2000), 785–789.
15. 15 Blaise, S., de Parseval, N., Benit, L., Heidmann, T., Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci USA 100:22 (2003), 13013–13018.
16. 16 Malassine, A., Frendo, J.L., Evain-Brion, D., A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update 9:6 (2003), 531–539.
17. 17 Renaud, S.J., Kubota, K., Rumi, M.A., Soares, M.J., The FOS transcription factor family differentially controls trophoblast migration and invasion. J Biol Chem 289:8 (2014), 5025–5039.
18. 18 Wright, J.K., Dunk, C.E., Amsalem, H., Maxwell, C., Keating, S., Lye, S.J., HER1 signaling mediates extravillous trophoblast differentiation in humans. Biol Reprod 83:6 (2010), 1036–1045.
19. 19 Damsky, C.H., Fitzgerald, M.L., Fisher, S.J., Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest 89:1 (1992), 210–222.
20. 20 Jokhi, P.P., King, A., Loke, Y.W., Reciprocal expression of epidermal growth factor receptor (EGF-R) and c-erbB2 by non-invasive and invasive human trophoblast populations. Cytokine 6:4 (1994), 433–442.
21. 21 Pijnenborg, R., Vercruysse, L., Hanssens, M., The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 27:9–10 (2006), 939–958.
22. 22 Rodesch, F., Simon, P., Donner, C., Jauniaux, E., Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 80:2 (1992), 283–285.
23. 23 Jauniaux, E., Watson, A.L., Hempstock, J., Bao, Y.P., Skepper, J.N., Burton, G.J., Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 157:6 (2000), 2111–2122.
24. 24 Pijnenborg, R., Robertson, W.B., Brosens, I., Dixon, G., Review article: trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 2:1 (1981), 71–91.
25. 25 Damsky, C.H., Fisher, S.J., Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors. Curr Opin Cell Biol 10:5 (1998), 660–666.
26. 26 Simmons, D.G., Cross, J.C., Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev Biol 284:1 (2005), 12–24.
27. 27 Simmons, D.G., Fortier, A.L., Cross, J.C., Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev Biol 304:2 (2007), 567–578.
28. 28 Ain, R., Canham, L.N., Soares, M.J., Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: novel endocrine phenotype and regulation. Dev Biol 260:1 (2003), 176–190.
29. 29 Vercruysse, L., Caluwaerts, S., Luyten, C., Pijnenborg, R., Interstitial trophoblast invasion in the decidua and mesometrial triangle during the last third of pregnancy in the rat. Placenta 27:1 (2006), 22–33.
30. 30 Caluwaerts, S., Vercruysse, L., Luyten, C., Pijnenborg, R., Endovascular trophoblast invasion and associated structural changes in uterine spiral arteries of the pregnant rat. Placenta 26:7 (2005), 574–584.
31. 31 Soares, M.J., Chakraborty, D., Karim Rumi, M.A., Konno, T., Renaud, S.J., Rat placentation: an experimental model for investigating the hemochorial maternal-fetal interface. Placenta 33:4 (2012), 233–243.
32. 32 Hofmann, A.P., Gerber, S.A., Croy, B.A., Uterine natural killer cells pace early development of mouse decidua basalis. Mol Hum Reprod 20:1 (2014), 66–76.
33. 33 Knott, J.G., Paul, S., Transcriptional regulators of the trophoblast lineage in mammals with hemochorial placentation. Reproduction 148:6 (2014), R121–R136.
34. 34 Maltepe, E., Bakardjiev, A.I., Fisher, S.J., The placenta: transcriptional, epigenetic, and physiological integration during development. J Clin Invest 120:4 (2010), 1016–1025.
35. 35 Suwinska, A., Czolowska, R., Ozdzenski, W., Tarkowski, A.K., Blastomeres of the mouse embryo lose totipotency after the fifth cleavage division: expression of Cdx2 and Oct4 and developmental potential of inner and outer blastomeres of 16- and 32-cell embryos. Dev Biol 322:1 (2008), 133–144.
36. 36 Hillman, N., Sherman, M.I., Graham, C., The effect of spatial arrangement on cell determination during mouse development. J Embryol Exp Morphol 28:2 (1972), 263–278.
37. 37 Lorthongpanich, C., Doris, T.P., Limviphuvadh, V., Knowles, B.B., Solter, D., Developmental fate and lineage commitment of singled mouse blastomeres. Development 139:20 (2012), 3722–3731.
38. 38 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 16:3 (2009), 398–410.
39. 39 Nishioka, N., Yamamoto, S., Kiyonari, H., et al. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech Dev 125:3–4 (2008), 270–283.
40. 40 Home, P., Saha, B., Ray, S., et al. Altered subcellular localization of transcription factor TEAD4 regulates first mammalian cell lineage commitment. Proc Natl Acad Sci USA 109:19 (2012), 7362–7367.
41. 41 Yagi, R., Kohn, M.J., Karavanova, I., et al. Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134:21 (2007), 3827–3836.
42. 42 Hossain, Z., Ali, S.M., Ko, H.L., et al. Glomerulocystic kidney disease in mice with a targeted inactivation of Wwtr1. Proc Natl Acad Sci USA 104:5 (2007), 1631–1636.
43. 43 Morin-Kensicki, E.M., Boone, B.N., Howell, M., et al. Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol Cell Biol 26:1 (2006), 77–87.
44. 44 Strumpf, D., Mao, C.A., Yamanaka, Y., et al. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132:9 (2005), 2093–2102.
45. 45 Ralston, A., Rossant, J., Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol 313:2 (2008), 614–629.
46. 46 Chawengsaksophak, K., James, R., Hammond, V.E., Kontgen, F., Beck, F., Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386:6620 (1997), 84–87.
47. 47 Wu, G., Gentile, L., Fuchikami, T., et al. Initiation of trophectoderm lineage specification in mouse embryos is independent of Cdx2. Development 137:24 (2010), 4159–4169.
48. 48 Niwa, H., Toyooka, Y., Shimosato, D., et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123:5 (2005), 917–929.
49. 49 Blij, S., Frum, T., Akyol, A., Fearon, E., Ralston, A., Maternal Cdx2 is dispensable for mouse development. Development 139:21 (2012), 3969–3972.
50. 50 Jedrusik, A., Cox, A., Wicher, K.B., Glover, D.M., Zernicka-Goetz, M., Maternal-zygotic knockout reveals a critical role of Cdx2 in the morula to blastocyst transition. Dev Biol. 398:2 (2015), 147–152.
51. 51 Jedrusik, A., Bruce, A.W., Tan, M.H., et al. Maternally and zygotically provided Cdx2 have novel and critical roles for early development of the mouse embryo. Dev Biol 344:1 (2010), 66–78.
52. 52 Dietrich, J.E., Hiiragi, T., Stochastic patterning in the mouse pre-implantation embryo. Development 134:23 (2007), 4219–4231.
53. 53 Tolkunova, E., Cavaleri, F., Eckardt, S., et al. The caudal-related protein cdx2 promotes trophoblast differentiation of mouse embryonic stem cells. Stem Cells 24:1 (2006), 139–144.
54. 54 Niwa, H., Miyazaki, J., Smith, A.G., Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:4 (2000), 372–376.
55. 55 Home, P., Ray, S., Dutta, D., Bronshteyn, I., Larson, M., Paul, S., GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J Biol Chem 284:42 (2009), 28729–28737.
56. 56 Ralston, A., Cox, B.J., Nishioka, N., et al. Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 137:3 (2010), 395–403.
57. 57 Nishiyama, A., Xin, L., Sharov, A.A., et al. Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Cell Stem Cell 5:4 (2009), 420–433.
58. 58 Ma, G.T., Roth, M.E., Groskopf, J.C., et al. GATA-2 and GATA-3 regulate trophoblast-specific gene expression in vivo. Development 124:4 (1997), 907–914.
59. 59 Ray, S., Dutta, D., Rumi, M.A., Kent, L.N., Soares, M.J., Paul, S., Context-dependent function of regulatory elements and a switch in chromatin occupancy between GATA3 and GATA2 regulate Gata2 transcription during trophoblast differentiation. J Biol Chem 284:8 (2009), 4978–4988.
60. 60 Russ, A.P., Wattler, S., Colledge, W.H., et al. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404:6773 (2000), 95–99.
61. 61 Kidder, B.L., Palmer, S., Examination of transcriptional networks reveals an important role for TCFAP2C, SMARCA4, and EOMES in trophoblast stem cell maintenance. Genome Res 20:4 (2010), 458–472.
62. 62 Kuckenberg, P., Buhl, S., Woynecki, T., et al. The transcription factor TCFAP2C/AP-2gamma cooperates with CDX2 to maintain trophectoderm formation. Mol Cell Biol. 30:13 (2010), 3310–3320.
63. 63 Auman, H.J., Nottoli, T., Lakiza, O., Winger, Q., Donaldson, S., Williams, T., Transcription factor AP-2gamma is essential in the extra-embryonic lineages for early postimplantation development. Development 129:11 (2002), 2733–2747.
64. 64 Winger, Q., Huang, J., Auman, H.J., Lewandoski, M., Williams, T., Analysis of transcription factor AP-2 expression and function during mouse preimplantation development. Biol Reprod 75:3 (2006), 324–333.
65. 65 Choi, I., Carey, T.S., Wilson, C.A., Knott, J.G., Transcription factor AP-2gamma is a core regulator of tight junction biogenesis and cavity formation during mouse early embryogenesis. Development 139:24 (2012), 4623–4632.
66. 66 Cao, Z., Carey, T.S., Ganguly, A., Wilson, C.A., Paul, S., Knott, J.G., Transcription factor AP-2gamma induces early Cdx2 expression and represses HIPPO signaling to specify the trophectoderm lineage. Development 142:9 (2015), 1606–1615.
67. 67 Martello, G., Sugimoto, T., Diamanti, E., et al. Esrrb is a pivotal target of the Gsk3/Tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 11:4 (2012), 491–504.
68. 68 Hanna, L.A., Foreman, R.K., Tarasenko, I.A., Kessler, D.S., Labosky, P.A., Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev 16:20 (2002), 2650–2661.
69. 69 Savarese, F., Davila, A., Nechanitzky, R., et al. Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression. Genes Dev 23:22 (2009), 2625–2638.
70. 70 Avilion, A.A., Nicolis, S.K., Pevny, L.H., Perez, L., Vivian, N., Lovell-Badge, R., Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17:1 (2003), 126–140.
71. 71 Luo, J., Sladek, R., Bader, J.A., Matthyssen, A., Rossant, J., Giguere, V., Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature 388:6644 (1997), 778–782.
72. 72 Tremblay, G.B., Kunath, T., Bergeron, D., et al. Diethylstilbestrol regulates trophoblast stem cell differentiation as a ligand of orphan nuclear receptor ERR beta. Genes Dev 15:7 (2001), 833–838.
73. 73 Latos, P.A., Goncalves, A., Oxley, D., Mohammed, H., Turro, E., Hemberger, M., Fgf and Esrrb integrate epigenetic and transcriptional networks that regulate self-renewal of trophoblast stem cells. Nat Commun, 6, 2015, 7776.
74. 74 Adachi, K., Nikaido, I., Ohta, H., et al. Context-dependent wiring of Sox2 regulatory networks for self-renewal of embryonic and trophoblast stem cells. Mol Cell 52:3 (2013), 380–392.
75. 75 Keramari, M., Razavi, J., Ingman, K.A., et al. Sox2 is essential for formation of trophectoderm in the preimplantation embryo. PLoS One, 5(11), 2010, e13952.
76. 76 Tompers, D.M., Foreman, R.K., Wang, Q., Kumanova, M., Labosky, P.A., Foxd3 is required in the trophoblast progenitor cell lineage of the mouse embryo. Dev Biol 285:1 (2005), 126–137.
77. 77 Lasorella, A., Uo, T., Iavarone, A., Id proteins at the cross-road of development and cancer. Oncogene 20:58 (2001), 8326–8333.
78. 78 Asanoma, K., Rumi, M.A., Kent, L.N., et al. FGF4-dependent stem cells derived from rat blastocysts differentiate along the trophoblast lineage. Dev Biol 351:1 (2011), 110–119.
79. 79 Guo, G., Huss, M., Tong, G.Q., et al. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 18:4 (2010), 675–685.
80. 80 Wang, J., Rao, S., Chu, J., et al. A protein interaction network for pluripotency of embryonic stem cells. Nature 444:7117 (2006), 364–368.
81. 81 Rhee, C., Lee, B.K., Beck, S., et al. Arid3a is essential to execution of the first cell fate decision via direct embryonic and extraembryonic transcriptional regulation. Genes Dev 28:20 (2014), 2219–2232.
82. 82 Webb, C.F., Bryant, J., Popowski, M., et al. The ARID family transcription factor bright is required for both hematopoietic stem cell and B lineage development. Mol Cell Biol 31:5 (2011), 1041–1053.
83. 83 Yamamoto, H., Flannery, M.L., Kupriyanov, S., et al. Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev 12:9 (1998), 1315–1326.
84. 84 Georgiades, P., Rossant, J., Ets2 is necessary in trophoblast for normal embryonic anteroposterior axis development. Development 133:6 (2006), 1059–1068.
85. 85 Wen, F., Tynan, J.A., Cecena, G., et al. Ets2 is required for trophoblast stem cell self-renewal. Dev Biol 312:1 (2007), 284–299.
86. 86 Donnison, M., Beaton, A., Davey, H.W., Broadhurst, R., L'Huillier, P., Pfeffer, P.L., Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 132:10 (2005), 2299–2308.
87. 87 Latos, P.A., Helliwell, C., Mosaku, O., et al. NuRD-dependent DNA methylation prevents ES cells from accessing a trophectoderm fate. Biol Open 1:4 (2012), 341–352.
88. 88 Ng, R.K., Dean, W., Dawson, C., et al. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 10:11 (2008), 1280–1290.
89. 89 Donnison, M., Broadhurst, R., Pfeffer, P.L., Elf5 and Ets2 maintain the mouse extraembryonic ectoderm in a dosage dependent synergistic manner. Dev Biol 397:1 (2015), 77–88.
90. 90 Latos, P.A., Sienerth, A.R., Murray, A., et al. Elf5-centered transcription factor hub controls trophoblast stem cell self-renewal and differentiation through stoichiometry-sensitive shifts in target gene networks. Genes Dev 29:23 (2015), 2435–2448.
91. 91 Pearton, D.J., Smith, C.S., Redgate, E., van Leeuwen, J., Donnison, M., Pfeffer, P.L., Elf5 counteracts precocious trophoblast differentiation by maintaining Sox2 and 3 and inhibiting Hand1 expression. Dev Biol 392:2 (2014), 344–357.
92. 92 Cockburn, K., Rossant, J., Making the blastocyst: lessons from the mouse. J Clin Invest 120:4 (2010), 995–1003.
93. 93 Rossant, J., Mouse and human blastocyst-derived stem cells: vive les differences. Development 142:1 (2015), 9–12.
94. 94 Douglas, G.C., VandeVoort, C.A., Kumar, P., Chang, T.C., Golos, T.G., Trophoblast stem cells: models for investigating trophectoderm differentiation and placental development. Endocr Rev 30:3 (2009), 228–240.
95. 95 De Paepe, C., Krivega, M., Cauffman, G., Geens, M., Van de Velde, H., Totipotency and lineage segregation in the human embryo. Mol Hum Reprod 20:7 (2014), 599–618.
96. 96 Ginis, I., Luo, Y., Miura, T., et al. Differences between human and mouse embryonic stem cells. Dev Biol 269:2 (2004), 360–380.
97. 97 Chuykin, I., Lapidus, I., Popova, E., et al. Characterization of trophoblast and extraembryonic endoderm cell lineages derived from rat preimplantation embryos. PLoS One, 5(3), 2010, e9794.
98. 98 Grigor'eva, E.V., Shevchenko, A.I., Mazurok, N.A., et al. FGF4 independent derivation of trophoblast stem cells from the common vole. PLoS One, 4(9), 2009, e7161.
99. 99 Vandevoort, C.A., Thirkill, T.L., Douglas, G.C., Blastocyst-derived trophoblast stem cells from the rhesus monkey. Stem Cells Dev 16:5 (2007), 779–788.
100. 100 Hashizume, K., Shimada, A., Nakano, H., Takahashi, T., Bovine trophoblast cell culture systems: a technique to culture bovine trophoblast cells without feeder cells. Methods Mol Med 121 (2006), 179–188.
101. 101 Flechon, J.E., Laurie, S., Notarianni, E., Isolation and characterization of a feeder-dependent, porcine trophectoderm cell line obtained from a 9-day blastocyst. Placenta 16:7 (1995), 643–658.
102. 102 Kunath, T., Yamanaka, Y., Detmar, J., et al. Developmental differences in the expression of FGF receptors between human and mouse embryos. Placenta 35:12 (2014), 1079–1088.
103. 103 Niakan, K.K., Eggan, K., Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol 375:1 (2013), 54–64.
104. 104 Hansis, C., Grifo, J.A., Krey, L.C., Oct-4 expression in inner cell mass and trophectoderm of human blastocysts. Mol Hum Reprod 6:11 (2000), 999–1004.
105. 105 Adjaye, J., Huntriss, J., Herwig, R., et al. Primary differentiation in the human blastocyst: comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells 23:10 (2005), 1514–1525.
106. 106 Cauffman, G., Van de Velde, H., Liebaers, I., Van Steirteghem, A., Oct-4 mRNA and protein expression during human preimplantation development. Mol Hum Reprod 11:3 (2005), 173–181.
107. 107 Berg, D.K., Smith, C.S., Pearton, D.J., et al. Trophectoderm lineage determination in cattle. Dev Cell 20:2 (2011), 244–255.
108. 108 De Paepe, C., Cauffman, G., Verloes, A., et al. Human trophectoderm cells are not yet committed. Hum Reprod 28:3 (2013), 740–749.
109. 109 Blakeley, P., Fogarty, N.M., del Valle, I., et al. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development 142:18 (2015), 3151–3165.
110. 110 Petropoulos, S., Edsgard, D., Reinius, B., et al. Single-cell RNA-Seq reveals lineage and X chromosome dynamics in human preimplantation embryos. Cell 165:4 (2016), 1012–1026.
111. 111 Piras, V., Tomita, M., Selvarajoo, K., Transcriptome-wide variability in single embryonic development cells. Sci Rep, 4, 2014, 7137.
112. 112 Yan, L., Yang, M., Guo, H., et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 20:9 (2013), 1131–1139.
113. 113 Deng, Q., Ramskold, D., Reinius, B., Sandberg, R., Single-cell RNA-seq reveals dynamic, random monoallelic gene expression in mammalian cells. Science 343:6167 (2014), 193–196.
114. 114 Xu, R.H., Chen, X., Li, D.S., et al. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 20:12 (2002), 1261–1264.
115. 115 Amita, M., Adachi, K., Alexenko, A.P., et al. Complete and unidirectional conversion of human embryonic stem cells to trophoblast by BMP4. Proc Natl Acad Sci USA 110:13 (2013), E1212–E1221.
116. 116 Zdravkovic, T., Nazor, K.L., Larocque, N., et al. Human stem cells from single blastomeres reveal pathways of embryonic or trophoblast fate specification. Development 142:23 (2015), 4010–4025.
117. 117 Rossant, J., Stem cells in the mammalian blastocyst. Harvey Lect 97 (2001), 17–40.
118. 118 Li, Y., Moretto-Zita, M., Soncin, F., et al. BMP4-directed trophoblast differentiation of human embryonic stem cells is mediated through a DeltaNp63 + cytotrophoblast stem cell state. Development 140:19 (2013), 3965–3976.
119. 119 Marchand, M., Horcajadas, J.A., Esteban, F.J., McElroy, S.L., Fisher, S.J., Giudice, L.C., Transcriptomic signature of trophoblast differentiation in a human embryonic stem cell model. Biol Reprod 84:6 (2011), 1258–1271.
120. 120 Roberts, R.M., Loh, K.M., Amita, M., et al. Differentiation of trophoblast cells from human embryonic stem cells: to be or not to be?. Reproduction 147:5 (2014), D1–D12.
121. 121 Lee, C.Q., Gardner, L., Turco, M., et al. What is trophoblast? A combination of criteria define human first-trimester trophoblast. Stem Cell Reports 6:2 (2016), 257–272.
122. 122 Hemberger, M., Udayashankar, R., Tesar, P., Moore, H., Burton, G.J., ELF5-enforced transcriptional networks define an epigenetically regulated trophoblast stem cell compartment in the human placenta. Hum Mol Genet 19:12 (2010), 2456–2467.
123. 123 Chen, Y., Wang, K., Gong, Y.G., Khoo, S.K., Leach, R., Roles of CDX2 and EOMES in human induced trophoblast progenitor cells. Biochem Biophys Res Commun 431:2 (2013), 197–202.
124. 124 Genbacev, O., Larocque, N., Ona, K., et al. Integrin alpha4-positive human trophoblast progenitors: functional characterization and transcriptional regulation. Hum Reprod 31:6 (2016), 1300–1314.
125. 125 Genbacev, O., Donne, M., Kapidzic, M., et al. Establishment of human trophoblast progenitor cell lines from the chorion. Stem Cells 29:9 (2011), 1427–1436.
126. 126 Banet, N., Gown, A.M., Shih Ie, M., et al. GATA-3 expression in trophoblastic tissues: an immunohistochemical study of 445 cases, including diagnostic utility. Am J Surg Pathol 39:1 (2015), 101–108.
127. 127 Biadasiewicz, K., Sonderegger, S., Haslinger, P., et al. Transcription factor AP-2alpha promotes EGF-dependent invasion of human trophoblast. Endocrinology 152:4 (2011), 1458–1469.
128. 128 Orendi, K., Gauster, M., Moser, G., Meiri, H., Huppertz, B., The choriocarcinoma cell line BeWo: syncytial fusion and expression of syncytium-specific proteins. Reproduction 140:5 (2010), 759–766.
129. 129 Semenza, G.L., Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda) 24 (2009), 97–106.
130. 130 Adelman, D.M., Gertsenstein, M., Nagy, A., Simon, M.C., Maltepe, E., Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 14:24 (2000), 3191–3203.
131. 131 Cowden Dahl, K.D., Fryer, B.H., Mack, F.A., et al. Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation. Mol Cell Biol 25:23 (2005), 10479–10491.
132. 132 Chakraborty, D., Rumi, M.A., Konno, T., Soares, M.J., Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions. Proc Natl Acad Sci USA 108:39 (2011), 16295–16300.
133. 133 Maltepe, E., Krampitz, G.W., Okazaki, K.M., et al. Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development 132:15 (2005), 3393–3403.
134. 134 Rajakumar, A., Conrad, K.P., Expression, ontogeny, and regulation of hypoxia-inducible transcription factors in the human placenta. Biol Reprod 63:2 (2000), 559–569.
135. 135 Genbacev, O., Zhou, Y., Ludlow, J.W., Fisher, S.J., Regulation of human placental development by oxygen tension. Science 277:5332 (1997), 1669–1672.
136. 136 Alsat, E., Wyplosz, P., Malassine, A., et al. Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro. J Cell Physiol 168:2 (1996), 346–353.
137. 137 Jiang, B., Kamat, A., Mendelson, C.R., Hypoxia prevents induction of aromatase expression in human trophoblast cells in culture: potential inhibitory role of the hypoxia-inducible transcription factor Mash-2 (mammalian Achaete-Scute homologous protein-2). Mol Endocrinol 14:10 (2000), 1661–1673.
138. 138 Caniggia, I., Mostachfi, H., Winter, J., et al. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest 105:5 (2000), 577–587.
139. 139 Kilburn, B.A., Wang, J., Duniec-Dmuchowski, Z.M., Leach, R.E., Romero, R., Armant, D.R., Extracellular matrix composition and hypoxia regulate the expression of HLA-G and integrins in a human trophoblast cell line. Biol Reprod 62:3 (2000), 739–747.
140. 140 Zhou, Y., Genbacev, O., Damsky, C.H., Fisher, S.J., Oxygen regulates human cytotrophoblast differentiation and invasion: implications for endovascular invasion in normal pregnancy and in pre-eclampsia. J Reprod Immunol 39:1–2 (1998), 197–213.
141. 141 James, J.L., Stone, P.R., Chamley, L.W., The effects of oxygen concentration and gestational age on extravillous trophoblast outgrowth in a human first trimester villous explant model. Hum Reprod 21:10 (2006), 2699–2705.
142. 142 Graham, C.H., Postovit, L.M., Park, H., Canning, M.T., Fitzpatrick, T.E., Adriana and Luisa Castellucci award lecture 1999: role of oxygen in the regulation of trophoblast gene expression and invasion. Placenta 21:5–6 (2000), 443–450.
143. 143 Robins, J.C., Heizer, A., Hardiman, A., Hubert, M., Handwerger, S., Oxygen tension directs the differentiation pathway of human cytotrophoblast cells. Placenta 28:11–12 (2007), 1141–1146.
144. 144 Hayashi, M., Sakata, M., Takeda, T., et al. Up-regulation of c-met protooncogene product expression through hypoxia-inducible factor-1alpha is involved in trophoblast invasion under low-oxygen tension. Endocrinology 146:11 (2005), 4682–4689.
145. 145 Rosario, G.X., Konno, T., Soares, M.J., Maternal hypoxia activates endovascular trophoblast cell invasion. Dev Biol 314:2 (2008), 362–375.
146. 146 Guillemot, F., Nagy, A., Auerbach, A., Rossant, J., Joyner, A.L., Essential role of Mash-2 in extraembryonic development. Nature 371:6495 (1994), 333–336.
147. 147 Schuijers, J., Junker, J.P., Mokry, M., et al. Ascl2 acts as an R-spondin/Wnt-responsive switch to control stemness in intestinal crypts. Cell Stem Cell 16:2 (2015), 158–170.
148. 148 Tanaka, M., Gertsenstein, M., Rossant, J., Nagy, A., Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev Biol 190:1 (1997), 55–65.
149. 149 Oh-McGinnis, R., Bogutz, A.B., Lefebvre, L., Partial loss of Ascl2 function affects all three layers of the mature placenta and causes intrauterine growth restriction. Dev Biol 351:2 (2011), 277–286.
150. 150 Alders, M., Hodges, M., Hadjantonakis, A.K., et al. The human Achaete-Scute homologue 2 (ASCL2, HASH2) maps to chromosome 11p15.5, close to IGF2 and is expressed in extravillus trophoblasts. Hum Mol Genet 6:6 (1997), 859–867.
151. 151 Janatpour, M.J., Utset, M.F., Cross, J.C., et al. A repertoire of differentially expressed transcription factors that offers insight into mechanisms of human cytotrophoblast differentiation. Dev Genet 25:2 (1999), 146–157.
152. 2 enhancement of human trophoblast differentiation and hCYP19 (aromatase) gene expression are mediated by proteasomal degradation of USF1 and USF2. Mol Cell Biol 25:20 (2005), 8824–8833.
153. 153 Jiang, B., Mendelson, C.R., USF1 and USF2 mediate inhibition of human trophoblast differentiation and CYP19 gene expression by Mash-2 and hypoxia. Mol Cell Biol 23:17 (2003), 6117–6128.
154. 154 King, K.E., Weinberg, W.C., p63: defining roles in morphogenesis, homeostasis, and neoplasia of the epidermis. Mol Carcinog 46:8 (2007), 716–724.
155. 155 Romano, R.A., Smalley, K., Magraw, C., et al. DeltaNp63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation. Development 139:4 (2012), 772–782.
156. 156 Senoo, M., Pinto, F., Crum, C.P., McKeon, F., p63 Is essential for the proliferative potential of stem cells in stratified epithelia. Cell 129:3 (2007), 523–536.
157. 157 Lee, Y., Kim, K.R., McKeon, F., et al. A unifying concept of trophoblastic differentiation and malignancy defined by biomarker expression. Hum Pathol 38:7 (2007), 1003–1013.
158. 158 Shih, I.M., Kurman, R.J., p63 expression is useful in the distinction of epithelioid trophoblastic and placental site trophoblastic tumors by profiling trophoblastic subpopulations. Am J Surg Pathol 28:9 (2004), 1177–1183.
159. 159 Li, Y., Moretto-Zita, M., Leon-Garcia, S., Parast, M.M., p63 inhibits extravillous trophoblast migration and maintains cells in a cytotrophoblast stem cell-like state. Am J Pathol 184:12 (2014), 3332–3343.
160. 160 Xue, W.C., Feng, H.C., Chan, K.Y., et al. Id helix-loop-helix proteins are differentially expressed in gestational trophoblastic disease. Histopathology 47:3 (2005), 303–309.
161. 161 Janatpour, M.J., McMaster, M.T., Genbacev, O., et al. Id-2 regulates critical aspects of human cytotrophoblast differentiation, invasion and migration. Development 127:3 (2000), 549–558.
162. 162 Eilers, M., Eisenman, R.N., Myc's broad reach. Genes Dev 22:20 (2008), 2755–2766.
163. 163 Roncalli, M., Bulfamante, G., Viale, G., et al. C-myc and tumour suppressor gene product expression in developing and term human trophoblast. Placenta 15:4 (1994), 399–409.
164. 164 Diebold, J., Arnholdt, H., Lai, M.D., Lohrs, U., C-myc expression in early human placenta—a critical evaluation of its localization. Virchows Arch B Cell Pathol Incl Mol Pathol 61:1 (1991), 65–73.
165. 165 Kumar, P., Luo, Y., Tudela, C., Alexander, J.M., Mendelson, C.R., The c-Myc-regulated microRNA-17~92 (miR-17~92) and miR-106a~363 clusters target hCYP19A1 and hGCM1 to inhibit human trophoblast differentiation. Mol Cell Biol 33:9 (2013), 1782–1796.
166. 166 Johnson, R.S., Spiegelman, B.M., Papaioannou, V., Pleiotropic effects of a null mutation in the c-fos proto-oncogene. Cell 71:4 (1992), 577–586.
167. 167 Bamberger, A.M., Bamberger, C.M., Aupers, S., Milde-Langosch, K., Loning, T., Makrigiannakis, A., Expression pattern of the activating protein-1 family of transcription factors in the human placenta. Mol Hum Reprod 10:4 (2004), 223–228.
168. 168 Anson-Cartwright, L., Dawson, K., Holmyard, D., Fisher, S.J., Lazzarini, R.A., Cross, J.C., The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 25:3 (2000), 311–314.
169. 169 Stecca, B., Nait-Oumesmar, B., Kelley, K.A., Voss, A.K., Thomas, T., Lazzarini, R.A., Gcm1 expression defines three stages of chorio-allantoic interaction during placental development. Mech Dev 115:1–2 (2002), 27–34.
170. 170 Hughes, M., Dobric, N., Scott, I.C., et al. The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells. Dev Biol 271:1 (2004), 26–37.
171. 171 Schubert, S.W., Lamoureux, N., Kilian, K., Klein-Hitpass, L., Hashemolhosseini, S., Identification of integrin-alpha4, Rb1, and syncytin a as murine placental target genes of the transcription factor GCMa/Gcm1. J Biol Chem 283:9 (2008), 5460–5465.
172. 172 Bainbridge, S.A., Minhas, A., Whiteley, K.J., et al. Effects of reduced Gcm1 expression on trophoblast morphology, fetoplacental vascularity, and pregnancy outcomes in mice. Hypertension 59:3 (2012), 732–739.
173. 173 Baczyk, D., Satkunaratnam, A., Nait-Oumesmar, B., Huppertz, B., Cross, J.C., Kingdom, J.C., Complex patterns of GCM1 mRNA and protein in villous and extravillous trophoblast cells of the human placenta. Placenta 25:6 (2004), 553–559.
174. 174 Chang, C.W., Cheong, M.L., Chang, G.D., Tsai, M.S., Chen, H., Involvement of Epac1/Rap1/CaMKI/HDAC5 signaling cascade in the regulation of placental cell fusion. Mol Hum Reprod 19:11 (2013), 745–755.
175. 175 Lin, F.Y., Chang, C.W., Cheong, M.L., et al. Dual-specificity phosphatase 23 mediates GCM1 dephosphorylation and activation. Nucleic Acids Res 39:3 (2011), 848–861.
176. 176 Chiang, M.H., Liang, F.Y., Chen, C.P., et al. Mechanism of hypoxia-induced GCM1 degradation: implications for the pathogenesis of preeclampsia. J Biol Chem 284:26 (2009), 17411–17419.
177. 177 Kashif, M., Hellwig, A., Kolleker, A., et al. p45NF-E2 represses Gcm1 in trophoblast cells to regulate syncytium formation, placental vascularization and embryonic growth. Development 138:11 (2011), 2235–2247.
178. 178 Chiu, Y.H., Chen, H., GATA3 inhibits GCM1 activity and trophoblast cell invasion. Sci Rep, 6, 2016, 21630.
179. 179 Baczyk, D., Drewlo, S., Proctor, L., Dunk, C., Lye, S., Kingdom, J., Glial cell missing-1 transcription factor is required for the differentiation of the human trophoblast. Cell Death Differ 16:5 (2009), 719–727.
180. 180 Yu, C., Shen, K., Lin, M., et al. GCMa regulates the syncytin-mediated trophoblastic fusion. J Biol Chem 277:51 (2002), 50062–50068.
181. 181 Yamada, K., Ogawa, H., Honda, S., Harada, N., Okazaki, T., A GCM motif protein is involved in placenta-specific expression of human aromatase gene. J Biol Chem 274:45 (1999), 32279–32286.
182. 182 Chang, M., Mukherjea, D., Gobble, R.M., Groesch, K.A., Torry, R.J., Torry, D.S., Glial cell missing 1 regulates placental growth factor (PGF) gene transcription in human trophoblast. Biol Reprod 78:5 (2008), 841–851.
183. 183 Wang, L.J., Cheong, M.L., Lee, Y.S., Lee, M.T., Chen, H., High-temperature requirement protein A4 (HtrA4) suppresses the fusogenic activity of syncytin-1 and promotes trophoblast invasion. Mol Cell Biol 32:18 (2012), 3707–3717.
184. 184 Delidaki, M., Gu, M., Hein, A., Vatish, M., Grammatopoulos, D.K., Interplay of cAMP and MAPK pathways in hCG secretion and fusogenic gene expression in a trophoblast cell line. Mol Cell Endocrinol 332:1–2 (2011), 213–220.
185. 185 Ghosh, D., Sachdev, S., Hannink, M., Roberts, R.M., Coordinate regulation of basal and cyclic 5'-adenosine monophosphate (cAMP)-activated expression of human chorionic gonadotropin-alpha by Ets-2 and cAMP-responsive element binding protein. Mol Endocrinol 19:4 (2005), 1049–1066.
186. 186 Zhou, Z., Wang, R., Yang, X., et al. The cAMP-responsive element binding protein (CREB) transcription factor regulates furin expression during human trophoblast syncytialization. Placenta 35:11 (2014), 907–918.
187. 187 Toufaily, C., Lokossou, A.G., Vargas, A., Rassart, E., Barbeau, B., A CRE/AP-1-like motif is essential for induced syncytin-2 expression and fusion in human trophoblast-like model. PLoS One, 10(3), 2015, e0121468.
188. 188 Schubert, S.W., Abendroth, A., Kilian, K., et al. bZIP-Type transcription factors CREB and OASIS bind and stimulate the promoter of the mammalian transcription factor GCMa/Gcm1 in trophoblast cells. Nucleic Acids Res 36:11 (2008), 3834–3846.
189. 189 Chang, C.W., Chuang, H.C., Yu, C., Yao, T.P., Chen, H., Stimulation of GCMa transcriptional activity by cyclic AMP/protein kinase A signaling is attributed to CBP-mediated acetylation of GCMa. Mol Cell Biol 25:19 (2005), 8401–8414.
190. 190 Nair, M., Teng, A., Bilanchone, V., Agrawal, A., Li, B., Dai, X., Ovol1 regulates the growth arrest of embryonic epidermal progenitor cells and represses c-myc transcription. J Cell Biol 173:2 (2006), 253–264.
191. 191 Payre, F., Vincent, A., Carreno, S., ovo/svb integrates Wingless and DER pathways to control epidermis differentiation. Nature 400:6741 (1999), 271–275.
192. 192 Renaud, S.J., Chakraborty, D., Mason, C.W., Rumi, M.A., Vivian, J.L., Soares, M.J., OVO-like 1 regulates progenitor cell fate in human trophoblast development. Proc Natl Acad Sci USA 112 (2015), E6175–E6184.
193. 193 Berger, J., Moller, D.E., The mechanisms of action of PPARs. Annu Rev Med 53 (2002), 409–435.
194. 194 Wang, Q., Fujii, H., Knipp, G.T., Expression of PPAR and RXR isoforms in the developing rat and human term placentas. Placenta 23:8–9 (2002), 661–671.
195. 195 Barak, Y., Nelson, M.C., Ong, E.S., et al. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell 4:4 (1999), 585–595.
196. 196 Schaiff, W.T., Knapp, F.F. Jr., Barak, Y., Biron-Shental, T., Nelson, D.M., Sadovsky, Y., Ligand-activated peroxisome proliferator activated receptor gamma alters placental morphology and placental fatty acid uptake in mice. Endocrinology 148:8 (2007), 3625–3634.
197. 197 Shalom-Barak, T., Nicholas, J.M., Wang, Y., et al. Peroxisome proliferator-activated receptor gamma controls Muc1 transcription in trophoblasts. Mol Cell Biol 24:24 (2004), 10661–10669.
198. 198 Parast, M.M., Yu, H., Ciric, A., Salata, M.W., Davis, V., Milstone, D.S., PPARgamma regulates trophoblast proliferation and promotes labyrinthine trilineage differentiation. PLoS One, 4(11), 2009, e8055.
199. 199 Capparuccia, L., Marzioni, D., Giordano, A., et al. PPARgamma expression in normal human placenta, hydatidiform mole and choriocarcinoma. Mol Hum Reprod 8:6 (2002), 574–579.
200. 200 Schaiff, W.T., Carlson, M.G., Smith, S.D., Levy, R., Nelson, D.M., Sadovsky, Y., Peroxisome proliferator-activated receptor-gamma modulates differentiation of human trophoblast in a ligand-specific manner. J Clin Endocrinol Metab 85:10 (2000), 3874–3881.
201. 201 Levytska, K., Drewlo, S., Baczyk, D., Kingdom, J., PPAR-gamma regulates trophoblast differentiation in the BeWo cell model. PPAR Res, 2014, 2014, 637251.
202. 202 Tarrade, A., Schoonjans, K., Guibourdenche, J., et al. PPAR gamma/RXR alpha heterodimers are involved in human CG beta synthesis and human trophoblast differentiation. Endocrinology 142:10 (2001), 4504–4514.
203. 203 Schaiff, W.T., Bildirici, I., Cheong, M., Chern, P.L., Nelson, D.M., Sadovsky, Y., Peroxisome proliferator-activated receptor-gamma and retinoid X receptor signaling regulate fatty acid uptake by primary human placental trophoblasts. J Clin Endocrinol Metab 90:7 (2005), 4267–4275.
204. 204 Fournier, T., Pavan, L., Tarrade, A., et al. The role of PPAR-gamma/RXR-alpha heterodimers in the regulation of human trophoblast invasion. Ann NY Acad Sci 973 (2002), 26–30.
205. 205 Tarrade, A., Schoonjans, K., Pavan, L., et al. PPARgamma/RXRalpha heterodimers control human trophoblast invasion. J Clin Endocrinol Metab 86:10 (2001), 5017–5024.
206. 206 Fournier, T., Handschuh, K., Tsatsaris, V., Evain-Brion, D., Involvement of PPARgamma in human trophoblast invasion. Placenta 28:suppl A (2007), S76–S81.
207. 207 Stephanou, A., Handwerger, S., Retinoic acid and thyroid hormone regulate placental lactogen expression in human trophoblast cells. Endocrinology 136:3 (1995), 933–938.
208. 208 Lu, X.J., Deb, S., Soares, M.J., Spontaneous differentiation of trophoblast cells along the spongiotrophoblast cell pathway: expression of members of the placental prolactin gene family and modulation by retinoic acid. Dev Biol 163:1 (1994), 86–97.
209. 209 Tarrade, A., Rochette-Egly, C., Guibourdenche, J., Evain-Brion, D., The expression of nuclear retinoid receptors in human implantation. Placenta 21:7 (2000), 703–710.
210. 210 Sapin, V., Ward, S.J., Bronner, S., Chambon, P., Dolle, P., Differential expression of transcripts encoding retinoid binding proteins and retinoic acid receptors during placentation of the mouse. Dev Dyn 208:2 (1997), 199–210.
211. 211 Sapin, V., Dolle, P., Hindelang, C., Kastner, P., Chambon, P., Defects of the chorioallantoic placenta in mouse RXRalpha null fetuses. Dev Biol 191:1 (1997), 29–41.
212. 212 Wendling, O., Chambon, P., Mark, M., Retinoid X receptors are essential for early mouse development and placentogenesis. Proc Natl Acad Sci USA 96:2 (1999), 547–551.
213. 213 Richardson, B.D., Cheng, Y.H., Langland, R.A., Handwerger, S., Differential expression of AP-2gamma and AP-2alpha during human trophoblast differentiation. Life Sci 69:18 (2001), 2157–2165.
214. 214 Hubert, M.A., Sherritt, S.L., Bachurski, C.J., Handwerger, S., Involvement of transcription factor NR2F2 in human trophoblast differentiation. PLoS One, 5(2), 2010, e9417.
215. 215 Kessler, C.A., Stanek, J.W., Stringer, K.F., Handwerger, S., ETS1 induces human trophoblast differentiation. Endocrinology 156:5 (2015), 1851–1859.
216. 216 Cheng, Y.H., Aronow, B.J., Hossain, S., Trapnell, B., Kong, S., Handwerger, S., Critical role for transcription factor AP-2alpha in human trophoblast differentiation. Physiol Genomics 18:1 (2004), 99–107.
217. 217 Zhang, Z., Zhang, L., Jia, L., et al. AP-2alpha suppresses invasion in BeWo cells by repression of matrix metalloproteinase-2 and -9 and up-regulation of E-cadherin. Mol Cell Biochem 381:1–2 (2013), 31–39.
218. 218 Kotani, T., Iwase, A., Ino, K., et al. Activator protein-2 impairs the invasion of a human extravillous trophoblast cell line. Endocrinology 150:9 (2009), 4376–4385.
219. 219 Morasso, M.I., Grinberg, A., Robinson, G., Sargent, T.D., Mahon, K.A., Placental failure in mice lacking the homeobox gene Dlx3. Proc Natl Acad Sci USA 96:1 (1999), 162–167.
220. 220 Chui, A., Pathirage, N.A., Johnson, B., et al. Homeobox gene distal-less 3 is expressed in proliferating and differentiating cells of the human placenta. Placenta 31:8 (2010), 691–697.
221. 221 Peng, L., Huang, Y., Jin, F., Jiang, S.W., Payne, A.H., Transcription enhancer factor-5 and a GATA-like protein determine placental-specific expression of the Type I human 3beta-hydroxysteroid dehydrogenase gene, HSD3B1. Mol Endocrinol 18:8 (2004), 2049–2060.
222. 222 Berghorn, K.A., Clark, P.A., Encarnacion, B., et al. Developmental expression of the homeobox protein Distal-less 3 and its relationship to progesterone production in mouse placenta. J Endocrinol 186:2 (2005), 315–323.
223. 223 Roberson, M.S., Meermann, S., Morasso, M.I., Mulvaney-Musa, J.M., Zhang, T., A role for the homeobox protein Distal-less 3 in the activation of the glycoprotein hormone alpha subunit gene in choriocarcinoma cells. J Biol Chem 276:13 (2001), 10016–10024.
224. 224 Jacquemin, P., Sapin, V., Alsat, E., Evain-Brion, D., Dolle, P., Davidson, I., Differential expression of the TEF family of transcription factors in the murine placenta and during differentiation of primary human trophoblasts in vitro. Dev Dyn 212:3 (1998), 423–436.
225. 225 Jacquemin, P., Martial, J.A., Davidson, I., Human TEF-5 is preferentially expressed in placenta and binds to multiple functional elements of the human chorionic somatomammotropin-B gene enhancer. J Biol Chem 272:20 (1997), 12928–12937.
226. 226 Barton, K., Muthusamy, N., Fischer, C., et al. The Ets-1 transcription factor is required for the development of natural killer cells in mice. Immunity 9:4 (1998), 555–563.
227. 227 Takai, N., Ueda, T., Narahara, H., Miyakawa, I., Expression of c-Ets1 protein in normal human placenta. Gynecol Obstet Invest 61:1 (2006), 15–20.
228. 228 Yamamoto, E., Ito, T., Abe, A., et al. Ikaros is expressed in human extravillous trophoblasts and involved in their migration and invasion. Mol Hum Reprod 11:11 (2005), 825–831.
229. 229 Ito, T., Nomura, S., Okada, M., et al. Ap-2 and Ikaros regulate transcription of human placental leucine aminopeptidase/oxytocinase gene. Biochem Biophys Res Commun 290:3 (2002), 1048–1053.
230. 230 Blanchon, L., Bocco, J.L., Gallot, D., et al. Co-localization of KLF6 and KLF4 with pregnancy-specific glycoproteins during human placenta development. Mech Dev 105:1–2 (2001), 185–189.
231. 231 Racca, A.C., Camolotto, S.A., Ridano, M.E., Bocco, J.L., Genti-Raimondi, S., Panzetta-Dutari, G.M., Kruppel-like factor 6 expression changes during trophoblast syncytialization and transactivates sshCG and PSG placental genes. PLoS One, 6(7), 2011, e22438.
232. 232 Racca, A.C., Ridano, M.E., Camolotto, S., Genti-Raimondi, S., Panzetta-Dutari, G.M., A novel regulator of human villous trophoblast fusion: the Kruppel-like factor 6. Mol Hum Reprod 21:4 (2015), 347–358.
233. 233 MacDonald, B.T., Tamai, K., He, X., Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:1 (2009), 9–26.
234. 234 Krivega, M., Essahib, W., Van de Velde, H., WNT3 and membrane-associated beta-catenin regulate trophectoderm lineage differentiation in human blastocysts. Mol Hum Reprod 21:9 (2015), 711–722.
235. 235 Aoki, M., Mieda, M., Ikeda, T., Hamada, Y., Nakamura, H., Okamoto, H., R-spondin3 is required for mouse placental development. Dev Biol 301:1 (2007), 218–226.
236. 236 Ishikawa, T., Tamai, Y., Zorn, A.M., et al. Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development 128:1 (2001), 25–33.
237. 237 Monkley, S.J., Delaney, S.J., Pennisi, D.J., Christiansen, J.H., Wainwright, B.J., Targeted disruption of the Wnt2 gene results in placentation defects. Development 122:11 (1996), 3343–3353.
238. 238 Galceran, J., Farinas, I., Depew, M.J., Clevers, H., Grosschedl, R., Wnt3a–/– like phenotype and limb deficiency in Lef1(–/–)Tcf1(–/–) mice. Genes Dev 13:6 (1999), 709–717.
239. 239 Matsuura, K., Jigami, T., Taniue, K., et al. Identification of a link between Wnt/beta-catenin signalling and the cell fusion pathway. Nat Commun, 2, 2011, 548.
240. 240 Sonderegger, S., Husslein, H., Leisser, C., Knofler, M., Complex expression pattern of Wnt ligands and frizzled receptors in human placenta and its trophoblast subtypes. Placenta 28:suppl A (2007), S97–S102.
241. 241 Getsios, S., Chen, G.T., MacCalman, C.D., Regulation of beta-catenin mRNA and protein levels in human villous cytotrophoblasts undergoing aggregation and fusion in vitro: correlation with E-cadherin expression. J Reprod Fertil 119:1 (2000), 59–68.
242. 242 Pollheimer, J., Loregger, T., Sonderegger, S., et al. Activation of the canonical wingless/T-cell factor signaling pathway promotes invasive differentiation of human trophoblast. Am J Pathol 168:4 (2006), 1134–1147.
243. 243 Knofler, M., Pollheimer, J., Human placental trophoblast invasion and differentiation: a particular focus on Wnt signaling. Front Genet, 4, 2013, 190.
244. 244 Schreiber, M., Wang, Z.Q., Jochum, W., Fetka, I., Elliott, C., Wagner, E.F., Placental vascularisation requires the AP-1 component fra1. Development 127:22 (2000), 4937–4948.
245. 245 Kubota, K., Kent, L.N., Rumi, M.A., Roby, K.F., Soares, M.J., Dynamic regulation of AP-1 transcriptional complexes directs trophoblast differentiation. Mol Cell Biol 35:18 (2015), 3163–3177.
246. 246 Kent, L.N., Rumi, M.A., Kubota, K., Lee, D.S., Soares, M.J., FOSL1 is integral to establishing the maternal-fetal interface. Mol Cell Biol 31:23 (2011), 4801–4813.
247. 247 Takeda, K., Noguchi, K., Shi, W., et al. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci USA 94:8 (1997), 3801–3804.
248. 248 San Martin, S., Fitzgerald, J.S., Weber, M., et al. Stat3 and Socs3 expression patterns during murine placenta development. Eur J Histochem, 57(2), 2013, e19.
249. 249 Roberts, A.W., Robb, L., Rakar, S., et al. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc Natl Acad Sci USA 98:16 (2001), 9324–9329.
250. 250 Takahashi, Y., Carpino, N., Cross, J.C., Torres, M., Parganas, E., Ihle, J.N., SOCS3: an essential regulator of LIF receptor signaling in trophoblast giant cell differentiation. EMBO J 22:3 (2003), 372–384.
251. 251 Takahashi, Y., Dominici, M., Swift, J., Nagy, C., Ihle, J.N., Trophoblast stem cells rescue placental defect in SOCS3-deficient mice. J Biol Chem 281:17 (2006), 11444–11445.
252. 252 Corvinus, F.M., Fitzgerald, J.S., Friedrich, K., Markert, U.R., Evidence for a correlation between trophoblast invasiveness and STAT3 activity. Am J Reprod Immunol 50:4 (2003), 316–321.
253. 253 Busch, S., Renaud, S.J., Schleussner, E., Graham, C.H., Markert, U.R., mTOR mediates human trophoblast invasion through regulation of matrix-remodeling enzymes and is associated with serine phosphorylation of STAT3. Exp Cell Res 315:10 (2009), 1724–1733.
254. 254 Poehlmann, T.G., Fitzgerald, J.S., Meissner, A., et al. Trophoblast invasion: tuning through LIF, signalling via Stat3. Placenta 26:suppl A (2005), S37–S41.