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Abstract

Establishing the different lineages of the early mammalian embryo takes place over several days and several rounds of cell divisions from the fertilized egg. The resulting blastocyst contains the pluripotent cells of the epiblast, from which embryonic stem cells can be derived, as well as the extraembryonic lineages required for a mammalian embryo to survive in the uterine environment. The dynamics of the cellular and genetic interactions controlling the initiation and maintenance of these lineages in the mouse embryo are increasingly well understood through application of the tools of single-cell genomics, gene editing, and in vivo imaging. Exploring the similarities and differences between mouse and human development will be essential for translation of these findings into new insights into human biology, derivation of stem cells, and improvements in fertility treatments.

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2018-11-23
2024-03-28
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Literature Cited

  1. 1.  Abe K, Yamamoto R, Franke V, Cao M, Suzuki Y et al. 2015. The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3′ processing. EMBO J 34:1523–37
    [Google Scholar]
  2. 2.  Artus J, Panthier J-J, Hadjantonakis A-K 2010. A role for PDGF signaling in expansion of the extra-embryonic endoderm lineage of the mouse blastocyst. Development 137:3361–72
    [Google Scholar]
  3. 3.  Artus J, Piliszek A, Hadjantonakis A-K 2011. The primitive endoderm lineage of the mouse blastocyst: sequential transcription factor activation and regulation of differentiation by Sox17. Dev. Biol. 350:393–404
    [Google Scholar]
  4. 4.  Auman HJ, Nottoli T, Lakiza O, Winger Q, Donaldson S, Williams T 2002. Transcription factor AP-2γ is essential in the extra-embryonic lineages for early postimplantation development. Development 129:2733–47
    [Google Scholar]
  5. 5.  Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17:126–40
    [Google Scholar]
  6. 6.  Azami T, Waku T, Matsumoto K, Jeon H, Muratani M et al. 2017. Klf5 maintains the balance of primitive endoderm versus epiblast specification during mouse embryonic development by suppression of Fgf4. Development 144:3706–18
    [Google Scholar]
  7. 7.  Beck F, Erler T, Russell A, James R 1995. Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev. Dyn. 204:219–27
    [Google Scholar]
  8. 8.  Bedzhov I, Leung CY, Bialecka M, Zernicka-Goetz M 2014. In vitro culture of mouse blastocysts beyond the implantation stages. Nat. Protoc. 9:2732–39
    [Google Scholar]
  9. 9.  Benchetrit H, Herman S, van Wietmarschen N, Wu T, Makedonski K et al. 2015. Extensive nuclear reprogramming underlies lineage conversion into functional trophoblast stem-like cells. Cell Stem Cell 17:543–56
    [Google Scholar]
  10. 10.  Bessonnard S, De Mot L, Gonze D, Barriol M, Dennis C et al. 2014. Gata6, Nanog and Erk signaling control cell fate in the inner cell mass through a tristable regulatory network. Development 141:3637–48
    [Google Scholar]
  11. 11.  Biase FH, Cao X, Zhong S 2014. Cell fate inclination within 2-cell and 4-cell mouse embryos revealed by single-cell RNA sequencing. Genome Res 24:1787–96
    [Google Scholar]
  12. 12.  Biechele S, Cockburn K, Lanner F, Cox BJ, Rossant J 2013. Porcn-dependent Wnt signaling is not required prior to mouse gastrulation. Development 140:2961–71
    [Google Scholar]
  13. 13.  Blakeley P, Fogarty NME, del Valle I, Wamaitha SE, Hu TX et al. 2015. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development 142:3151–65
    [Google Scholar]
  14. 14.  Boroviak T, Loos R, Lombard P, Okahara J, Behr R et al. 2015. Lineage-specific profiling delineates the emergence and progression of naive pluripotency in mammalian embryogenesis. Dev. Cell 35:366–82
    [Google Scholar]
  15. 15.  Bourillot P-Y, Savatier P 2010. Krüppel-like transcription factors and control of pluripotency. BMC Biol 8:125
    [Google Scholar]
  16. 16.  Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947–56
    [Google Scholar]
  17. 17.  Burton A, Muller J, Tu S, Padilla-Longoria P, Guccione E, Torres-Padilla M-E 2013. Single-cell profiling of epigenetic modifiers identifies PRDM14 as an inducer of cell fate in the mammalian embryo. Cell Rep. 5:687–701
    [Google Scholar]
  18. 18.  Chambers I, Colby D, Robertson M, Nichols J, Lee S et al. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643–55
    [Google Scholar]
  19. 19.  Chazaud C, Yamanaka Y 2016. Lineage specification in the mouse preimplantation embryo. Development 143:1063–74
    [Google Scholar]
  20. 20.  Chazaud C, Yamanaka Y, Pawson T, Rossant J 2006. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 10:615–24
    [Google Scholar]
  21. 21.  Chen L, Yabuuchi A, Eminli S, Takeuchi A, Lu C-W et al. 2009. Cross-regulation of the Nanog and Cdx2 promoters. Cell Res 19:1052–61
    [Google Scholar]
  22. 22.  Chickarmane V, Peterson C 2008. A computational model for understanding stem cell, trophectoderm and endoderm lineage determination. PLOS ONE 3:e3478
    [Google Scholar]
  23. 23.  Ciruna BG, Rossant J 1999. Expression of the T-box gene Eomesodermin during early mouse development. Mech. Dev. 81:199–203
    [Google Scholar]
  24. 24.  Cole MF, Johnstone SE, Newman JJ, Kagey MH, Young RA 2008. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 22:746–55
    [Google Scholar]
  25. 25.  De Mot L, Gonze D, Bessonnard S, Chazaud C, Goldbeter A, Dupont G 2016. Cell fate specification based on tristability in the inner cell mass of mouse blastocysts. Biophys. J. 110:710–22
    [Google Scholar]
  26. 26.  Deglincerti A, Croft GF, Pietila LN, Zernicka-Goetz M, Siggia ED, Brivanlou AH 2016. Self-organization of the in vitro attached human embryo. Nature 533:251–54
    [Google Scholar]
  27. 27.  Deng Q, Ramskold D, Reinius B, Sandberg R 2014. Single-cell RNA-seq reveals dynamic, random monoallelic gene expression in mammalian cells. Science 343:193–96
    [Google Scholar]
  28. 28.  Dietrich JE, Hiiragi T 2007. Stochastic patterning in the mouse pre-implantation embryo. Development 134:4219–31
    [Google Scholar]
  29. 29.  Donnison M, Beaton A, Davey HW, Broadhurst R, L'Huillier P, Pfeffer PL 2005. Loss of the extra-embryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 132:2299–308
    [Google Scholar]
  30. 30.  Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S et al. 2011. Role of YAP/TAZ in mechanotransduction. Nature 474:179–83
    [Google Scholar]
  31. 31.  Evans M, Kaufman MH 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–55
    [Google Scholar]
  32. 32.  Feldman B, Poueymirou W, Papaioannou VE, DeChiara TM, Goldfarb M 1995. Requirement of FGF-4 for postimplantation mouse development. Science 267:246–49
    [Google Scholar]
  33. 33.  Festuccia N, Osorno R, Halbritter F, Karwacki-Neisius V, Navarro P et al. 2012. Esrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cells. Cell Stem Cell 11:477–90
    [Google Scholar]
  34. 34.  Fogarty NME, McCarthy A, Snijders KE, Powell BE, Kubikova N et al. 2017. Erratum: Genome editing reveals a role for OCT4 in human embryogenesis. Nature 551:256
    [Google Scholar]
  35. 35.  Frum T, Ralston A 2015. Cell signaling and transcription factors regulating cell fate during formation of the mouse blastocyst. Trends Genet 31:402–10
    [Google Scholar]
  36. 36.  Gardner RL, Rossant J 1979. Investigation of the fate of 4.5 day post-coitum mouse inner cell mass cells by blastocyst injection. J. Embryol. Exp. Morphol. 52:141–52
    [Google Scholar]
  37. 37.  Georgiades P, Rossant J 2006. Ets2 is necessary in trophoblast for normal embryonic anteroposterior axis development. Development 133:1059–68
    [Google Scholar]
  38. 38.  Goolam M, Scialdone A, Graham SJL, Macaulay IC, Jedrusik A et al. 2016. Heterogeneity in Oct4 and Sox2 targets biases cell fate in 4-cell mouse embryos. Cell 165:61–74
    [Google Scholar]
  39. 39.  Grabarek JB, Żyżyńska K, Saiz N, Piliszek A, Frankenberg S et al. 2012. Differential plasticity of epiblast and primitive endoderm precursors within the ICM of the early mouse embryo. Development 139:129–39
    [Google Scholar]
  40. 40.  Graham SJL, Wicher KB, Jedrusik A, Guo G, Herath W et al. 2014. BMP signalling regulates the pre-implantation development of extra-embryonic cell lineages in the mouse embryo. Nat. Commun. 5:5667
    [Google Scholar]
  41. 41.  Guo F, Li L, Li J, Wu X, Hu B et al. 2017. Single-cell multi-omics sequencing of mouse early embryos and embryonic stem cells. Cell Res 27:967–88
    [Google Scholar]
  42. 42.  Guo G, Huss M, Tong GQ, Wang C, Sun LL et al. 2010. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev. Cell 18:675–85
    [Google Scholar]
  43. 43.  Hemberger M, Udayashankar R, Tesar P, Moore H, Burton GJ 2010. ELF5-enforced transcriptional networks define an epigenetically regulated trophoblast stem cell compartment in the human placenta. Hum. Mol. Genet. 19:2456–67
    [Google Scholar]
  44. 44.  Home P, Ray S, Dutta D, Bronshteyn I, Larson M, Paul S 2009. GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J. Biol. Chem. 284:28729–37
    [Google Scholar]
  45. 45.  Huang D, Guo G, Yuan P, Ralston A, Sun L et al. 2017. The role of Cdx2 as a lineage specific transcriptional repressor for pluripotent network during the first developmental cell lineage segregation. Sci. Rep. 7:17156
    [Google Scholar]
  46. 46.  Irie N, Kuratani S 2014. The developmental hourglass model: a predictor of the basic body plan?. Development 141:4649–55
    [Google Scholar]
  47. 47.  Ishiuchi T, Enriquez-Gasca R, Mizutani E, Bošković A, Ziegler-Birling C et al. 2015. Early embryonic-like cells are induced by downregulating replication-dependent chromatin assembly. Nat. Struct. Mol. Biol. 22:662–71
    [Google Scholar]
  48. 48.  Ivanova N, Dobrin R, Lu R, Kotenko I, Levorse J et al. 2006. Dissecting self-renewal in stem cells with RNA interference. Nature 442:533–38
    [Google Scholar]
  49. 49.  Jiang J, Chan Y-S, Loh Y-H, Cai J, Tong G-Q et al. 2008. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat. Cell Biol. 10:353–60
    [Google Scholar]
  50. 50.  Johnson MH, Ziomek CA 1981. The foundation of two distinct cell lineages within the mouse morula. Cell 24:71–80
    [Google Scholar]
  51. 51.  Kang M, Garg V, Hadjantonakis A-K 2017. Lineage establishment and progression within the inner cell mass of the mouse blastocyst requires FGFR1 and FGFR2. Dev. Cell 41:496–510.e5
    [Google Scholar]
  52. 52.  Kang M, Piliszek A, Artus J, Hadjantonakis A-K 2013. FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development 140:267–79
    [Google Scholar]
  53. 53.  Knott JG, Paul S 2014. Transcriptional regulators of the trophoblast lineage in mammals with hemochorial placentation. Reproduction 148:R121–36
    [Google Scholar]
  54. 54.  Knox K, Baker JC 2008. Genomic evolution of the placenta using co-option and duplication and divergence. Genome Res 18:695–705
    [Google Scholar]
  55. 55.  Ko MSH 2016. Zygotic genome activation revisited: looking through the expression and function of Zscan4. Curr. Top. Dev. Biol. 120:103–24
    [Google Scholar]
  56. 56.  Kobayashi T, Zhang H, Tang WWC, Irie N, Withey S et al. 2017. Principles of early human development and germ cell program from conserved model systems. Nature 546:416–20
    [Google Scholar]
  57. 57.  Kono K, Tamashiro DAA, Alarcon VB 2014. Inhibition of RHO-ROCK signaling enhances ICM and suppresses TE characteristics through activation of Hippo signaling in the mouse blastocyst. Dev. Biol. 394:142–55
    [Google Scholar]
  58. 58.  Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F 1999. The transcription factor GATA6 is essential for early extraembryonic development. Development 126:723–32
    [Google Scholar]
  59. 59.  Krawchuk D, Honma-Yamanaka N, Anani S, Yamanaka Y 2013. FGF4 is a limiting factor controlling the proportions of primitive endoderm and epiblast in the ICM of the mouse blastocyst. Dev. Biol. 384:65–71
    [Google Scholar]
  60. 60.  Krupa M, Mazur E, Szczepańska K, Filimonow K, Maleszewski M, Suwińska A 2014. Allocation of inner cells to epiblast vs primitive endoderm in the mouse embryo is biased but not determined by the round of asymmetric divisions (8 →16- and 16 →32-cells). Dev. Biol. 385:136–48
    [Google Scholar]
  61. 61.  Kuckenberg P, Buhl S, Woynecki T, van Fürden B, Tolkunova E et al. 2010. The transcription factor TCFAP2C/AP-2γ cooperates with CDX2 to maintain trophectoderm formation. Mol. Cell. Biol. 30:3310–20
    [Google Scholar]
  62. 62.  Kuijk EW, van Tol LTA, Van de Velde H, Wubbolts R, Welling M et al. 2012. The roles of FGF and MAP kinase signaling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Development 139:871–82
    [Google Scholar]
  63. 63.  Kunath T, Arnaud D, Uy GD, Okamoto I, Chureau C et al. 2005. Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development 132:1649–61
    [Google Scholar]
  64. 64.  Kurimoto K, Yabuta Y, Ohinata Y, Ono Y, Uno KD et al. 2006. An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res 34:e42
    [Google Scholar]
  65. 65.  Leung CY, Zernicka-Goetz M 2015. Mapping the journey from totipotency to lineage specification in the mouse embryo. Curr. Opin. Genet. Dev. 34:71–76
    [Google Scholar]
  66. 66.  Loh Y-H, Wu Q, Chew J-L, Vega VB, Zhang W et al. 2006. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 38:431–40
    [Google Scholar]
  67. 67.  Lu F, Zhang Y 2015. Cell totipotency: molecular features, induction, and maintenance. Natl. Sci. Rev. 2:217–25
    [Google Scholar]
  68. 68.  Luo J, Sladek R, Bader JA, Matthyssen A, Rossant J, Giguère V 1997. Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-β. Nature 388:778–82
    [Google Scholar]
  69. 69.  Macfarlan TS, Gifford WD, Driscoll S, Lettieri K, Rowe HM et al. 2012. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487:57–63
    [Google Scholar]
  70. 70.  Maeso I, Dunwell TL, Wyatt CD, Marletaz F, Veto B et al. 2016. Evolutionary origin and functional divergence of totipotent cell homeobox genes in eutherian mammals. BMC Biol 14:45
    [Google Scholar]
  71. 71.  Maitre JL, Turlier H, Illukkumbura R, Eismann B, Niwayama R et al. 2016. Asymmetric division of contractile domains couples cell positioning and fate specification. Nature 536:344–48
    [Google Scholar]
  72. 72.  Marks H, Kalkan T, Menafra R, Denissov S, Jones K et al. 2012. The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149:590–604
    [Google Scholar]
  73. 73.  Martin GR 1981. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. PNAS 78:7634–38
    [Google Scholar]
  74. 74.  Merrill BJ, Pasolli HA, Polak L, Rendl M, García-García MJ et al. 2004. Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 131:263–74
    [Google Scholar]
  75. 75.  Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M et al. 2003. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631–42
    [Google Scholar]
  76. 76.  Mohammed H, Hernando-Herraez I, Savino A, Scialdone A, Macaulay I et al. 2017. Single-cell landscape of transcriptional heterogeneity and cell fate decisions during mouse early gastrulation. Cell Rep 20:1215–28
    [Google Scholar]
  77. 77.  Molotkov A, Mazot P, Brewer JR, Cinalli RM, Soriano P 2017. Distinct requirements for FGFR1 and FGFR2 in primitive endoderm development and exit from pluripotency. Dev. Cell 41:511–26.e4
    [Google Scholar]
  78. 78.  Morris SA, Graham SJL, Jedrusik A, Zernicka-Goetz M 2013. The differential response to Fgf signalling in cells internalized at different times influences lineage segregation in preimplantation mouse embryos. Open Biol 3:130104
    [Google Scholar]
  79. 79.  Morris SA, Teo RT, Li H, Robson P, Glover DM, Zernicka-Goetz M 2010. Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. PNAS 107:6364–69
    [Google Scholar]
  80. 80.  Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F et al. 1998. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev 12:3579–90
    [Google Scholar]
  81. 81.  Nakamura T, Okamoto I, Sasaki K, Yabuta Y, Iwatani C et al. 2016. A developmental coordinate of pluripotency among mice, monkeys and humans. Nature 537:57–62
    [Google Scholar]
  82. 82.  Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z et al. 2008. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat. Cell Biol 10:1280–90
    [Google Scholar]
  83. 83.  Niakan KK, Eggan K 2013. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev. Biol. 375:54–64
    [Google Scholar]
  84. 84.  Nichols J, Silva J, Roode M, Smith A 2009. Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 136:3215–22
    [Google Scholar]
  85. 85.  Nichols J, Smith A 2011. The origin and identity of embryonic stem cells. Development 138:3–8
    [Google Scholar]
  86. 86.  Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D et al. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379–91
    [Google Scholar]
  87. 87.  Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M et al. 2009. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16:398–410
    [Google Scholar]
  88. 88.  Nishioka N, Yamamoto S, Kiyonari H, Sato H, Sawada A et al. 2008. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech. Dev. 125:270–83
    [Google Scholar]
  89. 89.  Nissen SB, Perera M, Gonzalez JM, Morgani SM, Jensen MH et al. 2017. Four simple rules that are sufficient to generate the mammalian blastocyst. PLOS Biol 15:e2000737
    [Google Scholar]
  90. 90.  Niwa H 2007. How is pluripotency determined and maintained?. Development 134:635–46
    [Google Scholar]
  91. 91.  Niwa H, Miyazaki J, Smith AG 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24:372–76
    [Google Scholar]
  92. 92.  Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K et al. 2005. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123:917–29
    [Google Scholar]
  93. 93.  Ohnishi Y, Huber W, Tsumura A, Kang M, Xenopoulos P et al. 2014. Cell-to-cell expression variability followed by signal reinforcement progressively segregates early mouse lineages. Nat. Cell Biol. 16:27–37
    [Google Scholar]
  94. 94.  Okae H, Toh H, Sato T, Hiura H, Takahashi S et al. 2018. Derivation of human trophoblast stem cells. Cell Stem Cell 22:50–63.e6
    [Google Scholar]
  95. 95.  Panciera T, Azzolin L, Cordenonsi M, Piccolo S 2017. Mechanobiology of YAP and TAZ in physiology and disease. Nat. Rev. Mol. Cell Biol. 18:758–70
    [Google Scholar]
  96. 96.  Peaston AE, Evsikov AV, Graber JH, de Vries WN, Holbrook AE et al. 2004. Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell 7:597–606
    [Google Scholar]
  97. 97.  Petropoulos S, Edsgard D, Reinius B, Deng Q, Panula SP et al. 2016. Single-cell RNA-seq reveals lineage and X chromosome dynamics in human preimplantation embryos. Cell 165:1012–26
    [Google Scholar]
  98. 98.  Piliszek A, Madeja ZE, Plusa B 2017. Suppression of ERK signalling abolishes primitive endoderm formation but does not promote pluripotency in rabbit embryo. Development 144:3719–30
    [Google Scholar]
  99. 99.  Plachta N, Bollenbach T, Pease S, Fraser SE, Pantazis P 2011. Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nat. Cell Biol. 13:117–23
    [Google Scholar]
  100. 100.  Plusa B, Piliszek A, Frankenberg S, Artus J, Hadjantonakis A-K 2008. Distinct sequential cell behaviours directing primitive endoderm formation in the mouse blastocyst. Development 135:3081–91
    [Google Scholar]
  101. 101.  Posfai E, Petropoulos S, de Barros FRO, Schell JP, Jurisica I et al. 2017. Position- and Hippo signaling-dependent plasticity during lineage segregation in the early mouse embryo. eLife 6:e22906
    [Google Scholar]
  102. 102.  Ralston A, Cox BJ, Nishioka N, Sasaki H, Chea E et al. 2010. Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 137:395–403
    [Google Scholar]
  103. 103.  Rayon T, Menchero S, Nieto A, Xenopoulos P, Crespo M et al. 2014. Notch and Hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev. Cell 30:410–22
    [Google Scholar]
  104. 104.  Rayon T, Menchero S, Rollán I, Ors I, Helness A et al. 2016. Distinct mechanisms regulate Cdx2 expression in the blastocyst and in trophoblast stem cells. Sci. Rep. 6:27139
    [Google Scholar]
  105. 105.  Roode M, Blair K, Snell P, Elder K, Marchant S et al. 2012. Human hypoblast formation is not dependent on FGF signalling. Dev. Biol. 361:358–63
    [Google Scholar]
  106. 106.  Rossant J 2015. Mouse and human blastocyst-derived stem cells: Vive les differences. Development 142:9–12
    [Google Scholar]
  107. 107.  Rossant J, Chazaud C, Yamanaka Y 2003. Lineage allocation and asymmetries in the early mouse embryo. Philos. Trans. R. Soc. B 358:1341–49
    [Google Scholar]
  108. 108.  Rossant J, Tam PPL 2009. Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136:701–13
    [Google Scholar]
  109. 109.  Rossant J, Tam PPL 2017. New insights into early human development: lessons for stem cell derivation and differentiation. Cell Stem Cell 20:18–28
    [Google Scholar]
  110. 110.  Russ AP, Wattler S, Colledge WH, Aparicio SAJR, Carlton MBL et al. 2000. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404:95–99
    [Google Scholar]
  111. 111.  Saiz N, Williams KM, Seshan VE, Hadjantonakis A-K 2016. Asynchronous fate decisions by single cells collectively ensure consistent lineage composition in the mouse blastocyst. Nat. Commun. 7:13463
    [Google Scholar]
  112. 112.  Sasaki H 2017. Roles and regulations of Hippo signaling during preimplantation mouse development. Dev. Growth Differ. 59:12–20
    [Google Scholar]
  113. 113.  Sasaki K, Nakamura T, Okamoto I, Yabuta Y, Iwatani C et al. 2016. The germ cell fate of cynomolgus monkeys is specified in the nascent amnion. Dev. Cell 39:169–85
    [Google Scholar]
  114. 114.  Schöler HR, Balling R, Hatzopoulous AK, Suzuki N, Gruss P 1989. Octamer binding proteins confer transcriptional activity in early mouse embryogenesis. EMBO J 8:2551–57
    [Google Scholar]
  115. 115.  Shao Y, Taniguchi K, Townshend RF, Miki T, Gumucio DL, Fu J 2017. A pluripotent stem cell-based model for post-implantation human amniotic sac development. Nat. Commun. 8:208
    [Google Scholar]
  116. 116.  Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K et al. 2005. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132:2093–102
    [Google Scholar]
  117. 117.  Suwińska A, Czołowska R, Ożdżeński W, Tarkowski AK 2008. 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. 322:133–44
    [Google Scholar]
  118. 118.  Svoboda P, Franke V, Schultz RM 2015. Sculpting the transcriptome during the oocyte-to-embryo transition in mouse. Curr. Top. Dev. Biol. 113:305–49
    [Google Scholar]
  119. 119.  Tang F, Barbacioru C, Nordman E, Bao S, Lee C et al. 2011. Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLOS ONE 6:e21208
    [Google Scholar]
  120. 120.  Tarkowski AK, Wroblewska J 1967. Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J. Embryol. Exp. Morphol. 18:155–80
    [Google Scholar]
  121. 121.  Tewary M, Ostblom J, Prochazka L, Zulueta-Coarasa T, Shakiba N et al. 2017. A stepwise model of reaction-diffusion and positional information governs self-organized human peri-gastrulation-like patterning. Development 144:4298–312
    [Google Scholar]
  122. 122.  Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M 2007. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445:214–18
    [Google Scholar]
  123. 123.  Tosenberger A, Gonze D, Bessonnard S, Cohen-Tannoudji M, Chazaud C, Dupont G 2017. A multiscale model of early cell lineage specification including cell division. NPJ Syst. Biol. Appl. 3:16
    [Google Scholar]
  124. 124.  Vassilev A, Kaneko KJ, Shu H, Zhao Y, DePamphilis ML 2001. TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev 15:1229–41
    [Google Scholar]
  125. 125.  Wamaitha SE, del Valle I, Cho LTY, Wei Y, Fogarty NME et al. 2015. Gata6 potently initiates reprograming of pluripotent and differentiated cells to extraembryonic endoderm stem cells. Genes Dev 29:1239–55
    [Google Scholar]
  126. 126.  Warmflash A, Sorre B, Etoc F, Siggia ED, Brivanlou AH 2014. A method to recapitulate early embryonic spatial patterning in human embryonic stem cells. Nat. Methods 11:847–54
    [Google Scholar]
  127. 127.  Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–62
    [Google Scholar]
  128. 128.  White MD, Angiolini JF, Alvarez YD, Kaur G, Zhao ZW et al. 2016. Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165:75–87
    [Google Scholar]
  129. 129.  Wicklow E, Blij S, Frum T, Hirate Y, Lang RA et al. 2014. HIPPO pathway members restrict SOX2 to the inner cell mass where it promotes ICM fates in the mouse blastocyst. PLOS Genet 10:e1004618
    [Google Scholar]
  130. 130.  Wigger M, Kisielewska K, Filimonow K, Plusa B, Maleszewski M, Suwińska A 2017. Plasticity of the inner cell mass in mouse blastocyst is restricted by the activity of FGF/MAPK pathway. Sci. Rep. 7:15136
    [Google Scholar]
  131. 131.  Wu G, Gentile L, Fuchikami T, Sutter J, Psathaki K et al. 2010. Initiation of trophectoderm lineage specification in mouse embryos is independent of Cdx2. Development 137:4159–69
    [Google Scholar]
  132. 132.  Wu G, Lei L, Schöler HR 2017. Totipotency in the mouse. J. Mol. Med. 95:687–94
    [Google Scholar]
  133. 133.  Wu S, Liu Y, Zheng Y, Dong J, Pan D 2008. The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev. Cell 14:388–98
    [Google Scholar]
  134. 134.  Yagi R, Kohn MJ, Karavanova I, Kaneko KJ, Vullhorst D et al. 2007. Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134:3827–36
    [Google Scholar]
  135. 135.  Yamanaka Y, Lanner F, Rossant J 2010. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137:715–24
    [Google Scholar]
  136. 136.  Young RA 2011. Control of the embryonic stem cell state. Cell 144:940–54
    [Google Scholar]
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