Cell fate decisions and axis determination in the early mouse embryo

Development

Volumn 139, Issue 1, 2011, Pages 3-14

  Takaoka, Katsuyoshi ^a,b   Hamada, Hiroshi ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

AP axis; Blastocyst; Cell fate; Inner cell mass; Primitive endoderm; Trophectoderm

Indexed keywords

TRANSCRIPTION FACTOR;

BLASTOCYST; CELL FATE; CELL LINEAGE; ECTODERM; EMBRYO DEVELOPMENT; EMBRYO POLARITY; ENDODERM; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; REVIEW;

EID: 82855176836     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.060095     Document Type: Review

References (108)

1. Andersson, O., Bertolino, P. and Ibanez, C. F. (2007). Distinct and cooperative roles of mammalian Vg1 homologs GDF1 and GDF3 during early embryonic development. Dev. Biol. 311, 500-511.
2. Arman, E., Haffner-Krausz, R., Chen, Y., Heath, J. K. and Lonai, P. (1998). Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl. Acad. Sci. USA 95, 5082-5087.
3. Beck, S., Le Good, J. A., Guzman, M., Ben Haim, N., Roy, K., Beermann, F. and Constam, D. B. (2002). Extraembryonic proteases regulate Nodal signalling during gastrulation. Nat. Cell Biol. 4, 981-985.
4. Beddington, R. S. and Robertson, E. J. (1998). Anterior patterning in mouse. Trends Genet. 14, 277-284.
5. Ben-Haim, N., Lu, C., Guzman-Ayala, M., Pescatore, L., Mesnard, D., Bischofberger, M., Naef, F., Robertson, E. J. and Constam, D. B. (2006). The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev. Cell 11, 313-323.
6. Beppu, H., Kawabata, M., Hamamoto, T., Chytil, A., Minowa, O., Noda, T. and Miyazono, K. (2000). BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev. Biol. 221, 249-258.
7. Brennan, J., Lu, C. C., Norris, D. P., Rodriguez, T. A., Beddington, R. S. and Robertson, E. J. (2001). Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411, 965-969.
8. Camus, A., Perea-Gomez, A., Moreau, A. and Collignon, J. (2006). Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev. Biol. 295, 743-755.
9. Carter, M. G., Hamatani, T., Sharov, A. A., Carmack, C. E., Qian, Y., Aiba, K., Ko, N. T., Dudekula, D. B., Brzoska, P. M., Hwang, S. S. et al. (2003). In situ- synthesized novel microarray optimized for mouse stem cell and early developmental expression profiling. Genome Res. 13, 1011-1021.
10. Chambers, I., Silva, J., Colby, D., Nichols, J., Nijmeijer, B., Robertson, M., Vrana, J., Jones, K., Grotewold, L. and Smith, A. (2007). Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1234.
11. Chazaud, C., Yamanaka, Y., Pawson, T. and Rossant, J. (2006). Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev. Cell 10, 615-624.
12. Chen, C., Ware, S. M., Sato, A., Houston-Hawkins, D. E., Habas, R., Matzuk, M. M., Shen, M. M. and Brown, C. W. (2006). The Vg1-related protein Gdf3 acts in a Nodal signaling pathway in the pre-gastrulation mouse embryo. Development 133, 319-329.
13. Cheng, A. M., Saxton, T. M., Sakai, R., Kulkarni, S., Mbamalu, G., Vogel, W., Tortorice, C. G., Cardiff, R. D., Cross, J. C., Muller, W. J. et al. (1998). Mammalian Grb2 regulates multiple steps in embryonic development and malignant transformation. Cell 95, 793-803.
14. Chu, J. and Shen, M. M. (2010). Functional redundancy of EGF-CFC genes in epiblast and extraembryonic patterning during early mouse embryogenesis. Dev. Biol. 342, 63-73.
15. del Barco Barrantes, I., Davidson, G., Grone, H. J., Westphal, H. and Niehrs, C. (2003). Dkk1 and noggin cooperate in mammalian head induction. Genes Dev. 17, 2239-2244.
16. Dietrich, J. E. and Hiiragi, T. (2007). Stochastic patterning in the mouse pre- implantation embryo. Development 134, 4219-4231.
17. Ding, J., Yang, L., Yan, Y. T., Chen, A., Desai, N., Wynshaw-Boris, A. and Shen, M. M. (1998). Cripto is required for correct orientation of the anterior- posterior axis in the mouse embryo. Nature 395, 702-707.
18. Erhardt, S., Su, I. H., Schneider, R., Barton, S., Bannister, A. J., Perez-Burgos, L., Jenuwein, T., Kouzarides, T., Tarakhovsky, A. and Surani, M. A. (2003). Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 130, 4235-4248.
19. Feldman, B., Poueymirou, W., Papaioannou, V. E., DeChiara, T. M. and Goldfarb, M. (1995). Requirement of FGF-4 for postimplantation mouse development. Science 267, 246-249.
20. Gardner, R. L. (1997). The early blastocyst is bilaterally symmetrical and its axis of symmetry is aligned with the animal-vegetal axis of the zygote in the mouse. Development 124, 289-301.
21. Gerbe, F., Cox, B., Rossant, J. and Chazaud, C. (2008). Dynamic expression of Lrp2 pathway members reveals progressive epithelial differentiation of primitive endoderm in mouse blastocyst. Dev. Biol. 313, 594-602.
22. Gerhart, J., Danilchik, M., Doniach, T., Roberts, S., Rowning, B. and Stewart, R. (1989). Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 107 Suppl., 37-51.
23. Granier, C., Gurchenkov, V., Perea-Gomez, A., Camus, A., Ott, S., Papanayotou, C., Iranzo, J., Moreau, A., Reid, J., Koentges, G. et al. (2011). Nodal cis-regulatory elements reveal epiblast and primitive endoderm heterogeneity in the peri-implantation mouse embryo. Dev. Biol. 349, 350-362.
24. Guo, G. J., Huss, M., Tong, G. Q., Wang, C. Y., Sun, L. L., Clarke, N. D. and Robson, P. (2010). Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev. Cell 18, 675-685.
25. Hamazaki, T., Kehoe, S. M., Nakano, T. and Terada, N. (2006). The Grb2/Mek pathway represses Nanog in murine embryonic stem cells. Mol. Cell. Biol. 26, 7539-7549.
26. Hiiragi, T. and Solter, D. (2004). First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei. Nature 430, 360-364.
27. Huelsken, J., Vogel, R., Brinkmann, V., Erdmann, B., Birchmeier, C. and Birchmeier, W. (2000). Requirement for beta-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148, 567-578.
28. Huynh, J. R. and St Johnston, D. (2004). The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr. Biol. 14, R438-R449.
29. Hyafil, F., Morello, D., Babinet, C. and Jacob, F. (1980). A cell-surface glycoprotein involved in the compaction of embryonal carcinoma-cells and cleavage stage embryos. Cell 21, 927-934.
30. Johnson, M. H. and McConnell, J. M. (2004). Lineage allocation and cell polarity during mouse embryogenesis. Semin. Cell Dev. Biol. 15, 583-597.
31. Johnson, M. H. and Ziomek, C. A. (1981). The foundation of two distinct cell lineages within the mouse morula. Cell 24, 71-80.
32. Kemp, C., Willems, E., Abdo, S., Lambiv, L. and Leyns, L. (2005). Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Dev. Dyn. 233, 1064-1075.
33. Kielman, M. F., Rindapaa, M., Gaspar, C., van Poppel, N., Breukel, C., van Leeuwen, S., Taketo, M. M., Roberts, S., Smits, R. and Fodde, R. (2002). Apc modulates embryonic stem-cell differentiation by controlling the dosage of beta-catenin signaling. Nat. Genet. 32, 594-605.
34. Kimura, C., Yoshinaga, K., Tian, E., Suzuki, M., Aizawa, S. and Matsuo, I. (2000). Visceral endoderm mediates forebrain development by suppressing posteriorizing signals. Dev. Biol. 225, 304-321.
35. Kimura, C., Shen, M. M., Takeda, N., Aizawa, S. and Matsuo, I. (2001). Complementary functions of Otx2 and Cripto in initial patterning of mouse epiblast. Dev. Biol. 235, 12-32.
36. Kimura-Yoshida, C., Nakano, H., Okamura, D., Nakao, K., Yonemura, S., Belo, J. A., Aizawa, S., Matsui, Y. and Matsuo, I. (2005). Canonical Wnt signaling and its antagonist regulate anterior-posterior axis polarization by guiding cell migration in mouse visceral endoderm. Dev. Cell 9, 639-650.
37. Kloc, M. and Etkin, L. D. (2005). RNA localization mechanisms in oocytes. J. Cell Sci. 118, 269-282.
38. Kurotaki, Y., Hatta, K., Nakao, K., Nabeshima, Y. and Fujimori, T. (2007). Blastocyst axis is specified independently of early cell lineage but aligns with the ZP shape. Science 316, 719-723.
39. Lanner, F. and Rossant, J. (2010). The role of FGF/Erk signaling in pluripotent cells. Development 137, 3351-3360.
40. Lanner, F., Lee, K. L., Sohl, M., Holmborn, K., Yang, H., Wilbertz, J., Poellinger, L., Rossant, J. and Farnebo, F. Heparan sulfation-dependent fibroblast growth factor signaling maintains embryonic stem cells primed for differentiation in a heterogeneous state. Stem Cells 28, 191-200.
41. Li, L., Zheng, P. and Dean, J. (2010). Maternal control of early mouse development. Development 137, 859-870.
42. Lowe, L. A., Yamada, S. and Kuehn, M. R. (2001). Genetic dissection of nodal function in patterning the mouse embryo. Development 128, 1831-1843.
43. Lu, C. C. and Robertson, E. J. (2004). Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning. Dev. Biol. 273, 149-159.
44. Meilhac, S. M., Adams, R. J., Morris, S. A., Danckaert, A., Le Garrec, J. F. and Zernicka-Goetz, M. (2009). Active cell movements coupled to positional induction are involved in lineage segregation in the mouse blastocyst. Dev. Biol. 331, 210-221.
45. Mesnard, D. and Constam, D. B. Imaging proprotein convertase activities and their regulation in the implanting mouse blastocyst. J. Cell Biol. 191, 129-139.
46. Mesnard, D., Guzman-Ayala, M. and Constam, D. B. (2006). Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 133, 2497-2505.
47. Migeotte, I., Omelchenko, T., Hall, A. and Anderson, K. V. (2010). Rac1- dependent collective cell migration is required for specification of the anterior- posterior body axis of the mouse. PLoS Biol. 8, e1000442.
48. Mishina, Y., Suzuki, A., Ueno, N. and Behringer, R. R. (1995). Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9, 3027-3037.
49. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M. and Yamanaka, S. (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642.
50. Miura, S. and Mishina, Y. (2007). The DVE changes distal epiblast fate from definitive endoderm to neurectoderm by antagonizing nodal signaling. Dev. Dyn. 236, 1602-1610.
51. Miura, S., Singh, A. P. and Mishina, Y. (2010). Bmpr1a is required for proper migration of the AVE through regulation of Dkk1 expression in the pre-streak mouse embryo. Dev. Biol. 341, 246-254.
52. Morkel, M., Huelsken, J., Wakamiya, M., Ding, J., van de Wetering, M., Clevers, H., Taketo, M. M., Behringer, R. R., Shen, M. M. and Birchmeier, W. (2003). Beta-catenin regulates Cripto- and Wnt3-dependent gene expression programs in mouse axis and mesoderm formation. Development 130, 6283-6294.
53. Morris, S. A., Teo, R. T., Li, H., Robson, P., Glover, D. M. and Zernicka-Goetz, M. (2010). Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc. Natl. Acad. Sci. USA 107, 6364-6369.
54. Morris, S. M., Arden, S. D., Roberts, R. C., Kendrick-Jones, J., Cooper, J. A., Luzio, J. P. and Buss, F. (2002). Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 3, 331-341.
55. Motosugi, N., Bauer, T., Polanski, Z., Solter, D. and Hiiragi, T. (2005). Polarity of the mouse embryo is established at blastocyst and is not prepatterned. Genes Dev. 19, 1081-1092.
56. Nakamura, T., Mine, N., Nakaguchi, E., Mochizuki, A., Yamamoto, M., Yashiro, K., Meno, C. and Hamada, H. (2006). Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral- inhibition system. Dev. Cell 11, 495-504.
57. Nichols, J., Silva, J., Roode, M. and Smith, A. (2009). Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 136, 3215-3222.
58. Nishida, H. and Sawada, K. (2001). macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. Nature 409, 724-729.
59. Nishioka, N., Yamamoto, S., Kiyonari, H., Sato, H., Sawada, A., Ota, M., Nakao, K. and Sasaki, H. (2008). Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech. Dev. 125, 270-283.
60. Nishioka, N., Inoue, K., Adachi, K., Kiyonari, H., Ota, M., Ralston, A., Yabuta, N., Hirahara, S., Stephenson, R. O., Ogonuki, N. 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.
61. Niwa, H., Toyooka, Y., Shimosato, D., Strumpf, D., Takahashi, K., Yagi, R. and Rossant, J. (2005). Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123, 917-929.
62. Nomura, M. and Li, E. (1998). Smad2 role in mesoderm formation, left-right patterning and craniofacial development. Nature 393, 786-790.
63. Norris, D. P., Brennan, J., Bikoff, E. K. and Robertson, E. J. (2002). The Foxh1- dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 129, 3455-3468.
64. Pan, D. (2007). Hippo signaling in organ size control. Genes Dev. 21, 886-897.
65. Parfitt, D. E. and Zernicka-Goetz, M. (2010). Epigenetic modification affecting expression of cell polarity and cell fate genes to regulate lineage specification in the early mouse embryo. Mol. Biol. Cell 21, 2649-2660.
66. Pauken, C. M. and Capco, D. G. (2000). The expression and stage-specific localization of protein kinase C isotypes during mouse preimplantation development. Dev. Biol. 223, 411-421.
67. Perea-Gomez, A., Lawson, K. A., Rhinn, M., Zakin, L., Brulet, P., Mazan, S. and Ang, S. L. (2001). Otx2 is required for visceral endoderm movement and for the restriction of posterior signals in the epiblast of the mouse embryo. Development 128, 753-765.
68. Perea-Gomez, A., Vella, F. D., Shawlot, W., Oulad-Abdelghani, M., Chazaud, C., Meno, C., Pfister, V., Chen, L., Robertson, E., Hamada, H. et al. (2002). Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev. Cell 3, 745-756.
69. Piotrowska, K. and Zernicka-Goetz. M. (2001). Role for sperm in spatial patterning of the early mouse embryo. Nature 409, 517-521.
70. Plachta, N., Bollenbach, T., Pease, S., Fraser, S. E. and Pantazis, P. (2011). Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nat. Cell Biol. 13, 337.
71. Plusa, B., Frankenberg, S., Chalmers, A., Hadjantonakis, A. K., Moore, C. A., Papalopulu, N., Papaioannou, V. E., Glover, D. M. and Zernicka-Goetz, M. (2005). Downregulation of Par3 and aPKC function directs cells towards the ICM in the preimplantation mouse embryo. J. Cell Sci. 118, 505-515.
72. Plusa, B., Piliszek, A., Frankenberg, S., Artus, J. and Hadjantonakis, A. K. (2008). Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135, 3081-3091.
73. Rakeman, A. S. and Anderson, K. V. (2006). Axis specification and morphogenesis in the mouse embryo require Nap1, a regulator of WAVE- mediated actin branching. Development 133, 3075-3083.
74. Ralston, A., Cox, B. J., Nishioka, N., Sasaki, H., Chea, E., Rugg-Gunn, P., Guo, G., Robson, P., Draper, J. S. and Rossant, J. (2010). Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 137, 395-403.
75. Reik, W., Santos, F., Mitsuya, K., Morgan, H. and Dean, W. (2003). Epigenetic asymmetry in the mammalian zygote and early embryo: relationship to lineage commitment? Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 1403-1409.
76. Rivera-Perez, J. A., Mager, J. and Magnuson, T. (2003). Dynamic morphogenetic events characterize the mouse visceral endoderm. Dev. Biol. 261, 470-487.
77. Rossant, J. and Tam, P. P. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701-713.
78. Saucedo, L. J. and Edgar, B. A. (2007). Filling out the Hippo pathway. Nat. Rev. Mol. Cell Biol. 8, 613-621.
79. Schneider, S. Q. and Bowerman, B. (2003). Cell polarity and the cytoskeleton in the Caenorhabditis elegans zygote. Annu. Rev. Genet. 37, 221-249.
80. Shirayoshi, Y., Takeichi, M. and Okada, T. S. (1983). Roles of cell-cell contact in mouse early embryonic-development. Cell 25, 428-428.
81. Singh, A. M., Hamazaki, T., Hankowski, K. E. and Terada, N. (2007). A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25, 2534-2542.
82. Soares, M. L., Torres-Padilla, M. E. and Zernicka-Goetz, M. (2008). Bone morphogenetic protein 4 signaling regulates development of the anterior visceral endoderm in the mouse embryo. Dev. Growth Differ. 50, 615-621.
83. Srinivas, S., Rodriguez, T., Clements, M., Smith, J. C. and Beddington, R. S. (2004). Active cell migration drives the unilateral movements of the anterior visceral endoderm. Development 131, 1157-1164.
84. St Johnston, D. (2005). Moving messages: the intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 6, 363-375.
85. Strumpf, D., Mao, C. A., Yamanaka, Y., Ralston, A., Chawengsaksophak, K., Beck, F. and Rossant, J. (2005). Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093-2102.
86. Stuckey, D. W., Clements, M., Di-Gregorio, A., Senner, C. E., Le Tissier, P., Srinivas, S. and Rodriguez, T. A. (2011). Coordination of cell proliferation and anterior-posterior axis establishment in the mouse embryo. Development 138, 1521-1530.
87. Sugihara, K., Nakatsuji, N., Nakamura, K., Nakao, K., Hashimoto, R., Otani, H., Sakagami, H., Kondo, H., Nozawa, S., Aiba, A. et al. (1998). Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 17, 3427-3433.
88. Takaoka, K., Yamamoto, M., Shiratori, H., Meno, C., Rossant, J., Saijoh, Y. and Hamada, H. (2006). The mouse embryo autonomously acquires anterior- posterior polarity at implantation. Dev. Cell 10, 451-459.
89. Takaoka, K., Yamamoto, M. and Hamada, H. (2011). Origin and role of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat. Cell Biol. 13, 743-752.
90. Tao, H., Suzuki, M., Kiyonari, H., Abe, T., Sasaoka, T. and Ueno, N. (2009). Mouse prickle1, the homolog of a PCP gene, is essential for epiblast apical-basal polarity. Proc. Natl. Acad. Sci. USA 106, 14426-14431.
91. Tarkowski, A. K. and Wroblewska, J. (1967). Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J. Embryol. Exp. Morphol. 18, 155-180.
92. Thomas, P. and Beddington, R. (1996). Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6, 1487-1496.
93. Torres-Padilla, M. E., Parfitt, D. E., Kouzarides, T. and Zernicka-Goetz, M. (2007a). Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445, 214-218.
94. Torres-Padilla, M. E., Richardson, L., Kolasinska, P., Meilhac, S. M., Luetke-Eversloh, M. V. and Zernicka-Goetz, M. (2007b). The anterior visceral endoderm of the mouse embryo is established from both preimplantation precursor cells and by de novo gene expression after implantation. Dev. Biol. 309, 97-112.
95. Trichas, G., Joyce, B., Crompton, L. A., Wilkins, V., Clements, M., Tada, M., Rodriguez, T. A. and Srinivas, S. (2011). Nodal dependent differential localisation of dishevelled-2 demarcates regions of differing cell behaviour in the visceral endoderm. PLoS Biol. 9, e1001019.
96. VerMilyea, M. D., O'Neill, L. P. and Turner, B. M. (2009). Transcription- independent heritability of induced histone modifications in the mouse preimplantation embryo. PLoS ONE 4, e6086.
97. VerMilyea, M. D., Maneck, M., Yoshida, N., Blochberger, I., Suzuki, E., Suzuki, T., Spang, R., Klein, C. A. and Perry, A. C. (2011). Transcriptome asymmetry within mouse zygotes but not between early embryonic sister blastomeres. EMBO J. 30, 1841-1851.
98. Vinot, S., Le T., Ohno, S., Pawson, T., Maro, B. and Louvet-Vallee, S. (2005). Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8- cell stage during compaction. Dev. Biol. 282, 307-319.
99. Waldrip, W. R., Bikoff, E. K., Hoodless, P. A., Wrana, J. L. and Robertson, E. J. (1998). Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell 92, 797-808.
100. Wang, Q. T., Piotrowska, K., Ciemerych, M. A., Milenkovic, L., Scott, M. P., Davis, R. W. and Zernicka-Goetz, M. (2004). A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev. Cell 6, 133-144.
101. Wilder, P. J., Kelly, D., Brigman, K., Peterson, C. L., Nowling, T., Gao, Q. S., McComb, R. D., Capecchi, M. R. and Rizzino, A. (1997). Inactivation of the FGF-4 gene in embryonic stem cells alters the growth and/or the survival of their early differentiated progeny. Dev. Biol. 192, 614-629.
102. Winnier, G., Blessing, M., Labosky, P. A. and Hogan, B. L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
103. Yagi, R., Kohn, M. J., Karavanova, I., Kaneko, K. J., Vullhorst, D., DePamphilis, M. L. and Buonanno, A. (2007). Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 134, 3827-3836.
104. Yamamoto, M., Meno, C., Sakai, Y., Shiratori, H., Mochida, K., Ikawa, Y., Saijoh, Y. and Hamada, H. (2001). The transcription factor FoxH1 (FAST) mediates Nodal signaling during anterior-posterior patterning and node formation in the mouse. Genes Dev. 15, 1242-1256.
105. Yamamoto, M., Saijoh, Y., Perea-Gomez, A., Shawlot, W., Behringer, R. R., Ang, S. L., Hamada, H. and Meno, C. (2004). Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428, 387-392.
106. Yamamoto, M., Beppu, H., Takaoka, K., Meno, C., Li, E., Miyazono, K. and Hamada, H. (2009). Antagonism between Smad1 and Smad2 signaling determines the site of distal visceral endoderm formation in the mouse embryo. J. Cell Biol. 184, 323-334.
107. Yamanaka, Y., Lanner, F. and Rossant, J. (2010). FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137, 715-724.
108. Yang, D. H., Smith, E. R., Roland, I. H., Sheng, Z., He, J., Martin, W. D., Hamilton, T. C., Lambeth, J. D. and Xu, X. X. (2002). Disabled-2 is essential for endodermal cell positioning and structure formation during mouse embryogenesis. Dev. Biol. 251, 27-44.