Defining pathways that enforce cell lineage specification in early development and stem cells

Cell Cycle

Volumn 8, Issue 10, 2009, Pages 1515-1525

  Roper, Stephen ^a   Hemberger, Myriam ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Blastocyst; Cell fate; Development; Early embryo; Lineage commitment; Pluripotency; Stem cells; Transdifferentiation; Trophoblast

Indexed keywords

CYTOKINE; TRANSCRIPTION FACTOR;

CELL FATE; CELL LINEAGE; CELL MATURATION; CELL SPECIFICITY; CELL TRANSDIFFERENTIATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EPIGENETICS; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TROPHOBLAST;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CYTOKINES; EMBRYO, MAMMALIAN; SIGNAL TRANSDUCTION; STEM CELLS; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 66849129359     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.10.8381     Document Type: Review

References (132)

1. Rossant J. Stem cells and early lineage development. Cell 2008; 132:527-531
2. Kwon GS, Viotti M, Hadjantonakis AK. The endoderm of the mouse embryo arises by dynamic widespread intercalation of embryonic and extraembryonic lineages. Dev Cell 2008; 15:509-520
3. Gardner RL, Johnson MH. An investigation of inner cell mass and trophoblast tissues following their isolation from the mouse blastocyst. J Embryol Exp Morphol 1972; 28:279-312.
4. Rossant J. Investigation of the determinative state of the mouse inner cell mass II. The fate of isolated inner cell masses transferred to the oviduct. J Embryol Exp Morphol 1975; 33:991-1001.
5. Rossant J. Investigation of the determinative state of the mouse inner cell mass I. Aggregation of isolated inner cell masses with morulae. J Embryol Exp Morphol 1975; 33:979-990
6. Gardner RL, Papaioannou VE, Barton SC. Origin of the ectoplacental cone and secondary giant cells in mouse blastocysts reconstituted from isolated trophoblast and inner cell mass. J Embryol Exp Morphol 1973; 30:561-572
7. Johnson MH, Ziomek CA. Cell interactions influence the fate of mouse blastomeres undergoing the transition from the 16- to the 32-cell stage. Dev Biol 1983; 95:211-218 (Pubitemid 13157167)
8. Fleming TP. A quantitative analysis of cell allocation to trophectoderm and inner cell mass in the mouse blastocyst. Dev Biol 1987; 119:520-531 (Pubitemid 17026458)
9. Dyce J, George M, Goodall H, Fleming TP. Do trophectoderm and inner cell mass cells in the mouse blastocyst maintain discrete lineages? Development 1987; 100:685-698
10. Nichols J, Gardner RL. Heterogeneous differentiation of external cells in individual isolated early mouse inner cell masses in culture. J Embryol Exp Morphol 1984; 80:225-240 (Pubitemid 14149319)
11. Rossant J, Lis WT. Potential of isolated mouse inner cell masses to form trophectoderm derivatives in vivo. Dev Biol 1979; 70:255-261 (Pubitemid 9186484)
12. Kahan BW, Ephrussi B. Developmental potentialities of clonal in vitro cultures of mouse testicular teratoma. J Natl Cancer Inst 1970; 44:1015-1036
13. Kleinsmith LJ, Pierce GB Jr. Multipotentiality of single embryonal carcinoma cells. Cancer Res 1964; 24:1544-1551
14. Martin GR, Evans MJ. Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA 1975; 72:1441-1445
15. Martin GR, Wiley LM, Damjanov I. The development of cystic embryoid bodies in vitro from clonal teratocarcinoma stem cells. Dev Biol 1977; 61:230-244 (Pubitemid 8248676)
16. Mintz B, Illmensee K. Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc Natl Acad Sci USA 1975; 72:3585-3589
17. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292:154-156 (Pubitemid 11050741)
18. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981; 78:7634-7638 (Pubitemid 12186197)
19. Brook FA, Gardner RL. The origin and efficient derivation of embryonic stem cells in the mouse. Proc Natl Acad Sci USA 1997; 94:5709-5712 (Pubitemid 27241834)
20. Beddington RS, Robertson EJ. An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 1989; 105:733-737 (Pubitemid 19107071)
21. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci USA 1993; 90:8424-8428 (Pubitemid 23277681)
22. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998; 282:2072 (Pubitemid 29001261)
23. Uy GD, Downs KM, Gardner RL. Inhibition of trophoblast stem cell potential in chorionic ectoderm coincides with occlusion of the ectoplacental cavity in the mouse. Development 2002; 129:3913-3924 (Pubitemid 34994020)
24. Strickland S, Mahdavi V. The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell 1978; 15:393-403. (Pubitemid 9052408)
25. Strickland S, Smith KK, Marotti KR. Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell 1980; 21:347-355 (Pubitemid 10047088)
26. Kunath T, Arnaud D, Uy GD, Okamoto I, Chureau C, Yamanaka Y, et al. Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development 2005; 132:1649-1661 (Pubitemid 40575865)
27. Smith AG, Heath JK, Donaldson DD, Wong GG, Moreau J, Stahl M, et al. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 1988; 336:688-690 (Pubitemid 19007952)
28. Williams RL, Hilton DJ, Pease S, Willson TA, Stewart CL, Gearing DP, et al. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 1988; 336:684-687 (Pubitemid 19007951)
29. Gearing DP, Thut CJ, VandeBos T, Gimpel SD, Delaney PB, King J, et al. Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130. EMBO J 1991; 10:2839-2848 (Pubitemid 21905301)
30. Yoshida K, Chambers I, Nichols J, Smith A, Saito M, Yasukawa K, et al. Maintenance of the pluripotential phenotype of embryonic stem cells through direct activation of gp130 signaling pathways. Mech Dev 1994; 45:163-171 (Pubitemid 24061363)
31. Niwa H, Burdon T, Chambers I, Smith A. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 1998; 12:2048-2060 (Pubitemid 28323878)
32. Matsuda T, Nakamura T, Nakao K, Arai T, Katsuki M, Heike T, et al. STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells. EMBO J 1999; 18:4261-4269 (Pubitemid 29364128)
33. Nichols J, Davidson D, Taga T, Yoshida K, Chambers I, Smith A. Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mech Dev 1996; 57:123-131 (Pubitemid 26252547)
34. Yoshida K, Taga T, Saito M, Suematsu S, Kumanogoh A, Tanaka T, et al. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci USA 1996; 93:407-411 (Pubitemid 26041485)
35. Nichols J, Chambers I, Taga T, Smith A. Physiological rationale for responsiveness of mouse embryonic stem cells to gp130 cytokines. Development 2001; 128:2333-2339 (Pubitemid 32633366)
36. Hemberger M, Hughes M, Cross JC. Trophoblast stem cells differentiate in vitro into invasive trophoblast giant cells. Dev Biol 2004; 271:362-371 (Pubitemid 38833667)
37. Niswander L, Martin GR. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 1992; 114:755-768
38. Rappolee DA, Basilico C, Patel Y, Werb Z. Expression and function of FGF-4 in periimplantation development in mouse embryos. Development 1994; 120:2259-2269 (Pubitemid 24232292)
39. Haffner-Krausz R, Gorivodsky M, Chen Y, Lonai P. Expression of Fgfr2 in the early mouse embryo indicates its involvement in preimplantation development. Mech Dev 1999; 85:167-172 (Pubitemid 29343760)
40. Arman E, Haffner-Krausz R, Chen Y, Heath JK, Lonai P. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc Natl Acad Sci USA 1998; 95:5082-5087 (Pubitemid 28208554)
41. Feldman B, Poueymirou W, Papaioannou VE, DeChiara TM, Goldfarb M. Requirement of FGF-4 for postimplantation mouse development. Science 1995; 267:246-249
42. Gotoh N, Manova K, Tanaka S, Murohashi M, Hadari Y, Lee A, et al. The docking protein FRS2alpha is an essential component of multiple fibroblast growth factor responses during early mouse development. Mol Cell Biol 2005; 25:4105-4116 (Pubitemid 40617657)
43. Saba-El-Leil MK, Vella FD, Vernay B, Voisin L, Chen L, Labrecque N, et al. An essential function of the mitogen-activated protein kinase Erk2 in mouse trophoblast development. EMBO Rep 2003; 4:964-968 (Pubitemid 37407464)
44. Erlebacher A, Price KA, Glimcher LH. Maintenance of mouse trophoblast stem cell proliferation by TGFbeta/activin. Dev Biol 2004; 275:158-169 (Pubitemid 39298181)
45. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000; 24:372-376 (Pubitemid 30187435)
46. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003; 113:631-642 (Pubitemid 36694188)
47. Elling U, Klasen C, Eisenberger T, Anlag K, Treier M. Murine inner cell mass-derived lineages depend on Sall4 function. Proc Natl Acad Sci USA 2006; 103:16319-16324 (Pubitemid 44715194)
48. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17:126-140 (Pubitemid 36062514)
49. Yuan H, Corbi N, Basilico C, Dailey L. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 1995; 9:2635-2645
50. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, et al. Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 2005; 280:24731-24737 (Pubitemid 40934562)
51. Liang J, Wan M, Zhang Y, Gu P, Xin H, Jung SY, et al. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat Cell Biol 2008; 10:731-739
52. Chawengsaksophak K, de Graaff W, Rossant J, Deschamps J, Beck F. Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci USA 2004; 101:7641-7645 (Pubitemid 38658082)
53. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, et al. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005; 132:2093-2102 (Pubitemid 40744469)
54. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, et al. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 2000; 404:95-99 (Pubitemid 30143140)
55. Yagi R, Kohn MJ, Karavanova I, Kaneko KJ, Vullhorst D, DePamphilis ML, et al. Transcription factor TEAD4 specifies the trophectoderm lineage at the beginning of mammalian development. Development 2007; 134:3827-3836 (Pubitemid 350187342)
56. Nishioka N, Yamamoto S, Kiyonari H, Sato H, Sawada A, Ota M, et al. Tead4 is required for specification of trophectoderm in pre-implantation mouse embryos. Mech Dev 2008; 125:270-283
57. Soudais C, Bielinska M, Heikinheimo M, MacArthur CA, Narita N, Saffitz JE, et al. Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 1995; 121:3877-3888
58. Cai KQ, Capo-Chichi CD, Rula ME, Yang DH, Xu XX. Dynamic GATA6 expression in primitive endoderm formation and maturation in early mouse embryogenesis. Dev Dyn 2008; 237:2820-2829
59. Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F, Ip HS, et al. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev 1998; 12:3579-3590 (Pubitemid 28553248)
60. Futaki S, Hayashi Y, Emoto T, Weber CN, Sekiguchi K. Sox7 plays crucial roles in parietal endoderm differentiation in F9 embryonal carcinoma cells through regulating Gata-4 and Gata-6 expression. Mol Cell Biol 2004; 24:10492-10503 (Pubitemid 39507885)
61. Zhang J, Tam WL, Tong GQ, Wu Q, Chan HY, Soh BS, et al. Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1. Nat Cell Biol 2006; 8:1114-1123 (Pubitemid 44473607)
62. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003; 113:643-655 (Pubitemid 36694189)
63. Ivanova N, Dobrin R, Lu R, Kotenko I, Levorse J, DeCoste C, et al. Dissecting selfrenewal in stem cells with RNA interference. Nature 2006; 442:533-538 (Pubitemid 44167907)
64. Chew JL, Loh YH, Zhang W, Chen X, Tam WL, Yeap LS, et al. Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 2005; 25:6031-6046 (Pubitemid 40946556)
65. Kopp JL, Ormsbee BD, Desler M, Rizzino A. Small increases in the level of Sox2 trigger the differentiation of mouse embryonic stem cells. Stem Cells 2008; 26:903-911
66. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006; 38:431-440
67. Lim CY, Tam WL, Zhang J, Ang HS, Jia H, Lipovich L, et al. Sall4 regulates distinct transcription circuitries in different blastocyst-derived stem cell lineages. Cell Stem Cell 2008; 3:543-554
68. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005; 123:917-929 (Pubitemid 41721036)
69. Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W, et al. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 2008.
70. Lu CW, Yabuuchi A, Chen L, Viswanathan S, Kim K, Daley GQ. Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat Genet 2008; 40:921-926
71. Kunath T, Saba-El-Leil MK, Almousailleakh M, Wray J, Meloche S, Smith A. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007; 134:2895-2902 (Pubitemid 47386902)
72. Corson LB, Yamanaka Y, Lai KM, Rossant J. Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 2003; 130:4527-4537 (Pubitemid 37279407)
73. Hemberger M, Cross JC. Genes governing placental development. Trends Endocrinol Metab 2001; 12:162-168 (Pubitemid 33713557)
74. Watson ED, Cross JC. Development of structures and transport functions in the mouse placenta. Physiology 2005; 20:180-193 (Pubitemid 40807056)
75. Yang W, Klaman LD, Chen B, Araki T, Harada H, Thomas SM, et al. An Shp2/SFK/Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev Cell 2006; 10:317-327 (Pubitemid 43300089)
76. He S, Pant D, Schiffmacher A, Meece A, Keefer CL. Lymphoid enhancer factor 1-mediated Wnt signaling promotes the initiation of trophoblast lineage differentiation in mouse embryonic stem cells. Stem Cells 2008; 26:842-849
77. Schenke-Layland K, Angelis E, Rhodes KE, Heydarkhan-Hagvall S, Mikkola HK, Maclellan WR. Collagen IV induces trophoectoderm differentiation of mouse embryonic stem cells. Stem Cells 2007; 25:1529-1538
78. Jorgensen HF, Giadrossi S, Casanova M, Endoh M, Koseki H, Brockdorff N, et al. Stem cells primed for action: polycomb repressive complexes restrain the expression of lineage-specific regulators in embryonic stem cells. Cell Cycle 2006; 5:1411-1414 (Pubitemid 44153649)
79. Hemberger M, Nozaki T, Winterhager E, Yamamoto H, Nakagama H, Kamada N, et al. Parp1-deficiency induces differentiation of ES cells into trophoblast derivatives. Dev Biol 2003; 257:371-381 (Pubitemid 36506851)
80. Loh YH, Zhang W, Chen X, George J, Ng HH. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev 2007; 21:2545-2557 (Pubitemid 47607666)
81. Beck F, Erler T, Russell A, James R. Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev Dyn 1995; 204:219-227
82. Ralston A, Rossant J. Cdx2 acts downstream of cell polarization to cell-autonomously promote trophectoderm fate in the early mouse embryo. Dev Biol 2008; 313:614-629
83. Hollenberg SM, Sternglanz R, Cheng PF, Weintraub H. Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol Cell Biol 1995; 15:3813-3822
84. Cserjesi P, Brown D, Lyons GE, Olson EN. Expression of the novel basic helix-loop-helix gene eHAND in neural crest derivatives and extraembryonic membranes during mouse development. Dev Biol 1995; 170:664-678
85. Cross JC, Flannery ML, Blanar MA, Steingrimsson E, Jenkins NA, Copeland NG, et al. Hxt encodes a basic helix-loop-helix transcription factor that regulates trophoblast cell development. Development 1995; 121:2513-2523
86. Wilda M, Bachner D, Zechner U, Kehrer-Sawatzki H, Vogel W, Hameister H. Do the constraints of human speciation cause expression of the same set of genes in brain, testis and placenta? Cytogenet Cell Genet 2000; 91:300-302 (Pubitemid 32110382)
87. Hemberger M. The role of the X chromosome in mammalian extra embryonic development. Cytogenet Genome Res 2002; 99:210-217 (Pubitemid 37467845)
88. Soares MJ, Konno T, Alam SM. The prolactin family: effectors of pregnancy-dependent adaptations. Trends Endocrinol Metab 2007; 18:114-121 (Pubitemid 46464021)
89. Finkenzeller D, Kromer B, Thompson J, Zimmermann W. cea5, a structurally divergent member of the murine carcinoembryonic antigen gene family, is exclusively expressed during early placental development in trophoblast giant cells. J Biol Chem 1997; 272:31369-31376 (Pubitemid 28013272)
90. Finkenzeller D, Fischer B, McLaughlin J, Schrewe H, Ledermann B, Zimmermann W. Trophoblast cell-specific carcinoembryonic antigen cell adhesion molecule 9 is not required for placental development or a positive outcome of allotypic pregnancies. Mol Cell Biol 2000; 20:7140-7145
91. Wynne F, Ball M, McLellan AS, Dockery P, Zimmermann W, Moore T. Mouse pregnancy-specific glycoproteins: tissue-specific expression and evidence of association with maternal vasculature. Reproduction 2006; 131:721-732
92. Rawn SM, Cross JC. The evolution, regulation and function of placenta-specific genes. Annu Rev Cell Dev Biol 2008; 24:159-181
93. Deussing J, Kouadio M, Rehman S, Werber I, Schwinde A, Peters C. Identification and characterization of a dense cluster of placenta-specific cysteine peptidase genes and related genes on mouse chromosome 13. Genomics 2002; 79:225-240
94. Screen M, Dean W, Cross JC, Hemberger M. Cathepsin proteases have distinct roles in trophoblast function and vascular remodelling. Development 2008; 135:3311-3320
95. Simmons DG, Rawn S, Davies A, Hughes M, Cross JC. Spatial and temporal expression of the 23 murine Prolactin/Placental Lactogen-related genes is not associated with their position in the locus. BMC Genomics 2008; 9:352.
96. Lescisin KR, Varmuza S, Rossant J. Isolation and characterization of a novel trophoblast-specific cDNA in the mouse. Genes Dev 1988; 2:1639-1646
97. Simmons DG, Natale DR, Begay V, Hughes M, Leutz A, Cross JC. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 2008; 135:2083-2091
98. Soares MJ. The prolactin and growth hormone families: pregnancy-specific hormones/cytokines at the maternal-fetal interface. Reprod Biol Endocrinol 2004; 2:51. (Pubitemid 39130528)
99. Liu Y, Labosky PA. Regulation of embryonic stem cell self-renewal and pluripotency by Foxd3. Stem Cells 2008; 26:2475-2484
100. Parisi S, Passaro F, Aloia L, Manabe I, Nagai R, Pastore L, et al. Klf5 is involved in self-renewal of mouse embryonic stem cells. J Cell Sci 2008; 121:2629-2634
101. Ema M, Mori D, Niwa H, Hasegawa Y, Yamanaka Y, Hitoshi S, et al. Kruppel-like factor 5 is essential for blastocyst development and the normal self-renewal of mouse ESCs. Cell Stem Cell 2008; 3:555-567
102. Kaji K, Caballero IM, MacLeod R, Nichols J, Wilson VA, Hendrich B. The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 2006; 8:285-292 (Pubitemid 43336071)
103. Kaji K, Nichols J, Hendrich B. Mbd3, a component of the NuRD co-repressor complex, is required for development of pluripotent cells. Development 2007; 134:1123-1132 (Pubitemid 46630080)
104. Thomas PQ, Brown A, Beddington RS. Hex: a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors. Development 1998; 125:85-94. (Pubitemid 28048456)
105. Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, Li MZ, et al. Dicer is essential for mouse development. Nat Genet 2003; 35:215-217 (Pubitemid 37363172)
106. Dietrich JE, Hiiragi T. Stochastic patterning in the mouse pre-implantation embryo. Development 2007; 134:4219-4231
107. Downs KM. Systematic localization of Oct-3/4 to the gastrulating mouse conceptus suggests manifold roles in mammalian development. Dev Dyn 2008; 237:464-475
108. Hart AH, Hartley L, Ibrahim M, Robb L. Identification, cloning and expression analysis of the pluripotency promoting Nanog genes in mouse and human. Dev Dyn 2004; 230:187-198 (Pubitemid 38544086)
109. Tam WL, Lim CY, Han J, Zhang J, Ang YS, Ng HH, et al. T-cell factor 3 regulates embryonic stem cell pluripotency and self-renewal by the transcriptional control of multiple lineage pathways. Stem Cells 2008; 26:2019-2031
110. Yamaguchi S, Kimura H, Tada M, Nakatsuji N, Tada T. Nanog expression in mouse germ cell development. Gene Expr Patterns 2005; 5:639-646 (Pubitemid 40796609)
111. Guo G, Robson P. Transcription factor dynamics in the preimplantation embryo. MGI Direct Data Submission 2008; (www.informatics.jax.org).
112. Lickert H, Cox B, Wehrle C, Taketo MM, Kemler R, Rossant J. Dissecting Wnt/beta-catenin signaling during gastrulation using RNA interference in mouse embryos. Development 2005; 132:2599-2609 (Pubitemid 40883258)
113. Wood HB, Episkopou V. Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 1999; 86:197-201.
114. Yoshikawa T, Piao Y, Zhong J, Matoba R, Carter MG, Wang Y, et al. High-throughput screen for genes predominantly expressed in the ICM of mouse blastocysts by whole mount in situ hybridization. Gene Expr Patterns 2006; 6:213-224 (Pubitemid 43071918)
115. Sakaki-Yumoto M, Kobayashi C, Sato A, Fujimura S, Matsumoto Y, Takasato M, et al. The murine homolog of SALL4, a causative gene in Okihiro syndrome, is essential for embryonic stem cell proliferation, and cooperates with Sall1 in anorectal, heart, brain and kidney development. Development 2006; 133:3005-3013 (Pubitemid 44314277)
116. Kohlhase J, Heinrich M, Liebers M, Frohlich Archangelo L, Reardon W, Kispert A. Cloning and expression analysis of SALL4, the murine homologue of the gene mutated in Okihiro syndrome. Cytogenet Genome Res 2002; 98:274-277 (Pubitemid 37499859)
117. Adams IR, McLaren A. Identification and characterisation of mRif1: a mouse telomere-associated protein highly expressed in germ cells and embryo-derived pluripotent stem cells. Dev Dyn 2004; 229:733-744 (Pubitemid 38429102)
118. Hanna LA, Foreman RK, Tarasenko IA, Kessler DS, Labosky PA. Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev 2002; 16:2650-2661
119. Labosky PA, Kaestner KH. The winged helix transcription factor Hfh2 is expressed in neural crest and spinal cord during mouse development. Mech Dev 1998; 76:185-190 (Pubitemid 28467918)
120. Tompers DM, Foreman RK, Wang Q, Kumanova M, Labosky PA. Foxd3 is required in the trophoblast progenitor cell lineage of the mouse embryo. Dev Biol 2005; 285:126-137 (Pubitemid 41242820)
121. Jacquemin P, Hwang JJ, Martial JA, Dolle P, Davidson I. A novel family of developmentally regulated mammalian transcription factors containing the TEA/ATTS DNA binding domain. J Biol Chem 1996; 271:21775-21785 (Pubitemid 26303794)
122. Sawada A, Nishizaki Y, Sato H, Yada Y, Nakayama R, Yamamoto S, et al. Tead proteins activate the Foxa2 enhancer in the node in cooperation with a second factor. Development 2005; 132:4719-4729 (Pubitemid 41685282)
123. Hancock SN, Agulnik SI, Silver LM, Papaioannou VE. Mapping and expression analysis of the mouse ortholog of Xenopus Eomesodermin. Mech Dev 1999; 81:205-208 (Pubitemid 29183062)
124. Ciruna BG, Rossant J. Expression of the T-box gene Eomesodermin during early mouse development. Mech Dev 1999; 81:199-203. (Pubitemid 29183061)
125. Tremblay KD, Dunn NR, Robertson EJ. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 2001; 128:3609-3621 (Pubitemid 32962727)
126. Donnison M, Beaton A, Davey HW, Broadhurst R, Huillier P, Pfeffer PL. Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning. Development 2005; 132:2299-2308 (Pubitemid 40872800)
127. Luo J, Sladek R, Bader JA, Matthyssen A, Rossant J, Giguere V. Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature 1997; 388:778-782 (Pubitemid 27375157)
128. Pettersson K, Svensson K, Mattsson R, Carlsson B, Ohlsson R, Berkenstam A. Expression of a novel member of estrogen response element-binding nuclear receptors is restricted to the early stages of chorion formation during mouse embryogenesis. Mech Dev 1996; 54:211-223 (Pubitemid 26063338)
129. Guzman-Ayala M, Ben-Haim N, Beck S, Constam DB. Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment. Proc Natl Acad Sci USA 2004; 101:15656-15660 (Pubitemid 39473543)
130. Mitsunaga K, Araki K, Mizusaki H, Morohashi K, Haruna K, Nakagata N, et al. Loss of PGC-specific expression of the orphan nuclear receptor ERR-beta results in reduction of germ cell number in mouse embryos. Mech Dev 2004; 121:237-246 (Pubitemid 38293461)
131. Hamazaki T, Kehoe SM, Nakano T, Terada N. The Grb2/Mek pathway represses Nanog in murine embryonic stem cells. Mol Cell Biol 2006; 26:7539-7549 (Pubitemid 44547704)
132. Chazaud C, Yamanaka Y, Pawson T, Rossant J. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 2006; 10:615-624