Epiblast Ground State Is Controlled by Canonical Wnt/β-Catenin Signaling in the Postimplantation Mouse Embryo and Epiblast Stem Cells

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Sumi, Tomoyuki ^a   Oki, Shinya ^a   Kitajima, Keiko ^a   Meno, Chikara ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CELL TRANSPLANTATION; CONTROLLED STUDY; ECTODERM; EMBRYO; GENE EXPRESSION; MESODERM; MOUSE; NIDATION; NONHUMAN; PRIMORDIAL GERM CELL; SIGNAL TRANSDUCTION; STEM CELL;

AMIDES; ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; EMBRYO IMPLANTATION; EMBRYONIC STEM CELLS; GENE DELETION; GERM LAYERS; MESODERM; MICE; PLURIPOTENT STEM CELLS; PYRIDINES; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; WNT PROTEINS;

EID: 84877779850     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063378     Document Type: Article

References (54)

1. Clevers H, (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
2. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, et al. (1996) Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382: 638-642.
3. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, et al. (1999) Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22: 361-365.
4. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, et al. (2000) Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol 148: 567-578.
5. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, et al. (2008) The ground state of embryonic stem cell self-renewal. Nature 453: 519-523.
6. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH, (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10: 55-63.
7. Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, et al. (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448: 191-195.
8. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, et al. (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448: 196-199.
9. Ohtsuka S, Nishikawa-Torikai S, Niwa H, (2012) E-cadherin promotes incorporation of mouse epiblast stem cells into normal development. PLoS One 7: e45220.
10. Bernemann C, Greber B, Ko K, Sterneckert J, Han DW, et al. (2011) Distinct developmental ground states of epiblast stem cell lines determine different pluripotency features. Stem Cells 29: 1496-1503.
11. Han DW, Tapia N, Joo JY, Greber B, Arauzo-Bravo MJ, et al. (2010) Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages. Cell 143: 617-627.
12. Blauwkamp TA, Nigam S, Ardehali R, Weissman IL, Nusse R, (2012) Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat Commun 3: 1070.
13. Davidson KC, Adams AM, Goodson JM, McDonald CE, Potter JC, et al. (2012) Wnt/beta-catenin signaling promotes differentiation, not self-renewal, of human embryonic stem cells and is repressed by Oct4. Proc Natl Acad Sci U S A 109: 4485-4490.
14. Sumi T, Tsuneyoshi N, Nakatsuji N, Suemori H, (2008) Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 135: 2969-2979.
15. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, et al. (2001) Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128: 1253-1264.
16. Chenoweth JG, Tesar PJ, (2010) Isolation and maintenance of mouse epiblast stem cells. Methods Mol Biol 636: 25-44.
17. Lawson KA, Meneses JJ, Pedersen RA, (1991) Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113: 891-911.
18. Oki S, Kitajima K, Meno C, (2010) Dissecting the role of Fgf signaling during gastrulation and left-right axis formation in mouse embryos using chemical inhibitors. Dev Dyn 239: 1768-1778.
19. Ring DB, Johnson KW, Henriksen EJ, Nuss JM, Goff D, et al. (2003) Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52: 588-595.
20. Pfister S, Steiner KA, Tam PP, (2007) Gene expression pattern and progression of embryogenesis in the immediate post-implantation period of mouse development. Gene Expr Patterns 7: 558-573.
21. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, et al. (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461: 614-620.
22. Arnold SJ, Robertson EJ, (2009) Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10: 91-103.
23. Vallier L, Mendjan S, Brown S, Chng Z, Teo A, et al. (2009) Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 136: 1339-1349.
24. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, et al. (2007) A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25: 681-686.
25. Snow MHL, (1977) Gastrulation in the mouse: Growth and regionalization of the epiblast. J Embryol Exp Morphol 42: 293-303.
26. Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, et al. (1995) Lack of beta-catenin affects mouse development at gastrulation. Development 121: 3529-3537.
27. Morkel M, Huelsken J, Wakamiya M, Ding J, van de Wetering M, et al. (2003) Beta-catenin regulates Cripto- and Wnt3-dependent gene expression programs in mouse axis and mesoderm formation. Development 130: 6283-6294.
28. Greber B, Coulon P, Zhang M, Moritz S, Frank S, et al. (2011) FGF signalling inhibits neural induction in human embryonic stem cells. EMBO J 30: 4874-4884.
29. Yoo YD, Huang CT, Zhang X, Lavaute TM, Zhang SC, (2011) Fibroblast growth factor regulates human neuroectoderm specification through ERK1/2-PARP-1 pathway. Stem Cells 29: 1975-1982.
30. Lyashenko N, Winter M, Migliorini D, Biechele T, Moon RT, et al. (2011) Differential requirement for the dual functions of beta-catenin in embryonic stem cell self-renewal and germ layer formation. Nat Cell Biol 13: 753-761.
31. Otero JJ, Fu W, Kan L, Cuadra AE, Kessler JA, (2004) Beta-catenin signaling is required for neural differentiation of embryonic stem cells. Development 131: 3545-3557.
32. Tam PP, Parameswaran M, Kinder SJ, Weinberger RP, (1997) The allocation of epiblast cells to the embryonic heart and other mesodermal lineages: the role of ingression and tissue movement during gastrulation. Development 124: 1631-1642.
33. Tam PP, Zhou SX, (1996) The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev Biol 178: 124-132.
34. Ginsburg M, Snow MH, McLaren A, (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110: 521-528.
35. Tsang TE, Khoo PL, Jamieson RV, Zhou SX, Ang SL, et al. (2001) The allocation and differentiation of mouse primordial germ cells. Int J Dev Biol 45: 549-555.
36. Kim K, Zhao R, Doi A, Ng K, Unternaehrer J, et al. (2011) Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat Biotechnol 29: 1117-1119.
37. Wray J, Kalkan T, Gomez-Lopez S, Eckardt D, Cook A, et al. (2011) Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat Cell Biol 13: 838-845.
38. Nichols J, Smith A, (2009) Naive and primed pluripotent states. Cell Stem Cell 4: 487-492.
39. 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: 746-755.
40. Pereira L, Yi F, Merrill BJ, (2006) Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol Cell Biol 26: 7479-7491.
41. 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: 477-490.
42. Martello G, Sugimoto T, Diamanti E, Joshi A, Hannah R, et al. (2012) Esrrb is a pivotal target of the gsk3/tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 11: 491-504.
43. Mesnard D, Guzman-Ayala M, Constam DB, (2006) Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 133: 2497-2505.
44. Greber B, Wu G, Bernemann C, Joo JY, Han DW, et al. (2010) Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 6: 215-226.
45. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, et al. (2007) Nanog safeguards pluripotency and mediates germline development. Nature 450: 1230-1234.
46. Osorno R, Tsakiridis A, Wong F, Cambray N, Economou C, et al. (2012) The developmental dismantling of pluripotency is reversed by ectopic Oct4 expression. Development 139: 2288-2298.
47. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, et al. (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17: 126-140.
48. Hanna LA, Foreman RK, Tarasenko IA, Kessler DS, Labosky PA, (2002) Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev 16: 2650-2661.
49. Dottori M, Gross MK, Labosky P, Goulding M, (2001) The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 128: 4127-4138.
50. Pevny L, Placzek M, (2005) SOX genes and neural progenitor identity. Curr Opin Neurobiol 15: 7-13.
51. Lickert H, Cox B, Wehrle C, Taketo MM, Kemler R, et al. (2005) Dissecting Wnt/beta-catenin signaling during gastrulation using RNA interference in mouse embryos. Development 132: 2599-2609.
52. Teo AK, Arnold SJ, Trotter MW, Brown S, Ang LT, et al. (2011) Pluripotency factors regulate definitive endoderm specification through eomesodermin. Genes Dev 25: 238-250.
53. Thomson M, Liu SJ, Zou LN, Smith Z, Meissner A, et al. (2011) Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 145: 875-889.
54. Hong SH, Rampalli S, Lee JB, McNicol J, Collins T, et al. (2011) Cell fate potential of human pluripotent stem cells is encoded by histone modifications. Cell Stem Cell 9: 24-36.