Pluripotency factors in embryonic stem cells regulate differentiation into germ layers

Cell

Volumn 145, Issue 6, 2011, Pages 875-889

  Thomson, Matt ^a,b,c   Liu, Siyuan John ^a,b   Zou, Ling Nan ^a,c   Smith, Zack ^d   Meissner, Alexander ^c,d   Ramanathan, Sharad ^a,b,c,e  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d Harvard University   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; EMBRYONIC STEM CELL; GENE EXPRESSION; GERM LAYER; IN VITRO STUDY; MESODERM; MOUSE; NEUROECTODERM; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

EID: 79958263080     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.05.017     Document Type: Article

References (77)

1. E. Abranches, M. Silva, L. Pradier, H. Schulz, O. Hummel, D. Henrique, and E. Bekman Neural differentiation of embryonic stem cells in vitro: a road map to neurogenesis in the embryo PLoS ONE 4 2009 e6286
2. D.J. Anderson Stem cells and pattern formation in the nervous system: the possible versus the actual Neuron 30 2001 19 35 (Pubitemid 32441674)
3. J. Briscoe, A. Pierani, T.M. Jessell, and J. Ericson A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube Cell 101 2000 435 445
4. A.B. Cantor, and S.H. Orkin Hematopoietic development: a balancing act Curr. Opin. Genet. Dev. 11 2001 513 519 (Pubitemid 32800724)
5. X. Chen, H. Xu, P. Yuan, F. Fang, M. Huss, V.B. Vega, E. Wong, Y.L. Orlov, W. Zhang, and J. Jiang Integration of external signaling pathways with the core transcriptional network in embryonic stem cells Cell 133 2008 1106 1117 (Pubitemid 351787745)
6. J.L. Chew, Y.H. Loh, W. Zhang, X. Chen, W.L. Tam, L.S. Yeap, P. Li, Y.S. Ang, B. Lim, P. Robson, and H.H. Ng Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells Mol. Cell. Biol. 25 2005 6031 6046 (Pubitemid 40946556)
7. E.H. Davidson, J.P. Rast, P. Oliveri, A. Ransick, C. Calestani, C.H. Yuh, T. Minokawa, G. Amore, V. Hinman, and C. Arenas-Mena A genomic regulatory network for development Science 295 2002 1669 1678 (Pubitemid 34202895)
8. M. Ema, D. Mori, H. Niwa, Y. Hasegawa, Y. Yamanaka, S. Hitoshi, J. Mimura, Y. Kawabe, T. Hosoya, and M. Morita Krüppel-like factor 5 is essential for blastocyst development and the normal self-renewal of mouse ESCs Cell Stem Cell 3 2008 555 567
9. B. Greber, G. Wu, C. Bernemann, J.Y. Joo, D.W. Han, K. Ko, N. Tapia, D. Sabour, J. Sterneckert, P. Tesar, and H.R. Schöler Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells Cell Stem Cell 6 2010 215 226
10. J. Han, P. Yuan, H. Yang, J. Zhang, B.S. Soh, P. Li, S.L. Lim, S. Cao, J. Tay, and Y.L. Orlov Tbx3 improves the germ-line competency of induced pluripotent stem cells Nature 463 2010 1096 1100
11. G. Hu, J. Kim, Q. Xu, Y. Leng, S.H. Orkin, and S.J. Elledge A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal Genes Dev. 23 2009 837 848
12. N. Ivanova, R. Dobrin, R. Lu, I. Kotenko, J. Levorse, C. DeCoste, X. Schafer, Y. Lun, and I.R. Lemischka Dissecting self-renewal in stem cells with RNA interference Nature 442 2006 533 538 (Pubitemid 44167907)
13. S.A. Jackson, J. Schiesser, E.G. Stanley, and A.G. Elefanty Differentiating embryonic stem cells pass through 'temporal windows' that mark responsiveness to exogenous and paracrine mesendoderm inducing signals PLoS ONE 5 2010 e10706
14. J. Jiang, Y.S. Chan, Y.H. Loh, J. Cai, G.Q. Tong, C.A. Lim, P. Robson, S. Zhong, and H.H. Ng A core Klf circuitry regulates self-renewal of embryonic stem cells Nat. Cell Biol. 10 2008 353 360 (Pubitemid 351331023)
15. J.B. Kim, H. Zaehres, G. Wu, L. Gentile, K. Ko, V. Sebastiano, M.J. Araúzo-Bravo, D. Ruau, D.W. Han, M. Zenke, and H.R. Schöler Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors Nature 454 2008 646 650
16. J.Y. Li, M.T. Pu, R. Hirasawa, B.Z. Li, Y.N. Huang, R. Zeng, N.H. Jing, T. Chen, E. Li, H. Sasaki, and G.L. Xu Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog Mol. Cell. Biol. 27 2007 8748 8759
17. R. Lu, F. Markowetz, R.D. Unwin, J.T. Leek, E.M. Airoldi, B.D. MacArthur, A. Lachmann, R. Rozov, A. Ma'ayan, and L.A. Boyer Systems-level dynamic analyses of fate change in murine embryonic stem cells Nature 462 2009 358 362
18. A. Marson, S.S. Levine, M.F. Cole, G.M. Frampton, T. Brambrink, S. Johnstone, M.G. Guenther, W.K. Johnston, M. Wernig, and J. Newman Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells Cell 134 2008 521 533
19. S. Masui, Y. Nakatake, Y. Toyooka, D. Shimosato, R. Yagi, K. Takahashi, H. Okochi, A. Okuda, R. Matoba, and A.A. Sharov Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells Nat. Cell Biol. 9 2007 625 635 (Pubitemid 47214724)
20. S. Masui, S. Ohtsuka, R. Yagi, K. Takahashi, M.S. Ko, and H. Niwa Rex1/Zfp42 is dispensable for pluripotency in mouse ES cells BMC Dev. Biol. 8 2008 45
21. T.S. Mikkelsen, M. Ku, D.B. Jaffe, B. Issac, E. Lieberman, G. Giannoukos, P. Alvarez, W. Brockman, T.K. Kim, and R.P. Koche Genome-wide maps of chromatin state in pluripotent and lineage-committed cells Nature 448 2007 553 560 (Pubitemid 47206934)
22. K. Mitsui, Y. Tokuzawa, H. Itoh, K. Segawa, M. Murakami, K. Takahashi, M. Maruyama, M. Maeda, and S. Yamanaka The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells Cell 113 2003 631 642 (Pubitemid 36694188)
23. S. Miyagi, M. Nishimoto, T. Saito, M. Ninomiya, K. Sawamoto, H. Okano, M. Muramatsu, H. Oguro, A. Iwama, and A. Okuda The Sox2 regulatory region 2 functions as a neural stem cell-specific enhancer in the telencephalon J. Biol. Chem. 281 2006 13374 13381 (Pubitemid 43855248)
24. S. Nishikawa, L.M. Jakt, and T. Era Embryonic stem-cell culture as a tool for developmental cell biology Nat. Rev. Mol. Cell Biol. 8 2007 502 507 (Pubitemid 46809158)
25. H. Niwa How is pluripotency determined and maintained? Development 134 2007 635 646 (Pubitemid 46437906)
26. H. Niwa Mouse ES cell culture system as a model of development Dev. Growth Differ. 52 2010 275 283
27. H. Niwa, J. Miyazaki, and A.G. Smith Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells Nat. Genet. 24 2000 372 376 (Pubitemid 30187435)
28. N. Novershtern, A. Subramanian, L.N. Lawton, R.H. Mak, W.N. Haining, M.E. McConkey, N. Habib, N. Yosef, C.Y. Chang, and T. Shay Densely interconnected transcriptional circuits control cell states in human hematopoiesis Cell 144 2011 296 309
29. D.T. Odom, N. Zizlsperger, D.B. Gordon, G.W. Bell, N.J. Rinaldi, H.L. Murray, T.L. Volkert, J. Schreiber, P.A. Rolfe, and D.K. Gifford Control of pancreas and liver gene expression by HNF transcription factors Science 303 2004 1378 1381 (Pubitemid 38269432)
30. D. Pasini, P.A. Cloos, J. Walfridsson, L. Olsson, J.P. Bukowski, J.V. Johansen, M. Bak, N. Tommerup, J. Rappsilber, and K. Helin JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells Nature 464 2010 306 310
31. J.C. Peng, A. Valouev, T. Swigut, J. Zhang, Y. Zhao, A. Sidow, and J. Wysocka Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells Cell 139 2009 1290 1302
32. K. Sachs, O. Perez, D. Pe'er, D.A. Lauffenburger, and G.P. Nolan Causal protein-signaling networks derived from multiparameter single-cell data Science 308 2005 523 529 (Pubitemid 40570578)
33. N. Sato, L. Meijer, L. Skaltsounis, P. Greengard, and A.H. Brivanlou 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 2004 55 63 (Pubitemid 38524699)
34. B. Schuettengruber, and G. Cavalli Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice Development 136 2009 3531 3542
35. X. Shen, Y. Liu, Y.J. Hsu, Y. Fujiwara, J. Kim, X. Mao, G.C. Yuan, and S.H. Orkin EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency Mol. Cell 32 2008 491 502
36. M. Sikorska, J.K. Sandhu, P. Deb-Rinker, A. Jezierski, J. Leblanc, C. Charlebois, M. Ribecco-Lutkiewicz, M. Bani-Yaghoub, and P.R. Walker Epigenetic modifications of SOX2 enhancers, SRR1 and SRR2, correlate with in vitro neural differentiation J. Neurosci. Res. 86 2008 1680 1693 (Pubitemid 351859420)
37. J. Silva, and A. Smith Capturing pluripotency Cell 132 2008 532 536 (Pubitemid 351253697)
38. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676 (Pubitemid 44233629)
39. D. ten Berge, S.A. Brugmann, J.A. Helms, and R. Nusse Wnt and FGF signals interact to coordinate growth with cell fate specification during limb development Development 135 2008 3247 3257
40. D. ten Berge, W. Koole, C. Fuerer, M. Fish, E. Eroglu, and R. Nusse Wnt signaling mediates self-organization and axis formation in embryoid bodies Cell Stem Cell 3 2008 508 518
41. P.J. Tesar, J.G. Chenoweth, F.A. Brook, T.J. Davies, E.P. Evans, D.L. Mack, R.L. Gardner, and R.D. McKay New cell lines from mouse epiblast share defining features with human embryonic stem cells Nature 448 2007 196 199 (Pubitemid 47067378)
42. M. Tomioka, M. Nishimoto, S. Miyagi, T. Katayanagi, N. Fukui, H. Niwa, M. Muramatsu, and A. Okuda Identification of Sox-2 regulatory region which is under the control of Oct-3/4-Sox-2 complex Nucleic Acids Res. 30 2002 3202 3213 (Pubitemid 34846184)
43. T. Vierbuchen, A. Ostermeier, Z.P. Pang, Y. Kokubu, T.C. Südhof, and M. Wernig Direct conversion of fibroblasts to functional neurons by defined factors Nature 463 2010 1035 1041
44. J. Wang, S. Rao, J. Chu, X. Shen, D.N. Levasseur, T.W. Theunissen, and S.H. Orkin A protein interaction network for pluripotency of embryonic stem cells Nature 444 2006 364 368 (Pubitemid 44764111)
45. T.P. Yamaguchi, S. Takada, Y. Yoshikawa, N. Wu, and A.P. McMahon T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification Genes Dev. 13 1999 3185 3190 (Pubitemid 30030440)
46. Q.L. Ying, and A.G. Smith Defined conditions for neural commitment and differentiation Methods Enzymol. 365 2003 327 341 (Pubitemid 37531558)
47. Q.L. Ying, J. Nichols, I. Chambers, and A. Smith BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3 Cell 115 2003 281 292 (Pubitemid 37487702)
48. Q.L. Ying, M. Stavridis, D. Griffiths, M. Li, and A. Smith Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture Nat. Biotechnol. 21 2003 183 186 (Pubitemid 36188218)
49. Q.L. Ying, J. Wray, J. Nichols, L. Batlle-Morera, B. Doble, J. Woodgett, P. Cohen, and A. Smith The ground state of embryonic stem cell self-renewal Nature 453 2008 519 523 (Pubitemid 351733324)
50. Ai, H.; Lvov, Y.M.; Mills, D.K.; Jennings, M.; Alexander, J.S. Jones, S.A. (2003). Coating and selective deposition of nanofilm on silicone rubber for cell adhesion and growth. Cell Biochem. Biophys. 38, 103-114. (Pubitemid 41270813)
51. Bintu, L.; Buchler, N.E.; Garcia, H.G.; Gerland, U.; Hwa, T.; Kondev, J. Phillips, R. (2005). Transcriptional regulation by the numbers: models. Curr. Opin. Genet. Dev. 15, 116-124. (Pubitemid 40410659)
52. Carey, M.; Lin, Y.S.; Green, M.R. Ptashne, M. (1990). A mechanism for synergistic activation of a mammalian gene by GAL4 derivatives. Nature 345, 361-364.
53. Chen, X.; Xu, H.; Yuan, P.; Fang, F.; Huss, M.; Vega, V.B.; Wong, E.; Orlov, Y.L.; Zhang, W.; Jiang, J.; et al. (2008). Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117. (Pubitemid 351787745)
54. Chew, J.L.; Loh, Y.H.; Zhang, W.; Chen, X.; Tam, W.L.; Yeap, L.S.; Li, P.; Ang, Y.S.; Lim, B.; Robson, P. Ng, H.H. (2005). Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol. Cell. Biol. 25, 6031-6046. (Pubitemid 40946556)
55. Elowitz, M.B. Leibler, S. (2000). A synthetic oscillatory network of transcriptional regulators. Nature 403, 335-338. (Pubitemid 30062393)
56. Franois, P.; Hakim, V. Siggia, E.D. (2007). Deriving structure from evolution: metazoan segmentation. Mol. Syst. Biol. 3, 154.
57. Gaspard, N.; Bouschet, T.; Hourez, R.; Dimidschstein, J.; Naeije, G.; van den Ameele, J.; Espuny-Camacho, I.; Herpoel, A.; Passante, L.; Schiffmann, S.N.; et al. (2008). An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351-357.
58. Greber, B.; Wu, G.; Bernemann, C.; Joo, J.Y.; Han, D.W.; Ko, K.; Tapia, N.; Sabour, D.; Sterneckert, J.; Tesar, P. Schöler, H.R. (2010). Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 6, 215-226.
59. Hu, G.; Kim, J.; Xu, Q.; Leng, Y.; Orkin, S.H. Elledge, S.J. (2009). A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Genes Dev. 23, 837-848.
60. Jackson, S.A.; Schiesser, J.; Stanley, E.G. Elefanty, A.G. (2010). Differentiating embryonic stem cells pass through 'temporal windows' that mark responsiveness to exogenous and paracrine mesendoderm inducing signals. PLoS ONE 5, e10706.
61. Lengner, C.J.; Camargo, F.D.; Hochedlinger, K.; Welstead, G.G.; Zaidi, S.; Gokhale, S.; Scholer, H.R.; Tomilin, A. Jaenisch, R. (2007). Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cell 1, 403-415. (Pubitemid 47506536)
62. Marson, A.; Levine, S.S.; Cole, M.F.; Frampton, G.M.; Brambrink, T.; Johnstone, S.; Guenther, M.G.; Johnston, W.K.; Wernig, M.; Newman, J.; et al. (2008). Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134, 521-533.
63. Mikkelsen, T.S.; Ku, M.; Jaffe, D.B.; Issac, B.; Lieberman, E.; Giannoukos, G.; Alvarez, P.; Brockman, W.; Kim, T.K.; Koche, R.P.; et al. (2007). Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560. (Pubitemid 47206934)
64. Minucci, S.; Botquin, V.; Yeom, Y.I.; Dey, A.; Sylvester, I.; Zand, D.J.; Ohbo, K.; Ozato, K. Scholer, H.R. (1996). Retinoic acid-mediated down-regulation of Oct3/4 coincides with the loss of promoter occupancy in vivo. EMBO J. 15, 888-899. (Pubitemid 26064294)
65. Mitsui, K.; Tokuzawa, Y.; Itoh, H.; Segawa, K.; Murakami, M.; Takahashi, K.; Maruyama, M.; Maeda, M. Yamanaka, S. (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642. (Pubitemid 36694188)
66. Pasini, D.; Cloos, P.A.; Walfridsson, J.; Olsson, L.; Bukowski, J.P.; Johansen, J.V.; Bak, M.; Tommerup, N.; Rappsilber, J. Helin, K. (2010). JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464, 306-310.
67. Rodda, D.J.; Chew, J.L.; Lim, L.H.; Loh, Y.H.; Wang, B.; Ng, H.H. Robson, P. (2005). Transcriptional regulation of nanog by OCT4 and SOX2. J. Biol. Chem. 280, 24731-24737. (Pubitemid 40934562)
68. Shen, X.; Liu, Y.; Hsu, Y.J.; Fujiwara, Y.; Kim, J.; Mao, X.; Yuan, G.C. Orkin, S.H. (2008). EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 32, 491-502.
69. Sterneckert, J.; Stehling, M.; Bernemann, C.; Araúzo-Bravo, M.J.; Greber, B.; Gentile, L.; Ortmeier, C.; Sinn, M.; Wu, G.; Ruau, D.; et al. (2010). Neural induction intermediates exhibit distinct roles of Fgf signaling. Stem Cells 28, 1772-1781.
70. ten Berge, D.; Koole, W.; Fuerer, C.; Fish, M.; Eroglu, E. Nusse, R. (2008). Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 3, 508-518.
71. Tesar, P.J.; Chenoweth, J.G.; Brook, F.A.; Davies, T.J.; Evans, E.P.; Mack, D.L.; Gardner, R.L. McKay, R.D. (2007). New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196-199. (Pubitemid 47067378)
72. Wang, J.; Rao, S.; Chu, J.; Shen, X.; Levasseur, D.N.; Theunissen, T.W. Orkin, S.H. (2006). A protein interaction network for pluripotency of embryonic stem cells. Nature 444, 364-368. (Pubitemid 44764111)
73. Wernig, M.; Meissner, A.; Foreman, R.; Brambrink, T.; Ku, M.; Hochedlinger, K.; Bernstein, B.E. Jaenisch, R. (2007). In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448, 318-324. (Pubitemid 47080337)
74. Ying, Q.L.; Nichols, J.; Chambers, I. Smith, A. (2003a). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292. (Pubitemid 37487702)
75. Ying, Q.L. Smith, A.G. (2003). Defined conditions for neural commitment and differentiation. Methods Enzymol. 365, 327-341. (Pubitemid 37531558)
76. Ying, Q.L.; Stavridis, M.; Griffiths, D.; Li, M. Smith, A. (2003b). Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21, 183-186. (Pubitemid 36188218)
77. Ying, Q.L.; Wray, J.; Nichols, J.; Batlle-Morera, L.; Doble, B.; Woodgett, J.; Cohen, P. Smith, A. (2008). The ground state of embryonic stem cell self-renewal. Nature 453, 519-523. (Pubitemid 351733324)