Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast

Cell Stem Cell

Volumn 13, Issue 6, 2013, Pages 663-675

  Chan, Yun Shen ^a   Göke, Jonathan ^a   Ng, Jia Hui ^a   Lu, Xinyi ^a   Gonzales, Kevin Andrew Uy ^a,b   Tan, Cheng Peow ^a   Tng, Wei Quan ^a,b   Hong, Zhong Zhi ^a   Lim, Yee Siang ^a   Ng, Huck Hui ^a,b,c  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3L; DPPA3 PROTEIN; E1A ASSOCIATED P300 PROTEIN; GLYCOPROTEIN GP 130; KRUPPEL LIKE FACTOR 4; KRUPPEL LIKE FACTOR 5; OCTAMER TRANSCRIPTION FACTOR 4; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR TBX3; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BLASTOCYST; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; DEVELOPMENTAL GENE; ECTODERM; EMBRYO DEVELOPMENT; EMBRYOID BODY; EMBRYONIC STEM CELL; ENHANCER REGION; EPIGENETICS; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETIC ANALYSIS; GENETIC ASSOCIATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; INNER CELL MASS; PLURIPOTENT STEM CELL; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; X CHROMOSOME INACTIVATION;

ANIMALS; BLASTOCYST; CELL LINE; CELL PROLIFERATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; GATA6 TRANSCRIPTION FACTOR; GENE REGULATORY NETWORKS; GERM LAYERS; HOMEODOMAIN PROTEINS; HUMANS; LEUKEMIA INHIBITORY FACTOR; MICE; MODELS, BIOLOGICAL; PLURIPOTENT STEM CELLS; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES; TRANSCRIPTOME;

EID: 84890079514     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2013.11.015     Document Type: Article

References (56)

1. M. Abe, K. Hasegawa, H. Wada, T. Morimoto, T. Yanazume, T. Kawamura, M. Hirai, Y. Furukawa, and T. Kita GATA-6 is involved in PPARgamma-mediated activation of differentiated phenotype in human vascular smooth muscle cells Arterioscler. Thromb. Vasc. Biol. 23 2003 404 410
2. S. Anders, and W. Huber Differential expression analysis for sequence count data Genome Biol. 11 2010 R106
3. S. Bao, F. Tang, X. Li, K. Hayashi, A. Gillich, K. Lao, and M.A. Surani Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells Nature 461 2009 1292 1295
4. L.A. Boyer, T.I. Lee, M.F. Cole, S.E. Johnstone, S.S. Levine, J.P. Zucker, M.G. Guenther, R.M. Kumar, H.L. Murray, and R.G. Jenner Core transcriptional regulatory circuitry in human embryonic stem cells Cell 122 2005 947 956
5. I.G. Brons, L.E. Smithers, M.W. Trotter, P. Rugg-Gunn, B. Sun, S.M. Chuva de Sousa Lopes, S.K. Howlett, A. Clarkson, L. Ahrlund-Richter, R.A. Pedersen, and L. Vallier Derivation of pluripotent epiblast stem cells from mammalian embryos Nature 448 2007 191 195
6. C. Buecker, H.H. Chen, J.M. Polo, L. Daheron, L. Bu, T.S. Barakat, P. Okwieka, A. Porter, J. Gribnau, K. Hochedlinger, and N. Geijsen A murine ESC-like state facilitates transgenesis and homologous recombination in human pluripotent stem cells Cell Stem Cell 6 2010 535 546
7. I. Chambers, D. Colby, M. Robertson, J. Nichols, S. Lee, S. Tweedie, and A. Smith Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells Cell 113 2003 643 655
8. E.M. Chan, S. Ratanasirintrawoot, I.H. Park, P.D. Manos, Y.H. Loh, H. Huo, J.D. Miller, O. Hartung, J. Rho, and T.A. Ince Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells Nat. Biotechnol. 27 2009 1033 1037
9. 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
10. L. Dahéron, S.L. Opitz, H. Zaehres, M.W. Lensch, P.W. Andrews, J. Itskovitz-Eldor, and G.Q. Daley LIF/STAT3 signaling fails to maintain self-renewal of human embryonic stem cells Stem Cells 22 2004 770 778
11. D.V. Do, J. Ueda, D.M. Messerschmidt, C. Lorthongpanich, Y. Zhou, B. Feng, G. Guo, P.J. Lin, M.Z. Hossain, and W. Zhang A genetic and developmental pathway from STAT3 to the OCT4-NANOG circuit is essential for maintenance of ICM lineages in vivo Genes Dev. 27 2013 1378 1390
12. G.F. Dunglison, D.H. Barlow, and I.L. Sargent Leukaemia inhibitory factor significantly enhances the blastocyst formation rates of human embryos cultured in serum-free medium Hum. Reprod. 11 1996 191 196
13. M.J. Evans, and M.H. Kaufman Establishment in culture of pluripotential cells from mouse embryos Nature 292 1981 154 156
14. M.K. Furue, J. Na, J.P. Jackson, T. Okamoto, M. Jones, D. Baker, R. Hata, H.D. Moore, J.D. Sato, and P.W. Andrews Heparin promotes the growth of human embryonic stem cells in a defined serum-free medium Proc. Natl. Acad. Sci. USA 105 2008 13409 13414
15. O. Gafni, L. Weinberger, A.A. Mansour, Y.S. Manor, E. Chomsky, D. Ben-Yosef, Y. Kalma, S. Viukov, I. Maza, and A. Zviran Derivation of novel human ground state naive pluripotent stem cells Nature 2013 10.1038/nature12745 Published online October 30, 2013
16. J. Göke, Y.-S. Chan, J. Yan, M. Vingron, and H.-H. Ng Genome-wide kinase-chromatin interactions reveal the regulatory network of ERK signaling in human embryonic stem cells Mol. Cell 50 2013 844 855
17. G. Guo, and A. Smith A genome-wide screen in EpiSCs identifies Nr5a nuclear receptors as potent inducers of ground state pluripotency Development 137 2010 3185 3192
18. G. Guo, J. Yang, J. Nichols, J.S. Hall, I. Eyres, W. Mansfield, and A. Smith Klf4 reverts developmentally programmed restriction of ground state pluripotency Development 136 2009 1063 1069
19. G. Guo, M. Huss, G.Q. Tong, C. Wang, L. Li Sun, N.D. Clarke, and P. Robson Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst Dev. Cell 18 2010 675 685
20. J. Hanna, A.W. Cheng, K. Saha, J. Kim, C.J. Lengner, F. Soldner, J.P. Cassady, J. Muffat, B.W. Carey, and R. Jaenisch Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs Proc. Natl. Acad. Sci. USA 107 2010 9222 9227
21. R.K. Humphrey, G.M. Beattie, A.D. Lopez, N. Bucay, C.C. King, M.T. Firpo, S. Rose-John, and A. Hayek Maintenance of pluripotency in human embryonic stem cells is STAT3 independent Stem Cells 22 2004 522 530
22. N.Y. Ip, S.H. Nye, T.G. Boulton, S. Davis, T. Taga, Y. Li, S.J. Birren, K. Yasukawa, T. Kishimoto, and D.J. Anderson CNTF and LIF act on neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component gp130 Cell 69 1992 1121 1132
23. V. Karwacki-Neisius, J. Göke, R. Osorno, F. Halbritter, J.H. Ng, A.Y. Weiße, F.C. Wong, A. Gagliardi, N.P. Mullin, and N. Festuccia Reduced Oct4 expression directs a robust pluripotent state with distinct signaling activity and increased enhancer occupancy by Oct4 and Nanog Cell Stem Cell 12 2013 531 545
24. S.J. Kimber, S.F. Sneddon, D.J. Bloor, A.M. El-Bareg, J.A. Hawkhead, A.D. Metcalfe, F.D. Houghton, H.J. Leese, A. Rutherford, B.A. Lieberman, and D.R. Brison Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors Reproduction 135 2008 635 647
25. E.W. Kuijk, L.T. van Tol, H. Van de Velde, R. Wubbolts, M. Welling, N. Geijsen, and B.A. Roelen 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 2012 871 882
26. B. Langmead, C. Trapnell, M. Pop, and S.L. Salzberg Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol. 10 2009 R25
27. W. Li, W. Wei, S. Zhu, J. Zhu, Y. Shi, T. Lin, E. Hao, A. Hayek, H. Deng, and S. Ding Generation of rat and human induced pluripotent stem cells by combining genetic reprogramming and chemical inhibitors Cell Stem Cell 4 2009 16 19
28. W. Li, K. Li, W. Wei, and S. Ding Chemical approaches to stem cell biology and therapeutics Cell Stem Cell 13 2013 270 283
29. J. Lu, R. Hou, C.J. Booth, S.H. Yang, and M. Snyder Defined culture conditions of human embryonic stem cells Proc. Natl. Acad. Sci. USA 103 2006 5688 5693
30. T.E. Ludwig, M.E. Levenstein, J.M. Jones, W.T. Berggren, E.R. Mitchen, J.L. Frane, L.J. Crandall, C.A. Daigh, K.R. Conard, and M.S. Piekarczyk Derivation of human embryonic stem cells in defined conditions Nat. Biotechnol. 24 2006 185 187
31. G.R. Martin Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells Proc. Natl. Acad. Sci. USA 78 1981 7634 7638
32. N. Montserrat, E. Nivet, I. Sancho-Martinez, T. Hishida, S. Kumar, L. Miquel, C. Cortina, Y. Hishida, Y. Xia, C.R. Esteban, and J.C. Izpisua Belmonte Reprogramming of human fibroblasts to pluripotency with lineage specifiers Cell Stem Cell 13 2013 341 350
33. F. Neri, A. Krepelova, D. Incarnato, M. Maldotti, C. Parlato, F. Galvagni, F. Matarese, H.G. Stunnenberg, and S. Oliviero Dnmt3L antagonizes DNA methylation at bivalent promoters and favors DNA methylation at gene bodies in ESCs Cell 155 2013 121 134
34. J. Nichols, and A. Smith Pluripotency in the embryo and in culture Cold Spring Harb. Perspect. Biol. 4 2012 a008128
35. H. Niwa, T. Burdon, I. Chambers, and A. Smith Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3 Genes Dev. 12 1998 2048 2060
36. B. Plusa, A. Piliszek, S. Frankenberg, J. Artus, and A.K. Hadjantonakis Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst Development 135 2008 3081 3091
37. R.A. Reijo Pera, C. DeJonge, N. Bossert, M. Yao, J.Y. Hwa Yang, N.B. Asadi, W. Wong, C. Wong, and M.T. Firpo Gene expression profiles of human inner cell mass cells and embryonic stem cells Differentiation 78 2009 18 23
38. M. Roode, K. Blair, P. Snell, K. Elder, S. Marchant, A. Smith, and J. Nichols Human hypoblast formation is not dependent on FGF signalling Dev. Biol. 361 2012 358 363
39. J. Shu, C. Wu, Y. Wu, Z. Li, S. Shao, W. Zhao, X. Tang, H. Yang, L. Shen, and X. Zuo Induction of pluripotency in mouse somatic cells with lineage specifiers Cell 153 2013 963 975
40. J. Silva, J. Nichols, T.W. Theunissen, G. Guo, A.L. van Oosten, O. Barrandon, J. Wray, S. Yamanaka, I. Chambers, and A. Smith Nanog is the gateway to the pluripotent ground state Cell 138 2009 722 737
41. A.M. Singh, D. Reynolds, T. Cliff, S. Ohtsuka, A.L. Mattheyses, Y. Sun, L. Menendez, M. Kulik, and S. Dalton Signaling network crosstalk in human pluripotent cells: a Smad2/3-regulated switch that controls the balance between self-renewal and differentiation Cell Stem Cell 10 2012 312 326
42. G.K. Smyth limma: Linear Models for Microarray Data R. Gentleman, V. Carey, W. Huber, R. Irizarry, S. Dudoit, Bioinformatics and Computational Biology Solutions Using R and Bioconductor 2005 Springer New York 397 420
43. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. USA 102 2005 15545 15550
44. 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
45. J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, and J.M. Jones Embryonic stem cell lines derived from human blastocysts Science 282 1998 1145 1147
46. C. Trapnell, L. Pachter, and S.L. Salzberg TopHat: discovering splice junctions with RNA-Seq Bioinformatics 25 2009 1105 1111
47. C. Trapnell, D.G. Hendrickson, M. Sauvageau, L. Goff, J.L. Rinn, and L. Pachter Differential analysis of gene regulation at transcript resolution with RNA-seq Nat. Biotechnol. 31 2013 46 53
48. L. Vallier, M. Alexander, and R.A. Pedersen Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells J. Cell Sci. 118 2005 4495 4509
49. R. Vassena, S. Boué, E. González-Roca, B. Aran, H. Auer, A. Veiga, and J.C. Izpisua Belmonte Waves of early transcriptional activation and pluripotency program initiation during human preimplantation development Development 138 2011 3699 3709
50. W. Wang, J. Yang, H. Liu, D. Lu, X. Chen, Z. Zenonos, L.S. Campos, R. Rad, G. Guo, and S. Zhang Rapid and efficient reprogramming of somatic cells to induced pluripotent stem cells by retinoic acid receptor gamma and liver receptor homolog 1 Proc. Natl. Acad. Sci. USA 108 2011 18283 18288
51. L. Yan, M. Yang, H. Guo, L. Yang, J. Wu, R. Li, P. Liu, Y. Lian, X. Zheng, and J. Yan Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells Nat. Struct. Mol. Biol. 20 2013 1131 1139
52. J. Yang, A.L. van Oosten, T.W. Theunissen, G. Guo, J.C. Silva, and A. Smith Stat3 activation is limiting for reprogramming to ground state pluripotency Cell Stem Cell 7 2010 319 328
53. S. Yao, S. Chen, J. Clark, E. Hao, G.M. Beattie, A. Hayek, and S. Ding Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions Proc. Natl. Acad. Sci. USA 103 2006 6907 6912
54. Y. Zhang, T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu Model-based analysis of ChIP-Seq (MACS) Genome Biol. 9 2008 R137
55. Y. Zhang, W. Li, T. Laurent, and S. Ding Small molecules, big roles - the chemical manipulation of stem cell fate and somatic cell reprogramming J. Cell Sci. 125 2012 5609 5620
56. H. Zhou, W. Li, S. Zhu, J.Y. Joo, J.T. Do, W. Xiong, J.B. Kim, K. Zhang, H.R. Schöler, and S. Ding Conversion of mouse epiblast stem cells to an earlier pluripotency state by small molecules J. Biol. Chem. 285 2010 29676 29680