NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment

Cell Stem Cell

Volumn 10, Issue 5, 2012, Pages 583-594

  Reynolds, Nicola ^a   Latos, Paulina ^a   Hynes Allen, Antony ^a   Loos, Remco ^b   Leaford, Donna ^a   O'Shaughnessy, Aoife ^a   Mosaku, Olukunbi ^a   Signolet, Jason ^a   Brennecke, Philip ^a   Kalkan, Tüzer ^a   Costello, Ita ^c   Humphreys, Peter ^a   Mansfield, William ^a   Nakagawa, Kentaro ^d   Strouboulis, John ^e   Behrens, Axel ^d   Bertone, Paul ^a,b,f   Hendrich, Brian ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^e Biomedical Sciences Research Center Alexander Fleming Institute of Molecular Oncology   (Greece)

^f EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE;

ANIMAL CELL; ARTICLE; CELL LINEAGE; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; GENETIC HETEROGENEITY; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC HETEROGENEITY; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; MICE, KNOCKOUT; PLURIPOTENT STEM CELLS; TRANSCRIPTION FACTORS;

MAMMALIA;

EID: 84860647928     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.02.020     Document Type: Article

References (48)

1. J. Ahringer NuRD and SIN3 histone deacetylase complexes in development Trends Genet. 16 2000 351 356
2. I. Chambers The molecular basis of pluripotency in mouse embryonic stem cells Cloning Stem Cells 6 2004 386 391
3. 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
4. I. Chambers, J. Silva, D. Colby, J. Nichols, B. Nijmeijer, M. Robertson, J. Vrana, K. Jones, L. Grotewold, and A. Smith Nanog safeguards pluripotency and mediates germline development Nature 450 2007 1230 1234
5. C. Chen, X. Sun, Q. Ran, K.D. Wilkinson, T.J. Murphy, J.W. Simons, and J.-T. Dong Ubiquitin-proteasome degradation of KLF5 transcription factor in cancer and untransformed epithelial cells Oncogene 24 2005 3319 3327
6. Z.Y. Chen, X. Wang, Y. Zhou, G. Offner, and C.C. Tseng Destabilization of Kruppel-like factor 4 protein in response to serum stimulation involves the ubiquitin-proteasome pathway Cancer Res. 65 2005 10394 10400
7. 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
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. T. Enver, M. Pera, C. Peterson, and P.W. Andrews Stem cell states, fates, and the rules of attraction Cell Stem Cell 4 2009 387 397
10. 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
11. J. Hall, G. Guo, J. Wray, I. Eyres, J. Nichols, L. Grotewold, S. Morfopoulou, P. Humphreys, W. Mansfield, and R. Walker Oct4 and LIF/Stat3 additively induce Krüppel factors to sustain embryonic stem cell self-renewal Cell Stem Cell 5 2009 597 609
12. K. Hayashi, S.M. Lopes, F. Tang, and M.A. Surani Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states Cell Stem Cell 3 2008 391 401
13. S. Huang Non-genetic heterogeneity of cells in development: more than just noise Development 136 2009 3853 3862
14. K. Kaji, I.M. Caballero, R. MacLeod, J. Nichols, V.A. Wilson, and B. Hendrich The NuRD component Mbd3 is required for pluripotency of embryonic stem cells Nat. Cell Biol. 8 2006 285 292
15. K. Kaji, J. Nichols, and B. Hendrich Mbd3, a component of the NuRD co-repressor complex, is required for development of pluripotent cells Development 134 2007 1123 1132
16. T. Kalmar, C. Lim, P. Hayward, S. Muñoz-Descalzo, J. Nichols, J. Garcia-Ojalvo, and A. Martinez Arias Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells PLoS Biol. 7 2009 e1000149
17. M. Kashiwagi, B.A. Morgan, and K. Georgopoulos The chromatin remodeler Mi-2beta is required for establishment of the basal epidermis and normal differentiation of its progeny Development 134 2007 1571 1582
18. K.E. Kolodziej, F. Pourfarzad, E. de Boer, S. Krpic, F. Grosveld, and J. Strouboulis Optimal use of tandem biotin and V5 tags in ChIP assays BMC Mol. Biol. 10 2009 6
19. P.A. Latos, C. Helliwell, O. Mosaku, D.A. Dudzinska, B. Stubbs, M. Berdasco, M. Esteller, and B. Hendrich NuRD-dependent DNA methylation prevents ES cells from accessing a trophectoderm fate Biology Open 1 2012 341 352 10.1242/bio.2012513
20. H.G. Leitch, K. Blair, W. Mansfield, H. Ayetey, P. Humphreys, J. Nichols, M.A. Surani, and A. Smith Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state Development 137 2010 2279 2287
21. Y. Li, J. McClintick, L. Zhong, H.J. Edenberg, M.C. Yoder, and R.J. Chan Murine embryonic stem cell differentiation is promoted by SOCS-3 and inhibited by the zinc finger transcription factor Klf4 Blood 105 2005 635 637
22. X. Li, M. Ito, F. Zhou, N. Youngson, X. Zuo, P. Leder, and A.C. Ferguson-Smith A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints Dev. Cell 15 2008 547 557
23. H. Marks, T. Kalkan, R. Menafra, S. Denissov, K. Jones, H. Hofemeister, J. Nichols, A. Kranz, A.F. Stewart, A. Smith, and H.G. Stunnenberg The Transcriptional and Epigenomic Foundations of Ground State Pluripotency Cell 149 2012 590 604
24. Y. Matsui, K. Zsebo, and B.L. Hogan Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture Cell 70 1992 841 847
25. P. McDonel, I. Costello, and B. Hendrich Keeping things quiet: roles of NuRD and Sin3 co-repressor complexes during mammalian development Int. J. Biochem. Cell Biol. 41 2009 108 116
26. A. Miccio, Y. Wang, W. Hong, G.D. Gregory, H. Wang, X. Yu, J.K. Choi, S. Shelat, W. Tong, M. Poncz, and G.A. Blobel NuRD mediates activating and repressive functions of GATA-1 and FOG-1 during blood development EMBO J. 29 2010 442 456
27. M. Murawska, M. Hassler, R. Renkawitz-Pohl, A. Ladurner, and A. Brehm Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression PLoS Genet. 7 2011 e1002206
28. J. Nichols, J. Silva, M. Roode, and A. Smith Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo Development 136 2009 3215 3222
29. H. Niwa How is pluripotency determined and maintained? Development 134 2007 635 646
30. 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
31. H. Niwa, K. Ogawa, D. Shimosato, and K. Adachi A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells Nature 460 2009 118 122
32. M.A. Nóbrega, Y. Zhu, I. Plajzer-Frick, V. Afzal, and E.M. Rubin Megabase deletions of gene deserts result in viable mice Nature 431 2004 988 993
33. A. Raj, and A. van Oudenaarden Nature, nurture, or chance: stochastic gene expression and its consequences Cell 135 2008 216 226
34. J.L. Resnick, L.S. Bixler, L. Cheng, and P.J. Donovan Long-term proliferation of mouse primordial germ cells in culture Nature 359 1992 550 551
35. N. Reynolds, M. Salmon-Divon, H. Dvinge, A. Hynes-Allen, G. Balasooriya, D. Leaford, A. Behrens, P. Bertone, and B. Hendrich NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression EMBO J. 31 2012 593 605
36. 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
37. Y. Toyooka, D. Shimosato, K. Murakami, K. Takahashi, and H. Niwa Identification and characterization of subpopulations in undifferentiated ES cell culture Development 135 2008 909 918
38. Z. Wang, C. Zang, K. Cui, D.E. Schones, A. Barski, W. Peng, and K. Zhao Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes Cell 138 2009 1019 1031
39. W.A. Whyte, S. Bilodeau, D.A. Orlando, H.A. Hoke, G.M. Frampton, C.T. Foster, S.M. Cowley, and R.A. Young Enhancer decommissioning by LSD1 during embryonic stem cell differentiation Nature 482 2012 221 225
40. J. Wray, T. Kalkan, and A.G. Smith The ground state of pluripotency Biochem. Soc. Trans. 38 2010 1027 1032
41. J. Wray, T. Kalkan, S. Gomez-Lopez, D. Eckardt, A. Cook, R. Kemler, and A. Smith 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 2011 838 845
42. S. Yamanaka A fresh look at iPS cells Cell 137 2009 13 17
43. 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
44. T. Yoshida, I. Hazan, J. Zhang, S.Y. Ng, T. Naito, H.J. Snippert, E.J. Heller, X. Qi, L.N. Lawton, C.J. Williams, and K. Georgopoulos The role of the chromatin remodeler Mi-2beta in hematopoietic stem cell self-renewal and multilineage differentiation Genes Dev. 22 2008 1174 1189
45. Y. Zhang, H.H. Ng, H. Erdjument-Bromage, P. Tempst, A. Bird, and D. Reinberg Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation Genes Dev. 13 1999 1924 1935
46. X. Zhang, J. Zhang, T. Wang, M.A. Esteban, and D. Pei Esrrb activates Oct4 transcription and sustains self-renewal and pluripotency in embryonic stem cells J. Biol. Chem. 283 2008 35825 35833
47. J. Zhang, A.F. Jackson, T. Naito, M. Dose, J. Seavitt, F. Liu, E.J. Heller, M. Kashiwagi, T. Yoshida, and F. Gounari Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis Nat. Immunol. 13 2012 86 94
48. D. Zhu, J. Fang, Y. Li, and J. Zhang Mbd3, a component of NuRD/Mi-2 complex, helps maintain pluripotency of mouse embryonic stem cells by repressing trophectoderm differentiation PLoS ONE 4 2009 e7684