The function of chromatin modifiers in lineage commitment and cell fate specification

FEBS Journal

Volumn 282, Issue 9, 2015, Pages 1692-1702

  Signolet, Jason ^a   Hendrich, Brian ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

development; gene expression; gene regulatory network; NuRD; polycomb; stem cells

Indexed keywords

BMI1 PROTEIN; HISTONE DEACETYLASE; HISTONE H3; KRUPPEL LIKE FACTOR 4; KRUPPEL LIKE FACTOR 5; LEUKEMIA INHIBITORY FACTOR; POLYCOMB REPRESSIVE COMPLEX 2; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR NANOG; CHROMATIN;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL FATE; CELL RENEWAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; MESODERM; MORULA; MOUSE; NONHUMAN; NUCLEOSOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; ZYGOTE; ANIMAL; CELL LINEAGE; CYTOLOGY; METABOLISM;

MAMMALIA; METAZOA;

ANIMALS; CELL LINEAGE; CHROMATIN; EMBRYONIC STEM CELLS; GENE REGULATORY NETWORKS; MICE;

EID: 84928485442     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13132     Document Type: Article

References (98)

1. Nichols J, &, Smith A, (2012) Pluripotency in the embryo and in culture. Cold Spring Harb Perspect Biol 4, a008128.
2. Daley GQ, &, Scadden DT, (2008) Prospects for stem cell-based therapy. Cell 132, 544-548.
3. Ferreira LM, &, Mostajo-Radji MA, (2013) How induced pluripotent stem cells are redefining personalized medicine. Gene 520, 1-6.
4. Pourquie O, Bruneau B, Gotz M, Keller G, &, Smith A, (2013) Stem cells and regeneration: a special issue. Development (Cambridge, England) 140, 2445.
5. Clapier CR, &, Cairns BR, (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78, 273-304.
6. Iyer VR, (2012) Nucleosome positioning: bringing order to the eukaryotic genome. Trends Cell Biol 22, 250-256.
7. Struhl K, &, Segal E, (2013) Determinants of nucleosome positioning. Nat Struct Mol Biol 20, 267-273.
8. O'Shaughnessy A, &, Hendrich B, (2013) CHD4 in the DNA-damage response and cell cycle progression: not so NuRDy now. Biochem Soc Trans 41, 777-782.
9. Lessard JA, &, Crabtree GR, (2010) Chromatin regulatory mechanisms in pluripotency. Annu Rev Cell Dev Biol 26, 503-532.
10. Laugesen A, &, Helin K, (2014) Chromatin repressive complexes in stem cells, development, and cancer. Cell Stem Cell 14, 735-751.
11. Paul S, &, Knott JG, (2014) Epigenetic control of cell fate in mouse blastocysts: the role of covalent histone modifications and chromatin remodeling. Mol Reprod Dev 81, 171-182.
12. Bird A, (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16, 6-21.
13. Wray J, Kalkan T, &, Smith AG, (2010) The ground state of pluripotency. Biochem Soc Trans 38, 1027-1032.
14. Ying QL, 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.
15. Canham MA, Sharov AA, Ko MS, &, Brickman JM, (2010) Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol 8, e1000379.
16. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, &, Smith A, (2007) Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1234.
17. Kalmar T, Lim C, Hayward P, Munoz-Descalzo S, Nichols J, Garcia-Ojalvo J, &, Martinez Arias A, (2009) Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biol 7, e1000149.
18. Wu J, &, Tzanakakis ES, (2013) Deconstructing stem cell population heterogeneity: single-cell analysis and modeling approaches. Biotechnol Adv 31, 1047-1062.
19. Martinez Arias A, &, Brickman JM, (2011) Gene expression heterogeneities in embryonic stem cell populations: origin and function. Curr Opin Cell Biol 23, 650-656.
20. Raj A, &, van Oudenaarden A, (2008) Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226.
21. Kobayashi T, Mizuno H, Imayoshi I, Furusawa C, Shirahige K, &, Kageyama R, (2009) The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev 23, 1870-1875.
22. Huang S, (2009) Reprogramming cell fates: reconciling rarity with robustness. BioEssays 31, 546-560.
23. Arriaga EA, (2009) Determining biological noise via single cell analysis. Anal Bioanal Chem 393, 73-80.
24. Huang S, (2009) Non-genetic heterogeneity of cells in development: more than just noise. Development (Cambridge, England) 136, 3853-3862.
25. Maheshri N, &, O'Shea EK, (2007) Living with noisy genes: how cells function reliably with inherent variability in gene expression. Annu Rev Biophys Biomol Struct 36, 413-434.
26. Elowitz MB, Levine AJ, Siggia ED, &, Swain PS, (2002) Stochastic gene expression in a single cell. Science (New York, NY) 297, 1183-1186.
27. Newman JR, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL, &, Weissman JS, (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441, 840-846.
28. Raser JM, &, O'Shea EK, (2004) Control of stochasticity in eukaryotic gene expression. Science (New York, NY) 304, 1811-1814.
29. Morelli MJ, Allen RJ, &, Wolde PR, (2011) Effects of macromolecular crowding on genetic networks. Biophys J 101, 2882-2891.
30. Faddah DA, Wang H, Cheng AW, Katz Y, Buganim Y, &, Jaenisch R, (2013) Single-cell analysis reveals that expression of nanog is biallelic and equally variable as that of other pluripotency factors in mouse ESCs. Cell Stem Cell 13, 23-29.
31. Filipczyk A, Gkatzis K, Fu J, Hoppe PS, Lickert H, Anastassiadis K, &, Schroeder T, (2013) Biallelic expression of nanog protein in mouse embryonic stem cells. Cell Stem Cell 13, 12-13.
32. Miyanari Y, &, Torres-Padilla ME, (2012) Control of ground-state pluripotency by allelic regulation of Nanog. Nature 483, 470-473.
33. Niwa H, Ogawa K, Shimosato D, &, Adachi K, (2009) A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 460, 118-122.
34. Reynolds N, Latos P, Hynes-Allen A, Loos R, Leaford D, O'Shaughnessy A, Mosaku O, Signolet J, Brennecke P, Kalkan T, et al.,. (2012) NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment. Cell Stem Cell 10, 583-594.
35. Toyooka Y, Shimosato D, Murakami K, Takahashi K, &, Niwa H, (2008) Identification and characterization of subpopulations in undifferentiated ES cell culture. Development (Cambridge, England) 135, 909-918.
36. Wray J, Kalkan T, Gomez-Lopez S, Eckardt D, Cook A, Kemler R, &, Smith A, (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.
37. Hayashi K, Lopes SM, Tang F, &, Surani MA, (2008) Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3, 391-401.
38. Huang S, (2010) Cell lineage determination in state space: a systems view brings flexibility to dogmatic canonical rules. PLoS Biol 8, e1000380.
39. Chang HH, Hemberg M, Barahona M, Ingber DE, &, Huang S, (2008) Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453, 544-547.
40. Huang S, Ernberg I, &, Kauffman S, (2009) Cancer attractors: a systems view of tumors from a gene network dynamics and developmental perspective. Semin Cell Dev Biol 20, 869-876.
41. Wang J, Xu L, Wang E, &, Huang S, (2010) The potential landscape of genetic circuits imposes the arrow of time in stem cell differentiation. Biophys J 99, 29-39.
42. Levy SF, &, Siegal ML, (2008) Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol 6, e264.
43. Lu R, Markowetz F, Unwin RD, Leek JT, Airoldi EM, MacArthur BD, Lachmann A, Rozov R, Ma'ayan A, Boyer LA, et al.,. (2009) Systems-level dynamic analyses of fate change in murine embryonic stem cells. Nature 462, 358-362.
44. Ng HH, &, Surani MA, (2011) The transcriptional and signalling networks of pluripotency. Nat Cell Biol 13, 490-496.
45. Ahringer J, (2000) NuRD and SIN3 histone deacetylase complexes in development. Trends Genet 16, 351-356.
46. Allen HF, Wade PA, &, Kutateladze TG, (2013) The NuRD architecture. Cell Mol Life Sci 70, 3513-3524.
47. McDonel P, Costello I, &, Hendrich B, (2009) Keeping things quiet: roles of NuRD and Sin3 co-repressor complexes during mammalian development. Int J Biochem Cell Biol 41, 108-116.
48. Reynolds N, O'Shaughnessy A, &, Hendrich B, (2013) Transcriptional repressors: multifaceted regulators of gene expression. Development (Cambridge, England) 140, 505-512.
49. Shimbo T, Du Y, Grimm SA, Dhasarathy A, Mav D, Shah RR, Shi H, &, Wade PA, (2013) MBD3 localizes at promoters, gene bodies and enhancers of active genes. PLoS Genet 9, e1004028.
50. Baubec T, Ivanek R, Lienert F, &, Schubeler D, (2013) Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 153, 480-492.
51. Gunther K, Rust M, Leers J, Boettger T, Scharfe M, Jarek M, Bartkuhn M, &, Renkawitz R, (2013) Differential roles for MBD2 and MBD3 at methylated CpG islands, active promoters and binding to exon sequences. Nucleic Acids Res 41, 3010-3021.
52. Kaji K, Caballero IM, MacLeod R, Nichols J, Wilson VA, &, Hendrich B, (2006) The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 8, 285-292.
53. Narlikar GJ, Sundaramoorthy R, &, Owen-Hughes T, (2013) Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154, 490-503.
54. Morris SA, Baek S, Sung MH, John S, Wiench M, Johnson TA, Schiltz RL, &, Hager GL, (2014) Overlapping chromatin-remodeling systems collaborate genome wide at dynamic chromatin transitions. Nat Struct Mol Biol 21, 73-81.
55. Kaji K, Nichols J, &, Hendrich B, (2007) Mbd3, a component of the NuRD co-repressor complex, is required for development of pluripotent cells. Development (Cambridge, England) 134, 1123-1132.
56. Latos PA, Helliwell C, Mosaku O, Dudzinska DA, Stubbs B, Berdasco M, Esteller M, &, Hendrich B, (2012) NuRD-dependent DNA methylation prevents ES cells from accessing a trophectoderm fate. Biol Open 1, 341-352.
57. Zhu D, Fang J, Li Y, &, Zhang J, (2009) Mbd3, a component of NuRD/Mi-2 complex, helps maintain pluripotency of mouse embryonic stem cells by repressing trophectoderm differentiation. PLoS One 4, e7684.
58. dos Santos RL, Tosti L, Radzisheuskaya A, Caballero IM, Kaji K, Hendrich B, &, Silva JC, (2014) MBD3/NuRD facilitates induction of pluripotency in a context-dependent manner. Cell Stem Cell 15, 102-110.
59. Kashiwagi M, Morgan BA, &, Georgopoulos K, (2007) The chromatin remodeler Mi-2beta is required for establishment of the basal epidermis and normal differentiation of its progeny. Development (Cambridge, England) 134, 1571-1582.
60. Yoshida T, Hazan I, Zhang J, Ng SY, Naito T, Snippert HJ, Heller EJ, Qi X, Lawton LN, Williams CJ, et al.,. (2008) The role of the chromatin remodeler Mi-2{beta} in hematopoietic stem cell self-renewal and multilineage differentiation. Genes Dev 22, 1174-1189.
61. Mazumdar A, Wang RA, Mishra SK, Adam L, Bagheri-Yarmand R, Mandal M, Vadlamudi RK, &, Kumar R, (2001) Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nat Cell Biol 3, 30-37.
62. Schmitt C, Tonnelle C, Dalloul A, Chabannon C, Debre P, &, Rebollo A, (2002) Aiolos and Ikaros: regulators of lymphocyte development, homeostasis and lymphoproliferation. Apoptosis 7, 277-284.
63. Bowen NJ, Fujita N, Kajita M, &, Wade PA, (2004) Mi-2/NuRD: multiple complexes for many purposes. Biochim Biophys Acta 1677, 52-57.
64. Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, &, Wade PA, (2003) MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113, 207-219.
65. Faust C, Schumacher A, Holdener B, &, Magnuson T, (1995) The eed mutation disrupts anterior mesoderm production in mice. Development (Cambridge, England) 121, 273-285.
66. O'Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, &, Jenuwein T, (2001) The polycomb-group gene Ezh2 is required for early mouse development. Mol Cell Biol 21, 4330-4336.
67. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, &, Helin K, (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23, 4061-4071.
68. Margueron R, &, Reinberg D, (2011) The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349.
69. Voigt P, LeRoy G, Drury WJ III, Zee BM, Son J, Beck DB, Young NL, Garcia BA, &, Reinberg D, (2012) Asymmetrically modified nucleosomes. Cell 151, 181-193.
70. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, et al.,. (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8, 532-538.
71. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al.,. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
72. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, et al.,. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560.
73. Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H, Jonsdottir GA, Stewart R, &, Thomson JA, (2007) Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1, 299-312.
74. Faust C, Lawson KA, Schork NJ, Thiel B, &, Magnuson T, (1998) The Polycomb-group gene eed is required for normal morphogenetic movements during gastrulation in the mouse embryo. Development (Cambridge, England) 125, 4495-4506.
75. Pasini D, Bracken A, Hansen J, Capillo M, &, Helin K, (2007) The polycomb group protein Suz12 Is required for embryonic stem cell differentiation. Mol Cell Biol 27, 3769-3779.
76. Williams RR, Azuara V, Perry P, Sauer S, Dvorkina M, Jorgensen H, Roix J, McQueen P, Misteli T, Merkenschlager M, et al.,. (2006) Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J Cell Sci 119, 132-140.
77. Chamberlain SJ, Yee D, &, Magnuson T, (2008) Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 26, 1496-1505.
78. Shen X, Liu Y, Hsu YJ, Fujiwara Y, Kim J, Mao X, Yuan G, &, Orkin SH, (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.
79. Marks H, Kalkan T, Menafra R, Denissov S, Jones K, Hofemeister H, Nichols J, Kranz A, Stewart AF, Smith A, et al.,. (2012) The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590-604.
80. Denissov S, Hofemeister H, Marks H, Kranz A, Ciotta G, Singh S, Anastassiadis K, Stunnenberg HG, &, Stewart AF, (2014) Mll2 is required for H3K4 trimethylation on bivalent promoters in embryonic stem cells, whereas Mll1 is redundant. Development (Cambridge, England) 141, 526-537.
81. Hu D, Garruss AS, Gao X, Morgan MA, Cook M, Smith ER, &, Shilatifard A, (2013) The Mll2 branch of the COMPASS family regulates bivalent promoters in mouse embryonic stem cells. Nat Struct Mol Biol 20, 1093-1097.
82. Riising EM, Comet I, Leblanc B, Wu X, Johansen JV, &, Helin K, (2014) Gene silencing triggers polycomb repressive complex 2 recruitment to CpG islands genome wide. Mol Cell 55, 347-360.
83. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, et al.,. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441, 349-353.
84. Bienz M, &, Muller J, (1995) Transcriptional silencing of homeotic genes in Drosophila. BioEssays 17, 775-784.
85. White RA, &, Lehmann R, (1986) A gap gene, hunchback, regulates the spatial expression of Ultrabithorax. Cell 47, 311-321.
86. Struhl G, &, Akam M, (1985) Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J 4, 3259-3264.
87. Kehle J, Beuchle D, Treuheit S, Christen B, Kennison JA, Bienz M, &, Müller J, (1998) dMi-2, a hunchback-interacting protein that functions in Polycomb repression. Science (New York, NY) 282, 1897-1900.
88. Unhavaithaya Y, Shin TH, Miliaras N, Lee J, Oyama T, &, Mello CC, (2002) MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans. Cell 111, 991-1002.
89. Eshed Y, Baum SF, &, Bowman JL, (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99, 199-209.
90. Ogas J, Cheng JC, Sung ZR, &, Somerville C, (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science (New York, NY) 277, 91-94.
91. Ogas J, Kaufmann S, Henderson J, &, Somerville C, (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 96, 13839-13844.
92. Ferrari KJ, Scelfo A, Jammula S, Cuomo A, Barozzi I, Stutzer A, Fischle W, Bonaldi T, &, Pasini D, (2014) Polycomb-dependent H3K27me1 and H3K27me2 regulate active transcription and enhancer fidelity. Mol Cell 53, 49-62.
93. Morey L, &, Helin K, (2010) Polycomb group protein-mediated repression of transcription. Trends Biochem Sci 35, 323-332.
94. Reynolds N, Salmon-Divon M, Dvinge H, Hynes-Allen A, Balasooriya G, Leaford D, Behrens A, Bertone P, &, Hendrich B, (2012) NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression. EMBO J 31, 593-605.
95. Morey L, Brenner C, Fazi F, Villa R, Gutierrez A, Buschbeck M, Nervi C, Minucci S, Fuks F, &, Di Croce L, (2008) MBD3, a component of the NuRD complex, facilitates chromatin alteration and deposition of epigenetic marks. Mol Cell Biol 28, 5912-5923.
96. Halley JD, Burden FR, &, Winkler DA, (2009) Stem cell decision making and critical-like exploratory networks. Stem Cell Res 2, 165-177.
97. Torres-Sosa C, Huang S, &, Aldana M, (2012) Criticality is an emergent property of genetic networks that exhibit evolvability. PLoS Comput Biol 8, e1002669.
98. Balazsi G, van Oudenaarden A, &, Collins JJ, (2011) Cellular decision making and biological noise: from microbes to mammals. Cell 144, 910-925.