The epigenomics of embryonic stem cell differentiation

International Journal of Biological Sciences

Volumn 9, Issue 10, 2013, Pages 1134-1144

  Kraushaar, Daniel C ^a   Zhao, Keji ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Chromatin; Differentiation; Embryonic stem cells; Epigenomics

Indexed keywords

ADENOSINE TRIPHOSPHATE;

CELL DIFFERENTIATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOLOGY; DIFFERENTIATION; DNA METHYLATION; EMBRYONIC STEM CELL; EPIGENETICS; HUMAN; METABOLISM; REVIEW;

CHROMATIN; DIFFERENTIATION; EMBRYONIC STEM CELLS; EPIGENOMICS;

ADENOSINE TRIPHOSPHATE; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIGENOMICS; HUMANS;

EID: 84896398544     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.7998     Document Type: Review

References (116)

1. Bradley A, Evans M, Kaufman MH, Robertson E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 1984; 309: 255-6.
2. Lanner F, Rossant J. The role of FGF/Erk signaling in pluripotent cells. Development 2010; 137: 3351-60.
3. Li Z, Chen YG. Functions of BMP signaling in embryonic stem cell fate determination. Exp Cell Res 2013; 319: 113-9.
4. Loebel DA, Watson CM, De Young RA, Tam PP. Lineage choice and differentiation in mouse embryos and embryonic stem cells. Dev Biol 2003; 264: 1-14.
5. Okita K, Yamanaka S. Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr Stem Cell Res Ther 2006; 1: 103-11.
6. Kraushaar DC, Dalton S, Wang L. Heparan sulfate: a key regulator of embryonic stem cell fate. Biol Chem 2013; 394: 741-51.
7. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 1992; 69: 915-26.
8. Bultman S, Gebuhr T, Yee D et al. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 2000; 6: 1287-95.
9. O'Carroll D, Erhardt S, Pagani M et al. The polycomb-group gene Ezh2 is required for early mouse development. Mol Cell Biol 2001; 21: 4330-6.
10. Wang Z, Schones DE, Zhao K. Characterization of human epigenomes. Curr Opin Genet Dev 2009; 19: 127-34.
11. Zhou VW, Goren A, Bernstein BE. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 2011; 12: 7-18.
12. Smallwood A, Ren B. Genome organization and long-range regulation of gene expression by enhancers. Curr Opin Cell Biol 2013; 25: 387-94.
13. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-76.
14. Yu J, Vodyanik MA, Smuga-Otto K et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917-20.
15. Chin MH, Mason MJ, Xie W et al. Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 2009; 5: 111-23.
16. Guenther MG, Frampton GM, Soldner F et al. Chromatin structure and gene expression programs of human embryonic and induced pluripotent stem cells. Cell Stem Cell 2010; 7: 249-57.
17. Mikkelsen TS, Hanna J, Zhang X et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 2008; 454: 49-55.
18. Maherali N, Sridharan R, Xie W et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007; 1: 55-70.
19. Efroni S, Duttagupta R, Cheng J et al. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2008; 2: 437-47.
20. Stock JK, Giadrossi S, Casanova M et al. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 2007; 9: 1428-35.
21. Meshorer E, Yellajoshula D, George E et al. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 2006; 10: 105-16.
22. Wiblin AE, Cui W, Clark AJ, Bickmore WA. Distinctive nuclear organisation of centromeres and regions involved in pluripotency in human embryonic stem cells. J Cell Sci 2005; 118: 3861-8.
23. Pajerowski JD, Dahl KN, Zhong FL et al. Physical plasticity of the nucleus in stem cell differentiation. Proc Natl Acad Sci U S A 2007; 104: 15619-24.
24. Mikkelsen TS, Ku M, Jaffe DB et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007; 448: 553-60.
25. Wen B, Wu H, Shinkai Y et al. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet 2009; 41: 246-50.
26. Boyer LA, Plath K, Zeitlinger J et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006; 441: 349-53.
27. Azuara V, Perry P, Sauer S et al. Chromatin signatures of pluripotent cell lines. Nat Cell Biol 2006; 8: 532-8.
28. Creyghton MP, Cheng AW, Welstead GG et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 2010; 107: 21931-6.
29. Zentner GE, Tesar PJ, Scacheri PC. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res 2011; 21: 1273-83.
30. Gifford CA, Ziller MJ, Gu H et al. Transcriptional and epigenetic dynamics during specification of human embryonic stem cells. Cell 2013; 153: 1149-63.
31. Roh TY, Cuddapah S, Cui K, Zhao K. The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci U S A 2006; 103: 15782-7.
32. Cui K, Zang C, Roh TY et al. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 2009; 4: 80-93.
33. Abraham BJ, Cui K, Tang Q, Zhao K. Dynamic regulation of epigenomic landscapes during hematopoiesis. BMC Genomics 2013; 14: 193.
34. Mazzarella L, Jorgensen HF, Soza-Ried J et al. Embryonic stem cell-derived hemangioblasts remain epigenetically plastic and require PRC1 to prevent neural gene expression. Blood 2011; 117: 83-7.
35. Wei G, Wei L, Zhu J et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 2009; 30: 155-67.
36. Burney MJ, Johnston C, Wong KY et al. An epigenetic signature of developmental potential in neural stem cells and early neurons. Stem Cells 2013; 31: 1868-80.
37. Dou Y, Milne TA, Ruthenburg AJ et al. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol 2006; 13: 713-9.
38. Zhou W, Zhu P, Wang J et al. Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol Cell 2008; 29: 69-80.
39. Nakagawa T, Kajitani T, Togo S et al. Deubiquitylation of histone H2A activates transcriptional initiation via trans-histone cross-talk with H3K4 diand trimethylation. Genes Dev 2008; 22: 37-49.
40. Ku M, Koche RP, Rheinbay E et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 2008; 4: e1000242.
41. Lee TI, Jenner RG, Boyer LA et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006; 125: 301-13.
42. Chamberlain SJ, Yee D, Magnuson T. Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 2008; 26: 1496-505.
43. Wang C, Lee JE, Cho YW et al. UTX regulates mesoderm differentiation of embryonic stem cells independent of H3K27 demethylase activity. Proc Natl Acad Sci U S A 2012; 109: 15324-9.
44. Ang YS, Tsai SY, Lee DF et al. Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 2011; 145: 183-97.
45. Jiang H, Shukla A, Wang X et al. Role for Dpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains. Cell 2011; 144: 513-25.
46. Lubitz S, Glaser S, Schaft J et al. Increased apoptosis and skewed differentiation in mouse embryonic stem cells lacking the histone methyltransferase Mll2. Mol Biol Cell 2007; 18: 2356-66.
47. Hu D, Garruss AS, Gao X et al. The Mll2 branch of the COMPASS family regulates bivalent promoters in mouse embryonic stem cells. Nat Struct Mol Biol 2013; 20: 1093-7.
48. Adamo A, Sese B, Boue S et al. LSD1 regulates the balance between self-renewal and differentiation in human embryonic stem cells. Nat Cell Biol 2011; 13: 652-9.
49. Kidder BL, Hu G, Yu ZX et al. Extended self-renewal and accelerated reprogramming in the absence of Kdm5b. Mol Cell Biol 2013.
50. Shogren-Knaak M, Ishii H, Sun JM et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006; 311: 844-7.
51. Loyola A, Almouzni G. Bromodomains in living cells participate in deciphering the histone code. Trends Cell Biol 2004; 14: 279-81.
52. Wang Z, Zang C, Cui K et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138: 1019-31.
53. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 2009; 10: 32-42.
54. Yang XJ, Seto E. Collaborative spirit of histone deacetylases in regulating chromatin structure and gene expression. Curr Opin Genet Dev 2003; 13: 143-53.
55. Kidder BL, Palmer S. HDAC1 regulates pluripotency and lineage specific transcriptional networks in embryonic and trophoblast stem cells. Nucleic Acids Res 2012; 40: 2925-39.
56. Carrozza MJ, Li B, Florens L et al. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 2005; 123: 581-92.
57. Lee JH, Hart SR, Skalnik DG. Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis 2004; 38: 32-8.
58. Dovey OM, Foster CT, Cowley SM. Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc Natl Acad Sci U S A 2010; 107: 8242-7.
59. Huangfu D, Maehr R, Guo W et al. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 2008; 26: 795-7.
60. Huangfu D, Osafune K, Maehr R et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 2008; 26: 1269-75.
61. Liang G, Taranova O, Xia K, Zhang Y. Butyrate promotes induced pluripotent stem cell generation. J Biol Chem 2010; 285: 25516-21.
62. Mali P, Chou BK, Yen J et al. Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency-associated genes. Stem Cells 2010; 28: 713-20.
63. Fazzio TG, Huff JT, Panning B. An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 2008; 134: 162-74.
64. Chen X, Xu H, Yuan P et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008; 133: 1106-17.
65. Li X, Li L, Pandey R et al. The histone acetyltransferase MOF is a key regulator of the embryonic stem cell core transcriptional network. Cell Stem Cell 2012; 11: 163-78.
66. Zhong X, Jin Y. Critical roles of coactivator p300 in mouse embryonic stem cell differentiation and Nanog expression. J Biol Chem 2009; 284: 9168-75.
67. Ho L, Ronan JL, Wu J et al. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc Natl Acad Sci U S A 2009; 106: 5181-6.
68. Ho L, Jothi R, Ronan JL et al. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc Natl Acad Sci U S A 2009; 106: 5187-91.
69. Kidder BL, Palmer S, Knott JG. SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells 2009; 27: 317-28.
70. Ho L, Miller EL, Ronan JL et al. esBAF facilitates pluripotency by conditioning the genome for LIF/STAT3 signalling and by regulating polycomb function. Nat Cell Biol 2011; 13: 903-13.
71. Yildirim O, Li R, Hung JH et al. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 2011; 147: 1498-510.
72. Pastor WA, Pape UJ, Huang Y et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011; 473: 394-7.
73. Koh KP, Yabuuchi A, Rao S et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011; 8: 200-13.
74. Ito S, D'Alessio AC, Taranova OV et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010; 466: 1129-33.
75. Wu H, D'Alessio AC, Ito S et al. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 2011; 473: 389-93.
76. Wu H, D'Alessio AC, Ito S et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 2011; 25: 679-84.
77. Hall JA, Georgel PT. CHD proteins: a diverse family with strong ties. Biochem Cell Biol 2007; 85: 463-76.
78. Gaspar-Maia A, Alajem A, Polesso F et al. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 2009; 460: 863-8.
79. Konev AY, Tribus M, Park SY et al. CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 2007; 317: 1087-90.
80. Schnetz MP, Bartels CF, Shastri K et al. Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res 2009; 19: 590-601.
81. Schnetz MP, Handoko L, Akhtar-Zaidi B et al. CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet 2010; 6: e1001023.
82. Bilodeau S, Kagey MH, Frampton GM et al. SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev 2009; 23: 2484-9.
83. Loh YH, Zhang W, Chen X et al. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev 2007; 21: 2545-57.
84. Szenker E, Ray-Gallet D, Almouzni G. The double face of the histone variant H3.3. Cell Res 2011; 21: 421-34.
85. Redon C, Pilch D, Rogakou E et al. Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 2002; 12: 162-9.
86. Goldberg AD, Banaszynski LA, Noh KM et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010; 140: 678-91.
87. McKittrick E, Gafken PR, Ahmad K, Henikoff S. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci U S A 2004; 101: 1525-30.
88. Hake SB, Garcia BA, Duncan EM et al. Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem 2006; 281: 559-68.
89. Hodl M, Basler K. Transcription in the absence of histone H3.3. Curr Biol 2009; 19: 1221-6.
90. Ray-Gallet D, Woolfe A, Vassias I et al. Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell 2011; 44: 928-41.
91. Jin C, Zang C, Wei G et al. H3.3/H2A. Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet 2009; 41: 941-5.
92. Kraushaar DC, Jin W, Maunakea A et al. Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol 2013; 14: R121.
93. Banaszynski LA, Wen D, Dewell S et al. Hira-Dependent Histone H3.3 Deposition Facilitates PRC2 Recruitment at Developmental Loci in ES Cells. Cell 2013; 155: 107-20.
94. Wong LH, McGhie JD, Sim M et al. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 2010; 20: 351-60.
95. Wong LH, Ren H, Williams E et al. Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res 2009; 19: 404-14.
96. Kafer GR, Lehnert SA, Pantaleon M et al. Expression of genes coding for histone variants and histone-associated proteins in pluripotent stem cells and mouse preimplantation embryos. Gene Expr Patterns 2010; 10: 299-305.
97. Barski A, Cuddapah S, Cui K et al. High-resolution profiling of histone methylations in the human genome. Cell 2007; 129: 823-37.
98. Illingworth RS, Botting CH, Grimes GR et al. PRC1 and PRC2 are not required for targeting of H2A. Z to developmental genes in embryonic stem cells. PLoS One 2012; 7: e34848.
99. Hu G, Cui K, Northrup D et al. H2A. Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2013; 12: 180-92.
100. Li Z, Gadue P, Chen K et al. Foxa2 and H2A. Z mediate nucleosome depletion during embryonic stem cell differentiation. Cell 2012; 151: 1608-16.
101. Dion MF, Kaplan T, Kim M et al. Dynamics of replication-independent histone turnover in budding yeast. Science 2007; 315: 1405-8.
102. Senner CE. The role of DNA methylation in mammalian development. Reprod Biomed Online 2011; 22: 529-35.
103. Prendergast GC, Ziff EB. Methylation-sensitive sequence-specific DNA binding by the c-Myc basic region. Science 1991; 251: 186-9.
104. Birke M, Schreiner S, Garcia-Cuellar MP et al. The MT domain of the proto-oncoprotein MLL binds to CpG-containing DNA and discriminates against methylation. Nucleic Acids Res 2002; 30: 958-65.
105. Jones PL, Veenstra GJ, Wade PA et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998; 19: 187-91.
106. Nan X, Ng HH, Johnson CA et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998; 393: 386-9.
107. Ng HH, Zhang Y, Hendrich B et al. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat Genet 1999; 23: 58-61.
108. Maunakea AK, Chepelev I, Cui K, Zhao K. Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition. Cell Res 2013.
109. Tsumura A, Hayakawa T, Kumaki Y et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 2006; 11: 805-14.
110. Jackson M, Krassowska A, Gilbert N et al. Severe global DNA hypomethylation blocks differentiation and induces histone hyperacetylation in embryonic stem cells. Mol Cell Biol 2004; 24: 8862-71.
111. Meissner A, Mikkelsen TS, Gu H et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008; 454: 766-70.
112. Laurent L, Wong E, Li G et al. Dynamic changes in the human methylome during differentiation. Genome Res 2010; 20: 320-31.
113. Fouse SD, Shen Y, Pellegrini M et al. Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2008; 2: 160-9.
114. Xie W, Schultz MD, Lister R et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 2013; 153: 1134-48.
115. Lister R, Pelizzola M, Dowen RH et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462: 315-22.
116. Guo JU, Su Y, Zhong C et al. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011; 145: 423-34.