Open chromatin in pluripotency and reprogramming

Nature Reviews Molecular Cell Biology

Volumn 12, Issue 1, 2011, Pages 36-47

  Gaspar Maia, Alexandre ^a,c   Alajem, Adi ^b   Meshorer, Eran ^b   Ramalho Santos, Miguel ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BRG1 PROTEIN; DEOXYRIBONUCLEASE I; DNA METHYLTRANSFERASE; HETEROCHROMATIN PROTEIN 1; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE; MESSENGER RNA; MICROCOCCAL NUCLEASE; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN P21; PROTEIN P53; RNA; TRANSCRIPTION FACTOR SOX2;

ADULT; CELL DIFFERENTIATION; CELL LINEAGE; CELL TYPE; CHROMATIN; DNA METHYLATION; EUCHROMATIN; GENE SILENCING; GENETIC TRANSCRIPTION; HETEROCHROMATIN; HUMAN; KNOCKOUT MOUSE; LANDSCAPE; NEOPLASM; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN CONFORMATION; REVIEW; TRANSCRIPTION INITIATION;

ANIMALS; CHROMATIN; HUMANS; MODELS, BIOLOGICAL; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELLS;

EID: 78650467973     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3036     Document Type: Review

References (142)

1. Evans, M. J. & Kaufman, M. H. Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156 (1981).
2. Martin, G. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl Acad. Sci. USA 78, 7634-7638 (1981).
3. Thomson, J. A. et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (1998).
4. Bradley, A., Evans, M., Kaufman, M. H. & Robertson, E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309, 255-266 (1984).
5. Kriegstein, A. & Alvarez-Buylla, A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184 (2009).
6. Dzierzak, E. The emergence of definitive hematopoietic stem cells in the mammal. Curr. Opin. Hematol. 12, 197-202 (2005). (Pubitemid 40676826)
7. Lee, G. et al. Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461, 402-406 (2009).
8. Carvajal-Vergara, X. et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 465, 808-812 (2010).
9. Matsui, Y., Zsebo, K. & Hogan, B. L. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70, 841-847 (1992).
10. Resnick, J. L., Bixler, L. S., Cheng, L. & Donovan, P. J. Long-term proliferation of mouse primordial germ cells in culture. Nature 359, 550-551 (1992).
11. Ko, K. et al. Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 5, 87-96 (2009).
12. Jaenisch, R. & Young, R. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132, 567-582 (2008).
13. Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006).
14. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007).
15. Lowry, W. E. et al. Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc. Natl Acad. Sci. USA 105, 2883-2888 (2008).
16. Park, I.-H. et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451, 141-146 (2008).
17. Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920 (2007).
18. Meshorer, E. & Misteli, T. Chromatin in pluripotent embryonic stem cells and differentiation. Nature Rev. Mol. Cell Biol. 7, 540-546 (2006). (Pubitemid 44036459)
19. Paweletz, N. Walther Flemming: pioneer of mitosis research. Nature Rev. Mol. Cell Biol. 2, 72-75 (2001).
20. Flemming, W. Zellsubstanz, Kern und Zelltheilung (ed. Vogel, F. C. W.; Leipzig, Germany, 1882).
21. Heitz, E. Das heterochromatin der moose. I. Jahrb Wiss Botanik 69, 762-818 (1928).
22. Reddien, P. W. & Sánchez-Alvarado, A. Fundamentals of planarian regenaration. Annu. Rev. Cell Dev. Biol. 20, 725-757 (2004).
23. Spangrude, G. J., Heimfeld, S. & Weissman, I. L. Purification and characterization of mouse hematopoietic stem cells. Science 241, 58-62 (1988).
24. Mattout, A. & Meshorer, E. Chromatin plasticity and genome organization in pluripotent embryonic stem cells. Curr. Opin. Cell Biol. 22, 334-341 (2010).
25. Park, S.-H. et al. Ultrastructure of human embryonic stem cells and spontaneous and retinoic acid-induced differentiating cells. Ultrastruct. Pathol. 28, 229-238 (2004).
26. Efroni, S. et al. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2, 437-447 (2008).
27. Ahmed, K. et al. Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS ONE 5, e10531 (2010).
28. Schaniel, C. et al. Smarcc1/Baf155 couples self-renewal gene repression with changes in chromatin structure in mouse embryonic stem cells. Stem Cells 27, 2979-2991 (2009).
29. Meshorer, E. et al. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 10, 105-116 (2006). (Pubitemid 43025681)
30. Wen, B., Wu, H., Shinkai, Y., Irizarry, R. & Feinberg, A. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nature Genet. 41, 246-250 (2009).
31. Hawkins, R. D. et al. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6, 479-491 (2010).
32. Krejcí, J. et al. Genome-wide reduction in H3K9 acetylation during human embryonic stem cell differentiation. J. Cell Physiol. 219, 677-687 (2009).
33. Bhattacharya, D., Talwar, S., Mazumder, A. & Shivashankar, G. V. Spatio-temporal plasticity in chromatin organization in mouse cell differentiation and during Drosophila embryogenesis. Biophys. J. 96, 3832-3839 (2009).
34. Szutorisz, H., Georgiou, A., Tora, L. & Dillon, N. The proteasome restricts permissive transcription at tissue-specific gene loci in embryonic stem cells. Cell 127, 1375-1388 (2006).
35. Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326 (2006).
36. Pan, G. et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1, 299-312 (2007).
37. Boyer, L. A., Mathur, D. & Jaenisch, R. Molecular control of pluripotency. Curr. Opin. Genet. Dev. 16, 455-462 (2006).
38. Kashyap, V. et al. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev. 18, 1093-1108 (2009).
39. Azuara, V. et al. Heritable gene silencing in lymphocytes delays chromatid resolution without affecting the timing of DNA replication. Nature Cell Biol. 5, 668-674 (2003).
40. Boyer, L. A. et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441, 349-353 (2006).
41. Lee, T. I. et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125, 301-313 (2006).
42. Chamberlain, S. J., Yee, D. & Magnuson, T. Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 26, 1496-1505 (2008).
43. Shen, X. et al. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 32, 491-502 (2008).
44. Pasini, D. et al. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464, 306-310 (2010).
45. Li, G. et al. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 24, 368-380 (2010).
46. Peng, J. C. et al. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139, 1290-1302 (2009).
47. Shen, X. et al. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139, 1303-1314 (2009).
48. Feldman, N. et al. G9a-mediated irreversible epigenetic inactivation of Oct 3/4 during early embryogenesis. Nature Cell Biol. 8, 188-194 (2006).
49. Epsztejn-Litman, S. et al. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nature Struct. Mol. Biol. 15, 1176-1183 (2008).
50. Loh, Y.-H., Zhang, W., Chen, X., George, J. & Ng, H.-H. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev. 21, 2545-2557 (2007).
51. Meissner, A. et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770 (2008).
52. Fouse, S. D. 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 2, 160-169 (2008).
53. Lister, R. et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322 (2009).
54. De la Serna, I. L., Ohkawa, Y. & Imbalzano, A. N. Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nature Rev. Genet. 7, 461-473 (2006).
55. Cairns, B. R. The logic of chromatin architecture and remodelling at promoters. Nature 461, 193-198 (2009).
56. Clapier, C. R. & Cairns, B. R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273-304 (2009).
57. Moshkin, Y. M., Mohrmann, L., van Ijcken, W. F. J. & Verrijzer, C. P. Functional differentiation of SWI/SNF remodelers in transcription and cell cycle control. Mol. Cell Biol. 27, 651-661 (2007).
58. Lessard, J. A. & Crabtree, G. R. Chromatin regulatory mechanisms in pluripotency. Annu. Rev. Cell Dev. Biol. 26, 503-532 (2010).
59. Ho, L. et al. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc. Natl Acad. Sci. USA 106, 5181-5186 (2009).
60. Kaeser, M. D., Aslanian, A., Dong, M.-Q., Yates, J. R. & Emerson, B. M. BRD7, a novel PBAF-specific SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells. J. Biol. Chem. 283, 32254-32263 (2008).
61. Bultman, S. et al. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287-1295 (2000).
62. Fazzio, T. G., Huff, J. T. & Panning, B. An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 134, 162-174 (2008).
63. Kidder, B. L., Palmer, S. & Knott, J. G. SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells 27, 317-328 (2009).
64. Ho, L. et al. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc. Natl Acad. Sci. USA 106, 5187-5191 (2009).
65. Gao, X. et al. ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc. Natl Acad. Sci. USA 105, 6656-6661 (2008).
66. Yan, Z. et al. BAF250B-associated SWI/SNF chromatin-remodeling complex is required to maintain undifferentiated mouse embryonic stem cells. Stem Cells 26, 1155-1165 (2008).
67. Bajpai, R. et al. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463, 958-962 (2010).
68. Schnetz, M. P. et al. Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res. 19, 590-601 (2009).
69. Gaspar-Maia, A. et al. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 460, 863-868 (2009).
70. Kaji, K. et al. The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nature Cell Biol. 8, 285-292 (2006).
71. Zhu, D., Fang, J., Li, Y. & Zhang, J. Mbd3, a component of NuRD/Mi-2 complex, helps maintain pluripotency of mouse embryonic stem cells by repressing trophectoderm differentiation. PLoS ONE 4, e7684 (2009).
72. Dovey, O. M., Foster, C. T. & Cowley, S. M. Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc. Natl Acad. Sci. USA 107, 8242-8247 (2010).
73. Guan, J.-S. et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459, 55-60 (2009).
74. Montgomery, R. L. et al. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev. 21, 1790-1802 (2007).
75. Zimmermann, S. et al. Reduced body size and decreased intestinal tumor rates in HDAC2-mutant mice. Cancer Res. 67, 9047-9054 (2007).
76. Trivedi, C. M. et al. Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3β activity. Nature Med. 13, 324-331 (2007).
77. Landry, J. et al. Essential role of chromatin remodeling protein Bptf in early mouse embryos and embryonic stem cells. PLoS Genet. 4, e1000241 (2008).
78. Fazzio, T. G. & Panning, B. Condensin complexes regulate mitotic progression and interphase chromatin structure in embryonic stem cells. J. Cell Biol. 188, 491-503 (2010).
79. Venkatasubrahmanyam, S., Hwang, W. W., Meneghini, M. D., Tong, A. H. Y. & Madhani, H. D. Genome-wide, as opposed to local, antisilencing is mediated redundantly by the euchromatic factors Set1 and H2AZ. Proc. Natl Acad. Sci. USA 104, 16609-16614 (2007).
80. Kimura, A., Umehara, T. & Horikoshi, M. Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nature Genet. 32, 370-377 (2002).
81. Osborne, E. A., Dudoit, S. & Rine, J. The establishment of gene silencing at single-cell resolution. Nature Genet. 41, 800-806 (2009).
82. McKittrick, E., Gafken, P. R., Ahmad, K. & Henikoff, S. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl Acad. Sci. USA, 101, 1525-1530 (2004).
83. Hake, S. B. et al. Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J. Biol. Chem. 281, 559-568 (2006).
84. Tagami, H., Ray-Gallet, D., Almouzni, G. & Nakatani, Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 11 6, 51-61 (2004). (Pubitemid 38156183)
85. Goldberg, A. D. et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678-691 (2010).
86. Mito, Y., Henikoff, J. G. & Henikoff, S. Genome-scale profiling of histone H3.3 replacement patterns. Nature Genet. 37, 1090-1097 (2005).
87. Ng, R. K. & Gurdon, J. B. Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nature Cell Biol. 10, 102-109 (2008).
88. Konev, A. Y. et al. CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 317, 1087-1090 (2007).
89. Sims, R. J. et al. Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J. Biol. Chem. 280, 41789-41792 (2005).
90. Sims, R. J. et al. Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol. Cell 28, 665-676 (2007).
91. Nishioka, K. et al. Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev. 16, 479-489 (2002).
92. Zegerman, P., Canas, B., Pappin, D. & Kouzarides, T. Histone H3 lysine 4 methylation disrupts binding of nucleosome remodeling and deacetylase (NuRD) repressor complex. J. Biol. Chem. 277, 11621-11624 (2002).
93. Ooi, S. K. T. et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714-717 (2007).
94. Ramalho-Santos, M. iPS cells: insights into basic biology. Cell 138, 616-618 (2009).
95. Brambrink, T. et al. Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell 2, 151-159 (2008).
96. Boyer, L. A. et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947-956 (2005).
97. Chen, X. et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117 (2008).
98. Nakagawa, M. et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nature Biotechnol. 26, 101-106 (2008).
99. Wernig, M. et al. A drug-inducible transgenic system for direct reprogramming of multiple somatic cell types. Nature Biotechnol. 26, 916-924 (2008).
100. Knoepfler, P. S. Why myc An unexpected ingredient in the stem cell cocktail. Cell Stem Cell 2, 18-21 (2008).
101. Sridharan, R. et al. Role of the murine reprogramming factors in the induction of pluripotency. Cell 136, 364-377 (2009).
102. Meissner, A., Wernig, M. & Jaenisch, R. Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nature Biotechnol. 25, 1177-1181 (2007).
103. Mikkelsen, T. S. et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 454, 49-55 (2008).
104. Hanna, J. et al. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462, 595-601 (2009).
105. Huangfu, D. et al. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nature Biotechnol. 26, 795-797 (2008).
106. Huangfu, D. et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nature Biotechnol. 26, 1269-1275 (2008).
107. Shi, Y. et al. A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell 2, 525-528 (2008).
108. Singhal, N. et al. Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 141, 943-955 (2010).
109. Yamanaka, S. & Blau, H. M. Nuclear reprogramming to a pluripotent state by three approaches. Nature 465, 704-712 (2010).
110. Egli, D. & Eggan, K. Recipient cell nuclear factors are required for reprogramming by nuclear transfer. Development 137, 1953-1963 (2010).
111. Kishigami, S. et al. Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340, 183-189 (2006).
112. Chin, M. H. et al. Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 5, 111-123 (2009).
113. Chin, M. H., Pellegrini, M., Plath, K. & Lowry, W. E. Molecular analyses of human induced pluripotent stem cells and embryonic stem cells. Cell Stem Cell 7, 263-269 (2010).
114. Polo, J. M. et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nature Biotech. 28, 848-855 (2010)
115. Kim, K. et al. Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290 (2010).
116. Filion, G. J. et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143, 212-224 (2010).
117. Bjerkvig, R., Tysnes, B. B., Aboody, K. S., Najbauer, J. & Terzis, A. J. A. The origin of the cancer stem cell: current controversies and new insights. Nature Rev. Cancer 5, 899-904 (2005).
118. Ruiz i Altaba, A., Sánchez, P. & Dahmane, N. Gli and hedgehog in cancer: tumours, embryos and stem cells. Nature Rev. Cancer 2, 361-372 (2002).
119. Reya, T., Morrison, S. J., Clarke, M. F. & Weissman, 1. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105-111 (2001).
120. Ben-Porath, I. et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nature Genet. 40, 499-507 (2008).
121. Komashko, V. M. et al. Using ChIP-chip technology to reveal common principles of transcriptional repression in normal and cancer cells. Genome Res. 18, 521-532 (2008).
122. Widschwendter, M. et al. Epigenetic stem cell signature in cancer. Nature Genet. 39, 157-158 (2007).
123. Ohm, J. E. et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nature Genet. 39, 237-242 (2007).
124. Wong, D. J. et al. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2, 333-344 (2008).
125. Knoepfler, P. S. et al. Myc influences global chromatin structure. EMBO J. 25, 2723-2734 (2006).
126. Cotterman, R. et al. N-Myc regulates a widespread euchromatic program in the human genome partially independent of its role as a classical transcription factor. Cancer Res. 68, 9654-9662 (2008).
127. Frye, M., Fisher, A. G. & Watt, F. M. Epidermal stem cells are defined by global histone modifications that are altered by Myc-induced differentiation. PLoS ONE 2, e763 (2007).
128. Kim, J. et al. A Myc Network Accounts for Similarities between Embryonic Stem and Cancer Cell Transcription Programs. Cell 143, 313-324 (2010).
129. Dialynas, G. K., Vitalini, M. W. & Wallrath, L. L. Linking Heterochromatin Protein 1 (HP 1) to cancer progression. Mutat. Res. 647, 13-20 (2008).
130. Hs° expression is associated with the metastatic phenotype in breast cancer. Cancer Res. 60, 3359-3363 (2000).
131. Tiwari, V. K. et al. PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biol. 6, 2911-2927 (2008).
132. Daley, G. Q. Common themes of dedifferentiation in somatic cell reprogramming and cancer. Cold Spring Harb. Symp. Quant. Biol. 73, 171-174 (2008).
133. Kim, J. K. et al. Srg3, a mouse homolog of yeast SWI3, is essential for early embryogenesis and involved in brain development. Mol. Cell Biol. 21, 7787-7795 (2001).
134. Klochendler-Yeivin, A. et al. The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Rep. 1, 500-506 (2000).
135. Shawlot, W., Deng, J. M., Fohn, L. E. & Behringer, R. R. Restricted (3-galactosidase expression of a hygromycin-lacZ gene targeted to the (3-actin locus and embryonic lethality of (3-actin mutant mice. Transgenic Res. 7, 95-103 (1998).
136. Marfella, C. G. A. et al. Mutation of the SNF2 family member Chd2 affects mouse development and survival. J. Cell Physiol. 209, 162-171 (2006).
137. Hurd, E. A. et al. Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues. Mamm. Genome 18, 94-104 (2007).
138. Nishiyama, M. et al. CHD8 suppresses p53-mediated apoptosis through histone H1 recruitment during early embryogenesis. Nature Cell Biol. 11, 172-182 (2009).
139. Marino, S. & Nusse, R. Mutants in the mouse NuRD/Mi2 component P66a are embryonic lethal. PLoS ONE 2, e519 (2007).
140. Hu, Y. et al. Homozygous disruption of the Tip60 gene causes early embryonic lethality. Dev. Dyn. 238, 2912-2921 (2009).
141. Tominaga, K. et al. MRG15 regulates embryonic development and cell proliferation. Mol. Cell Biol. 25, 2924-2937 (2005).
142. Herceg, Z. et al. Disruption of Trrap causes early embryonic lethality and defects in cell cycle progression. Nature Genet. 29, 206-211 (2001).