Histone variant macroH2A confers resistance to nuclear reprogramming

EMBO Journal

Volumn 30, Issue 12, 2011, Pages 2373-2387

  Pasque, Vincent ^a,b   Gillich, Astrid ^a,b   Garrett, Nigel ^a,b   Gurdon, John B ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

epiblast stem cells; inactive X chromosome; macroH2A; nuclear reprogramming; Xenopus oocytes

Indexed keywords

HISTONE H2A; MACROHISTONE H2A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL NUCLEUS TRANSPLANTATION; CHROMOSOMAL INSTABILITY; ECTODERM; EMBRYO; EPIGENETICS; MOUSE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; STEM CELL; X CHROMOSOME INACTIVATION; XENOPUS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMOSOMAL INSTABILITY; FEMALE; FIBROBLASTS; GENETIC VARIATION; HISTONES; MALE; MICE; MICE, TRANSGENIC; NUCLEAR REPROGRAMMING; OOCYTES; PLURIPOTENT STEM CELLS; RNA, UNTRANSLATED; TRANSCRIPTION, GENETIC; X CHROMOSOME INACTIVATION; XENOPUS;

MAMMALIA;

EID: 79958815889     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.144     Document Type: Article

References (79)

1. Abbott DW, Chadwick BP, Thambirajah AA, Ausio J (2005) Beyond the Xi: macroH2A chromatin distribution and post-translational modification in an avian system. J Biol Chem 280: 16437-16445 (Pubitemid 40616774)
2. Agrelo R, Souabni A, Novatchkova M, Haslinger C, Leeb M, Komnenovic V, Kishimoto H, Gresh L, Kohwi-Shigematsu T, Kenner L, Wutz A (2009) SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev Cell 16: 507-516
3. Angelov D, Molla A, Perche PY, Hans F, Cote J, Khochbin S, Bouvet P, Dimitrov S (2003) The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. Mol Cell 11 : 1033-1041 (Pubitemid 36566324)
4. Bao S, Miyoshi N, Okamoto I, Jenuwein T, Heard E, Azim Surani M (2005) Initiation of epigenetic reprogramming of the X chromosome in somatic nuclei transplanted to a mouse oocyte. EMBO Rep 6: 748-754 (Pubitemid 43108697)
5. Bao S, Tang F, Li X, Hayashi K, Gillich A, Lao K, Surani MA (2009) Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature 461: 1292-1295
6. Barzily-Rokni M, Friedman N, Ron-Bigger S, Isaac S, Michlin D, Eden A (2011) Synergism between DNA methylation and macroH2A1 occupancy in epigenetic silencing of the tumor suppressor gene p16(CDKN2A). Nucleic Acids Res 39: 1326-1335
7. Biddle A, Simeoni I, Gurdon JB (2009) Xenopus oocytes reactivate muscle gene transcription in transplanted somatic nuclei independently of myogenic factors. Development 136: 2695-2703
8. Blewitt ME, Gendrel AV, Pang Z, Sparrow DB, Whitelaw N, Craig JM, Apedaile A, Hilton DJ, Dunwoodie SL, Brockdorff N, Kay GF, Whitelaw E (2008) SmcHD1, containing a structural-mainte-nance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat Genet 40: 663-669 (Pubitemid 351601224)
9. Brockdorff N (2002) X-chromosome inactivation: closing in on proteins that bind Xist RNA. Trends Genet 18: 352-358 (Pubitemid 34804447)
10. Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448: 191-195 (Pubitemid 47067373)
11. Buschbeck M, Di Croce L (2010) Approaching the molecular and physiological function of macroH2A variants. Epigenetics 5: 118-123
12. Buschbeck M, Uribesalgo I, Wibowo I, Rue P, Martin D, Gutierrez A, Morey L, Guigo R, Lopez-Schier H, Di Croce L (2009) The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nat Struct Mol Biol 16: 1074-1079
13. Byrne JA, Simonsson S, Western PS, Gurdon JB (2003) Nuclei of adult mammalian somatic cells are directly reprogrammed to oct-4 stem cell gene expression by amphibian oocytes. Curr Biol 13: 1206-1213 (Pubitemid 36872943)
14. Casas-Delucchi CS, Brero A, Rahn HP, Solovei I, Wutz A, Cremer T, Leonhardt H, Cardoso MC (2011) Histone acetylation controls the inactive X chromosome replication dynamics. Nat Commun 2: 222
15. Chakravarthy S, Gundimella SK, Caron C, Perche PY, Pehrson JR, Khochbin S, Luger K (2005) Structural characterization of the histone variant macroH2A. Mol Cell Biol 25: 7616-7624 (Pubitemid 41170123)
16. Chang CC, Gao S, Sung LY, Corry GN, Ma Y, Nagy ZP, Tian XC, Rasmussen TP (2010) Rapid elimination of the histone variant MacroH2A from somatic cell heterochromatin after nuclear transfer. Cell Reprogram 12: 43-53
17. Chang EY, Ferreira H, Somers J, Nusinow DA, Owen-Hughes T, Narlikar GJ (2008) MacroH2A allows ATP-dependent chromatin remodeling by SWI/SNF and ACF complexes but specifically reduces recruitment of SWI/SNF. Biochemistry 47: 13726-13732
18. Changolkar LN, Costanzi C, Leu NA, Chen D, McLaughlin KJ, Pehrson JR (2007) Developmental changes in histone macroH2A1-mediated gene regulation. Mol Cell Biol 27: 2758-2764 (Pubitemid 46581363)
19. Changolkar LN, Singh G, Cui K, Berletch JB, Zhao K, Disteche CM, Pehrson JR (2010) Genome-wide distribution of macroH2A1 histone variants in mouse liver chromatin. Mol Cell Biol 30: 5473-5483
20. Clemson CM, McNeil JA, Willard HF, Lawrence JB (1996) XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol 132: 259-275 (Pubitemid 26052564)
21. Costanzi C, Pehrson JR (1998) Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393: 599-601 (Pubitemid 28319252)
22. Csankovszki G, Nagy A, Jaenisch R (2001) Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation. J Cell Biol 153: 773-784
23. Csankovszki G, Panning B, Bates B, Pehrson JR, Jaenisch R (1999) Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat Genet 22: 323-324 (Pubitemid 29369518)
24. Dai B, Rasmussen TP (2007) Global epiproteomic signatures distinguish embryonic stem cells from differentiated cells. Stem Cell 25: 2567-2574 (Pubitemid 47582749)
25. de Napoles M, Mermoud JE, Wakao R, Tang YA, Endoh M, Appanah R, Nesterova TB, Silva J, Otte AP, Vidal M, Koseki H, Brockdorff N (2004) Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell 7: 663-676 (Pubitemid 39462687)
26. Doyen CM, An W, Angelov D, Bondarenko V, Mietton F, Studitsky VM, Hamiche A, Roeder RG, Bouvet P, Dimitrov S (2006) Mechanism of polymerase II transcription repression by the histone variant macroH2A. Mol Cell Biol 26: 1156-1164 (Pubitemid 43146506)
27. Eggan K (2000) X-chromosome inactivation in cloned mouse embryos. Science 290: 1578-1581
28. Eskeland R, Leeb M, Grimes GR, Kress C, Boyle S, Sproul D, Gilbert N, Fan Y, Skoultchi AI, Wutz A, Bickmore WA (2010) Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol Cell 38: 452-464
29. Gamble MJ, Frizzell KM, Yang C, Krishnakumar R, Kraus WL (2010) The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev 24: 21-32
30. Gaume X, Monier K, Argoul F, Mongelard F, Bouvet P (2011) In vivo study of the histone chaperone activity of nucleolin by FRAP. Biochem Res Int 2011: 187624
31. Gillich A, Hayashi K (2011) Switching stem cell state through programmed germ cell reprogramming. Differentiation (doi: 10.1016/j.diff.2011.1001.1003)
32. Guo G, Yang J, Nichols J, Hall JS, Eyres I, Mansfield W, Smith A (2009) Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136: 1063-1069
33. Gurdon JB (1968) Changes in somatic cell nuclei inserted into growing and maturing amphibian oocytes. J Embryol Exp Morphol 20: 401-414
34. Gurdon JB, Melton DA (2008) Nuclear reprogramming in cells. Science 322: 1811-1815
35. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458: 223-227
36. Hadjantonakis AK, Cox LL, Tam PP, Nagy A (2001) An X-linked GFP transgene reveals unexpected paternal X-chromosome activity in trophoblastic giant cells of the mouse placenta. Genesis 29: 133-140 (Pubitemid 32260227)
37. Ha?kelien AM, Delbarre E, Gaustad KG, Buendia B, Collas P (2008) Expression of the myodystrophic R453W mutation of lamin A in C2C12 myoblasts causes promoter-specific and global epigenetic defects. Exp Cell Res 314: 1869-1880
38. Hall LL, Byron M, Pageau G, Lawrence JB (2009) AURKB-mediated effects on chromatin regulate binding versus release of XIST RNA to the inactive chromosome. J Cell Biol 186: 491-507
39. Halley-Stott RP, Pasque V, Astrand C, Miyamoto K, Simeoni I, Jullien J, Gurdon JB (2010) Mammalian nuclear transplantation to germinal vesicle stage Xenopus oocytes-a method for quantitative transcriptional reprogramming. Methods 51 : 56-65
40. Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Tsutui K, Nakagawa S (2010) The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev Cell 19: 469-476
41. Hayashi K, Lopes S, Tang F, Surani M (2008) Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3: 391-401
42. Hayashi K, Surani MA (2009) Self-renewing epiblast stem cells exhibit continual delineation of germ cells with epigenetic repro-gramming in vitro. Development 136: 3549-3556
43. Heard E, Disteche CM (2006) Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 20: 1848-1867 (Pubitemid 44079323)
44. Hernández-Muñoz I, Lund AH, van der Stoop P, Boutsma E, Muijrers I, Verhoeven E, Nusinow DA, Panning B, Marahrens Y, van Lohuizen M (2005) Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc Natl Acad Sci USA 102: 7635-7640 (Pubitemid 40741023)
45. Huynh KD, Lee JT (2003) Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature 426: 857-862 (Pubitemid 38056873)
46. Inoue K, Kohda T, Sugimoto M, Sado T, Ogonuki N, Matoba S, Shiura H, Ikeda R, Mochida K, Fujii T, Sawai K, Otte AP, Tian XC, Yang X, Ishino F, Abe K, Ogura A (2010) Impeding Xist expression from the active X chromosome improves mouse somatic cell nuclear transfer. Science 330: 496-499
47. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19: 187-191 (Pubitemid 28248804)
48. Jullien J, Astrand C, Halley-Stott RP, Garrett N, Gurdon JB (2010) Characterization of somatic cell nuclear reprogramming by oo-cytes in which a linker histone is required for pluripotency gene reactivation. Proc Natl Acad Sci USA 107 : 5483-5488
49. Kalantry S, Mills KC, Yee D, Otte AP, Panning B, Magnuson T (2006) The Polycomb group protein Eed protects the inactive X-chromo-some from differentiation-induced reactivation. Nat Cell Biol 8: 195-202
50. Kapoor A, Goldberg MS, Cumberland LK, Ratnakumar K, Segura MF, Emanuel PO, Menendez S, Vardabasso C, Leroy G, Vidal CI, Polsky D, Osman I, Garcia BA, Hernando E, Bernstein E (2010) The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature 468: 1105-1109
51. Kloc M, Spohr G, Etkin LD (1993) Translocation of repetitive RNA sequences with the germ plasm in Xenopus oocytes. Science 262: 1712-1714 (Pubitemid 24030090)
52. Kohlmaier A, Savarese F, Lachner M, Martens J, Jenuwein T, Wutz A (2004) A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol 2: E171
53. Koziol MJ, Rinn JL (2010) RNA traffic control of chromatin complexes. Curr Opin Genet Dev 20: 142-148
54. Leeb M, Steffen PA, Wutz A (2009) X chromosome inactivation sparked by non-coding RNAs. RNA Biol 6: 94-99
55. Leeb M, Wutz A (2007) Ring1B is crucial for the regulation of developmental control genes and PRC1 proteins but not X inactivation in embryonic cells. J Cell Biol 178: 219-229 (Pubitemid 47076459)
56. Lyon MF (1961) Gene action in the X-chromosome of the mouse Mus musculus L. Nature 190: 372-373
57. Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K, Stadtfeld M, Yachechko R, Tchieu J, Jaenisch R (2007) Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 1: 55-70
58. Mietton F, Sengupta AK, Molla A, Picchi G, Barral S, Heliot L, Grange T, Wutz A, Dimitrov S (2009) Weak, but uniform enrichment of the histone variant macroH2A1 along the inactive X chromosome. Mol Cell Biol 29: 150-156
59. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, Schorderet P, Bernstein BE, Jaenisch R, Lander ES, Meissner A (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454: 794
60. Murata K, Kouzarides T, Bannister AJ, Gurdon JB (2010) Histone H3 lysine 4 methylation is associated with the transcriptional repro-gramming efficiency of somatic nuclei by oocytes. Epigenetics Chromatin 3: 4
61. Nashun B, Yukawa M, Liu H, Akiyama T, Aoki F (2010) Changes in the nuclear deposition of histone H2A variants during pre-implantation development in mice. Development 137: 3785-3794
62. Nolen LD, Gao S, Han Z, Mann MR, Gie Chung Y, Otte AP, Bartolomei MS, Latham KE (2005) X chromosome reactivation and regulation in cloned embryos. Dev Biol 279: 525-540 (Pubitemid 40298756)
63. Panning B (2004) X inactivation in mouse ES cells: histone modifications and FISH. Meth Enzymol 376: 419-428 (Pubitemid 38200195)
64. Pasque V, Miyamoto K, Gurdon JB (2010) Efficiencies and mechanisms of nuclear reprogramming. Cold Spring Harb Symp Quant Biol (advance online publication 3 November 2010; doi: 2010. 1101/sqb.2010.2075.2002)
65. Payer B, Lee JT (2008) X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 42: 733-772
66. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300: 131-135 (Pubitemid 36423045)
67. Plath K, Talbot D, Hamer KM, Otte AP, Yang TP, Jaenisch R, Panning B (2004) Developmentally regulated alterations in Polycomb repressive complex 1 proteins on the inactive X chromosome. J Cell Biol 167: 1025-1035 (Pubitemid 40066619)
68. Rasmussen TP, Mastrangelo MA, Eden A, Pehrson JR, Jaenisch R (2000) Dynamic relocalization of histone MacroH2A1 from cen-trosomes to inactive X chromosomes during X inactivation. J Cell Biol 150: 1189-1198
69. Rasmussen TP, Wutz AP, Pehrson JR, Jaenisch RR (2001) Expression of Xist RNA is sufficient to initiate macrochromatin body formation. Chromosoma 11 0 : 411-420 (Pubitemid 33123218)
70. Rougeulle C, Chaumeil J, Sarma K, Allis CD, Reinberg D, Avner P, Heard E (2004) Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol Cell Biol 24: 5475-5484 (Pubitemid 38738179)
71. Sado T, Fenner MH, Tan SS, Tam P, Shioda T, Li E (2000) X inactivation in the mouse embryo deficient for Dnmt1: distinct effect of hypomethylation on imprinted and random X inactiva-tion. Dev Biol 225: 294-303
72. Silva J, Mak W, Zvetkova I, Appanah R, Nesterova TB, Webster Z, Peters AH, Jenuwein T, Otte AP, Brockdorff N (2003) Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 poly-comb group complexes. Dev Cell 4: 481-495 (Pubitemid 36437556)
73. Simonsson S, Gurdon J (2004) DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat Cell Biol 6: 984-990 (Pubitemid 39359851)
74. Sporn JC, Kustatscher G, Hothorn T, Collado M, Serrano M, Muley T, Schnabel P, Ladurner AG (2009) Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene 28: 3423-3428
75. Takagi N, Yoshida MA, Sugawara O, Sasaki M (1983) Reversal of X-inactivation in female mouse somatic cells hybridized with murine teratocarcinoma stem cells in vitro. Cell 34: 1053-1062 (Pubitemid 13023369)
76. Tanaka S (2006) Derivation and culture of mouse trophoblast stem cells in vitro. Methods Mol Biol 329: 35-44
77. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RD (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448: 196-199 (Pubitemid 47067378)
78. Wutz A, Jaenisch R (2000) A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol Cell 5: 695-705
79. Wutz A, Rasmussen TP, Jaenisch R (2002) Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 30: 167-174