Histone variants: the artists of eukaryotic chromatin

Science China Life Sciences

Volumn 58, Issue 3, 2015, Pages 232-239

  Li, Min ^a   Fang, YuDa ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

DNA repair; gene regulation; histone modification; histone variants; stress responsiveness

Indexed keywords

CHROMATIN; HISTONE;

CHROMATIN; DNA DAMAGE; DNA REPAIR; EUKARYOTIC CELL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; PLANT;

CHROMATIN; DNA DAMAGE; DNA REPAIR; EUKARYOTIC CELLS; GENE EXPRESSION REGULATION; HISTONES; PLANTS; TRANSCRIPTION, GENETIC;

EID: 84939995174     PISSN: 16747305     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11427-015-4817-4     Document Type: Review

References (123)

1. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell, 2004, 116: 259–272
2. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature, 1997, 389: 251–260
3. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell, 2007, 128: 707–719
4. Talbert PB, Henikoff S. Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol, 2010, 11: 264–275
5. Malik HS, Henikoff S. Phylogenomics of the nucleosome. Nat Struct Biol, 2003, 10: 882–891
6. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ. The human and mouse replication-dependent histone genes. Genomics, 2002, 80: 487–498
7. Okada T, Endo M, Singh MB, Bhalla PL. Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J, 2005, 44: 557–568
8. Henikoff S, Furuyama T, Ahmad K. Histone variants, nucleosome assembly and epigenetic inheritance. Trends Genet, 2004, 20: 320–326
9. Jenuwein T, Allis CD. Translating the histone code. Science, 2001, 293: 1074–1080
10. Escargueil AE, Soares DG, Salvador M, Larsen AK, Henriques JAP. What histone code for DNA repair? Mutat Res Rev Mut Res, 2008, 658: 259–270
11. Talbert PB, Ahmad K, Almouzni G, Ausio J, Berger F, Bhalla PL, Bonner WM, Cande WZ, Chadwick BP, Chan SWL, Cross GAM, Cui LW, Dimitrov SI, Doenecke D, Eirin-Lopez JM, Gorovsky MA, Hake SB, Hamkalo BA, Holec S, Jacobsen SE, Kamieniarz K, Khochbin S, Ladurner AG, Landsman D, Latham JA, Loppin B, Malik HS, Marzluff WF, Pehrson JR, Postberg J, Schneider R, Singh MB, Smith MM, Thompson E, Torres-Padilla ME, Tremethick DJ, Turner BM, Waterborg JH, Wollmann H, Yelagandula R, Zhu B, Henikoff S. A unified phylogeny-based nomenclature for histone variants. Epigenet Chromat, 2012, 5: 1756–8935
12. Wu RS, Nishioka D, Bonner WM. Differential conservation of histone 2A variants between mammals and sea urchins. J Cell Biol, 1982, 93: 426–431
13. Thatcher TH, Gorovsky MA. Phylogenetic analysis of the core histones H2A, H2B, H3, and H4. Nucleic Acids Res, 1994, 22: 174–179
14. Bernstein E, Hake SB. The nucleosome: a little variation goes a long way. Biochem Cell Biol, 2006, 84: 505–517
15. Lindsey GG, Orgeig S, Thompson P, Davies N, Maeder DL. Extended C-terminal tail of wheat histone H2A interacts with DNA of the “linker” region. J Mol Biol, 1991, 218: 805–813
16. Huh GH, Matsuura Y, Meshi T, Iwabuchi M. Differential expression of the two types of histone H2A genes in wheat. Biochim Biophys Acta, 1995, 1261: 155–160
17. Yelagandula R, Stroud H, Holec S, Zhou K, Feng SH, Zhong XH, Muthurajan UM, Nie X, Kawashima T, Groth M, Luger K, Jacobsen SE, Berger F. The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell, 2014, 158: 98–109
18. van Daal A, White EM, Elgin SC, Gorovsky MA. Conservation of intron position indicates separation of major and variant H2As is an early event in the evolution of eukaryotes. J Mol Evol, 1990, 30: 449–455
19. Suto RK, Clarkson MJ, Tremethick DJ, Luger K. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat Struct Biol, 2000, 7: 1121–1124
20. Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W. Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev, 2002, 12: 162–169
21. Mannironi C, Bonner WM, Hatch CL. H2A.X. a histone isoprotein with a conserved C-terminal sequence, is encoded by a novel mRNA with both DNA replication type and polyA 3′ processing signals. Nucleic Acids Res, 1989, 17: 9113–9126
22. van Attikum H, Gasser SM. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol, 2009, 19: 207–217
23. Raisner RM, Madhani HD. Patterning chromatin: form and function for H2A.Z variant nucleosomes. Curr Opin Genet Dev, 2006, 16: 119–124
24. Guillemette B, Bataille AR, Gevry N, Adam M, Blanchette M, Robert F, Gaudreau L. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol, 2005, 3: 2100–2110
25. Li B, Pattenden SG, Lee D, Gutierrez J, Chen J, Seidel C, Gerton J, Workman JL. Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling. Proc Natl Acad Sci USA, 2005, 102: 18385–18390
26. Mavrich TN, Jiang CZ, Ioshikhes IP, Li XY, Venters BJ, Zanton SJ, Tomsho LP, Qi J, Glaser RL, Schuster SC, Gilmour DS, Albert I, Pugh BF. Nucleosome organization in the Drosophila genome. Nature, 2008, 453: 358–362
27. Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature, 2008, 456: 125–129
28. Coleman-Derr D, Zilberman D. DNA methylation, H2A.Z, and the regulation of constitutive expression. Cold Spring Harb Symp Quant Biol, 2012, 77: 147–154
29. Suto RK, Clarkson MJ, Tremethick DJ, Luger K. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat Struct Biol, 2000, 7: 1121–1124
30. Krogan NJ, Keogh MC, Datta N, Sawa C, Ryan OW, Ding H, Haw RA, Pootoolal J, Tong A, Canadien V, Richards DP, Wu X, Emili A, Hughes TR, Buratowski S, Greenblatt JF. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell, 2003, 12: 1565–1576
31. Cai Y, Jin JJ, Florens L, Swanson SK, Kusch T, Li B, Workman JL, Washburn MP, Conaway RC, Conaway JW. The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J Biol Chem, 2005, 280: 13665–13670
32. Mizuguchi G, Shen XT, Landry J, Wu WH, Sen S, Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science, 2004, 303: 343–348
33. Martin-Trillo M, Larazo A, Poethig RS, Gomez-Mena C, Pineiro MA, Martinez-Zapater JM, Jarillo JA. EARLY IN SHORT DAYS 1 (ESD1) encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a putative component of chromatin remodelling complexes that positively regulates FLC accumulation in Arabidopsis. Development, 2006, 133: 1241–1252
34. Noh YS, Amasino RM. PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell, 2003, 15: 1671–1682
35. March-Diaz R, Garcia-Dominguez M, Florencio FJ, Reyes JC. SEF, a new protein required for flowering repression in Arabidopsis, interacts with PIE1 and ARP6. Plant Physiol, 2007, 143: 893–901
36. Shi L, Wang J, Hong F, Spector DL, Fang Y. Four amino acids guide the assembly or disassembly of Arabidopsis histone H3.3-containing nucleosomes. Proc Natl Acad Sci USA, 2011, 108: 10574–10578
37. Ahmad K, Henikoff S. Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci USA, 2002, 99: 16477–16484
38. Gendler K, Paulsen T, Napoli C. ChromDB: The chromatin database. Nucleic Acids Res, 2008, 36: D298–302
39. Bonnefoy E, Orsi GA, Couble P, Loppin B. The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization. PLoS Genet, 2007, 3: 1991–2006
40. Sawatsubashi S, Murata T, Lim J, Fujiki R, Ito S, Suzuki E, Tanabe M, Zhao Y, Kimura S, Fujiyama S, Ueda T, Umetsu D, Ito T, Takeyama K, Kato S. A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev, 2010, 24: 159–170
41. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo XY, Li X, Wen DC, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang CW, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng DY, Allis CD. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell, 2010, 140: 678–691
42. Sullivan KF, Hechenberger M, Masri K. Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol, 1994, 127: 581–592
43. Malik HS, Henikoff S. Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics, 2001, 157: 1293–1298
44. Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell, 2002, 14: 1053–1066
45. Ravi M, Shibata F, Ramahi JS, Nagaki K, Chen CB, Murata M, Chan SWL. Meiosis-specific loading of the centromere-specific histone CENH3 in Arabidopsis thaliana. PLoS Genet, 2011, 7: e1002121
46. Ravi M, Kwong PN, Menorca RMG, Valencia JT, Ramahi JS, Stewart JL, Tran RK, Sundaresan V, Comai L, Chan SWL. The rapidly evolving centromere-specific histone has stringent functional requirements in Arabidopsis thaliana. Genetics, 2010, 186: 461–471
47. Ravi M, Chan SWL. Haploid plants produced by centromere-mediated genome elimination. Nature, 2010, 464: 615–618
48. Seymour DK, Filiault DL, Henry IM, Monson-Miller J, Ravi M, Pang AD, Comai L, Chan SWL, Maloof JN. Rapid creation of Arabidopsis doubled haploid lines for quantitative trait locus mapping. Proc Natl Acad Sci USA, 2012, 109: 4227–4232
49. Wijnker E, van Dun K, de Snoo CB, Lelivelt CLC, Keurentjes JJB, Naharudin NS, Ravi M, Chan SWL, de Jong H, Dirks R. Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nat Genet, 2012, 44: 467–470
50. Cui B, Liu Y, Gorovsky MA. Deposition and function of histone H3 variants in Tetrahymena thermophila. Mol Cell Biol, 2006, 26: 7719–7730
51. Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M. A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev, 1995, 9: 573–586
52. Moore LL, Morrison M, Roth MB. HCP-1, a protein involved in chromosome segregation, is localized to the centromere of mitotic chromosomes in Caenorhabditis elegans. J Cell Biol, 1999, 147: 471–480
53. Earnshaw WC, Rothfield N. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma, 1985, 91: 313–321
54. Fang Y, Spector DL. Centromere positioning and dynamics in living Arabidopsis plants. Mol Biol Cell, 2005, 16: 5710–5718
55. Shuaib M, Ouararhni K, Dimitrov S, Hamiche A. HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres. Proc Natl Acad Sci USA, 2010, 107: 1349–1354
56. Muller S, de Oca RM, Lacoste N, Dingli F, Loew D, Almouzni G. Phosphorylation and DNA binding of HJURP determine its centromeric recruitment and function in CenH3 (CENP-A) loading. Cell Rep, 2014, 8: 190–203
57. Lever MA, Th’ng JPH, Sun XJ, Hendzel MJ. Rapid exchange of histone H1.1 on chromatin in living human cells. Nature, 2000, 408: 873–876
58. Misteli T, Gunjan A, Hock R, Bustin M, Brown DT. Dynamic binding of histone H1 to chromatin in living cells. Nature, 2000, 408: 877–881
59. Ushinsky SC, Bussey H, Ahmed AA, Wang Y, Friesen J, Williams BA, Storms RK. Histone H1 in Saccharomyces cerevisiae. Yeast, 1997, 13: 151–161
60. Patterton HG, Landel CC, Landsman D, Peterson CL, Simpson RT. The biochemical and phenotypic characterization of Hho1p, the putative linker histone H1 of Saccharomyces cerevisiae. J Biol Chem, 1998, 273: 7268–7276
61. Li CH, Mueller JE, Elfline M, Bryk M. Linker histone H1 represses recombination at the ribosomal DNA locus in the budding yeast Saccharomyces cerevisiae. Mol Microbiol, 2008, 67: 906–919
62. Hashimoto H, Takami Y, Sonoda E, Iwasaki T, Iwano H, Tachibana M, Takeda S, Nakayama T, Kimura H, Shinkai Y. Histone H1 null vertebrate cells exhibit altered nucleosome architecture. Nucleic Acids Res, 2010, 38: 3533–3545
63. Fan Y, Nikitina T, Morin-Kensicki EM, Zhao J, Magnuson TR, Woodcock CL, Skoultchi AI. H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol Cell Biol, 2003, 23: 4559–4572
64. Wierzbicki AT, Jerzmanowski A. Suppression of histone H1 genes in Arabidopsis results in heritable developmental defects and stochastic changes in DNA methylation. Genetics, 2005, 169: 997–1008
65. Rea M, Zheng W, Chen M, Braud C, Bhangu D, Rognan TN, Xiao W. Histone H1 affects gene imprinting and DNA methylation in Arabidopsis. Plant J, 2012, 71: 776–786
66. Ingouff M, Hamamura Y, GourgueS M, Higashiyama T, Berger F. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol, 2007, 17: 1032–1037
67. Ingouff M, Rademacher S, Holec S, Soljlc L, Xin N, Readshaw A, Foo SH, Lahouze B, Sprunck S, Berger F. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogram-ming in Arabidopsis. Curr Biol, 2010, 20: 2137–2143
68. van der Heijden GW, Dieker JW, Derijck AAHA, Muller S, Berden JHM, Braat DDM, van der Vlag J, de Boer P. Asymmetry in Histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev, 2005, 122: 1008–1022
69. Callaini G, Riparbelli MG. Fertilization in Drosophila melanogaster: centrosome inheritance and organization of the first mitotic spindle. Dev Biol, 1996, 176: 199–208
70. Montellier E, Boussouar F, Rousseaux S, Zhang K, Buchou T, Fenaille F, Shiota H, Debernardi A, Hery P, Curtet S, Jamshidikia M, Barral S, Holota H, Bergon A, Lopez F, Guardiola P, Pernet K, Imbert J, Petosa C, Tan MJ, Zhao YM, Gerard M, Khochbin S. Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev, 2013, 27: 1680–1692
71. Allis CD, Glover CV, Bowen JK, Gorovsky MA. Histone variants specific to the transcriptionally active, amitotically dividing macronucleus of the unicellular eucaryote, Tetrahymena thermophila. Cell, 1980, 20: 609–617
72. Santisteban MS, Kalashnikova T, Smith MM. Histone H2A.Z regulates transcription and is partially redundant with nucleosome remodeling complexes. Cell, 2000, 103: 411–422
73. Adam M, Robert F, Larochelle M, Gaudreau L. H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol Cell Biol, 2001, 21: 6270–6279
74. Meneghini MD, Wu M, Madhani HD. Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell, 2003, 112: 725–736
75. Hardy S, Jacques PE, Gevry N, Forest A, Fortin ME, Laflamme L, Gaudreau L, Robert F. The euchromatic and heterochromatic landscapes are shaped by antagonizing effects of transcription on H2A.Z deposition. PLoS Genet, 2009, 5: e1000687
76. Santisteban MS, Hang MD, Smith MM. Histone variant H2A.Z and RNA polymerase II transcription elongation. Mol Cell Biol, 2011, 31: 1848–1860
77. Swaminathan J, Baxter EM, Corces VG. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev, 2005, 19: 65–76
78. Dhillon N, Kamakaka RT. A histone variant, Htz1p, and a Sir1p-like protein, Esc2p, mediate silencing at HMR. Mol Cell, 2000, 6: 769–780
79. Fan JY, Rangasamy D, Luger K, Tremethick DJ. H2A.Z alters the nucleosome surface to promote HP1 alpha-mediated chromatin fiber folding. Mol Cell, 2004, 16: 655–661
80. Leach TJ, Mazzeo M, Chotkowski HL, Madigan JP, Wotring MG, Glaser RL. Histone H2A.Z is widely but nonrandomly distributed in chromosomes of Drosophila melanogaster. J Biol Chem, 2000, 275: 23267–23272
81. Raisner RM, Hartley PD, Meneghini MD, Bao MZ, Liu CL, Schreiber SL, Rando OJ, Madhani HD. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell, 2008, 134: 188–188
82. Barski A, Cuddapah S, Cui KR, Roh TY, Schones DE, Wang ZB, Wei G, Chepelev I, Zhao KJ. High-resolution profiling of histone methylations in the human genome. Cell, 2007, 129: 823–837
83. Fan JY, Gordon F, Luger K, Hansen JC, Tremethick DJ. The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states. Nat Struct Biol, 2002, 9: 172–176
84. Coleman-Derr D, Zilberman D. Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet, 2012, 8: e1002988
85. Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, Rando OJ. Dynamics of replication-independent histone turnover in budding yeast. Science, 2007, 315: 1405–1408
86. Rufiange A, Jacques PE, Bhat W, Robert F, Nourani A. Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3K56 acetylation and Asf1. Mol Cell, 2007, 27: 393–405
87. Mito Y, Henikoff JG, Henikoff S. Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet, 2005, 37: 1090–1097
88. Stroud H, Otero S, Desvoyes B, Ramirez-Parra E, Jacobsen SE, Gutierrez C. Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc Natl Acad Sci USA, 2012, 109: 5370–5375
89. Kraushaar DC, Jin WF, Maunakea A, Abraham B, Ha M, Zhao KJ. Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol, 2013, 14: R121
90. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem, 1998, 273: 5858–5868
91. Stiff T, O’Driscoll M, Rief N, Iwabuchi K, Lobrich M, Jeggo PA. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res, 2004, 64: 2390–2396
92. Stiff T, Walker SA, Cerosaletti K, Goodarzi AA, Petermann E, Concannon P, O’Driscoll M, Jeggo PA. ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J, 2006, 25: 5775–5782
93. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, Pommier Y. GammaH2AX and cancer. Nat Rev Cancer, 2008, 8: 957–967
94. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell, 2005, 123: 1213–1226
95. Wu L, Luo K, Lou Z, Chen J. MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc Natl Acad Sci USA, 2008, 105: 11200–11205
96. Melander F, Bekker-Jensen S, Falck J, Bartek J, Mailand N, Lukas J. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J Cell Biol, 2008, 181: 213–226
97. Lou Z, Minter-Dykhouse K, Franco S, Gostissa M, Rivera MA, Celeste A, Manis JP, van Deursen J, Nussenzweig A, Paull TT, Alt FW, Chen J. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol Cell, 2006, 21: 187–200
98. van Attikum H, Fritsch O, Hohn B, Gasser SM. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell, 2004, 119: 777–788
99. van Attikum H, Fritsch O, Gasser SM. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J, 2007, 26: 4113–4125
100. Ikura T, Tashiro S, Kakino A, Shima H, Jacob N, Amunugama R, Yoder K, Izumi S, Kuraoka I, Tanaka K, Kimura H, Ikura M, Nishikubo S, Ito T, Muto A, Miyagawa K, Takeda S, Fishel R, Igarashi K, Kamiya K. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol Cell Biol, 2007, 27: 7028–7040
101. Nazarov IB, Smirnova AN, Krutilina RI, Svetlova MP, Solovjeva LV, Nikiforov AA, Oei SL, Zalenskaya IA, Yau PM, Bradbury EM, Tomilin NV. Dephosphorylation of histone gamma-H2AX during repair of DNA double-strand breaks in mammalian cells and its inhibition by calyculin A. Radiat Res, 2003, 160: 309–317
102. Keogh MC, Kim JA, Downey M, Fillingham J, Chowdhury D, Harrison JC, Onishi M, Datta N, Galicia S, Emili A, Lieberman J, Shen X, Buratowski S, Haber JE, Durocher D, Greenblatt JF, Krogan NJ. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature, 2006, 439: 497–501
103. Chowdhury D, Keogh MC, Ishii H, Peterson CL, Buratowski S, Lieberman J. gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol Cell, 2005, 20: 801–809
104. Tsukuda T, Fleming AB, Nickoloff JA, Osley MA. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature, 2005, 438: 379–383
105. Berkovich E, Monnat RJ, Jr., Kastan MB. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat Cell Biol, 2007, 9: 683–690
106. Heo K, Kim H, Choi SH, Choi J, Kim K, Gu J, Lieber MR, Yang AS, An W. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell, 2008, 30: 86–97
107. Xu Y, Ayrapetov MK, Xu C, Gursoy-Yuzugullu O, Hu Y, Price BD. Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol Cell, 2012, 48: 723–733
108. Xu Y, Sun Y, Jiang X, Ayrapetov MK, Moskwa P, Yang S, Weinstock DM, Price BD. The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J Cell Biol, 2010, 191: 31–43
109. Sun Y, Jiang X, Xu Y, Ayrapetov MK, Moreau LA, Whetstine JR, Price BD. Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat Cell Biol, 2009, 11: 1376–1382
110. Murr R, Loizou JI, Yang YG, Cuenin C, Li H, Wang ZQ, Herceg Z. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol, 2006, 8: 91–99
111. Pierce AJ, Jasin M. Measuring recombination proficiency in mouse embryonic stem cells. Methods Mol Biol, 2005, 291: 373–384
112. Vermeulen M, Timmers HTM. Grasping trimethylation of histone H3 at lysine 4. Epigenomics, 2010, 2: 395–406
113. Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL. Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell, 2011, 144: 200–213
114. Kumar SV, Wigge PA. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell, 2010, 140: 136–147
115. Smith AP, Jain A, Deal RB, Nagarajan VK, Poling MD, Raghothama KG, Meagher RB. Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol, 2010, 152: 217–225
116. March-Diaz R, Garcia-Dominguez M, Lozano-Juste J, Leon J, Florencio FJ, Reyes JC. Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J, 2008, 53: 475–487
117. Tamada Y, Yun JY, Woo SC, Amasino RM. ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell, 2009, 21: 3257–3269
118. Lazaro A, Gomez-Zambrano A, Lopez-Gonzalez L, Pineiro M, Jarillo JA. Mutations in the Arabidopsis SWC6 gene, encoding a component of the SWR1 chromatin remodelling complex, accelerate flowering time and alter leaf and flower development. J Exp Bot, 2008, 59: 653–666
119. Deal RB, Topp CN, McKinney EC, Meagher RB. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell, 2007, 19: 74–83
120. He YH. Control of the transition to flowering by chromatin modifications. Mol Plant, 2009, 2: 554–564
121. March-Diaz R, Reyes JC. The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Mol Plant, 2009, 2: 565–577
122. Qin Y, Zhao L, Skaggs MI, Andreuzza S, Tsukamoto T, Panoli A, Wallace KN, Smith S, Siddiqi I, Yang Z, Yadegari R, Palanivelu R. ACTIN-RELATED PROTEIN6 regulates female meiosis by modulating meiotic gene expression in Arabidopsis. Plant Cell, 2014, 26: 1612–1628
123. Shu H, Nakamura M, Siretskiy A, Borghi L, Moraes I, Wildhaber T, Gruissem W, Hennig L. Arabidopsis replacement histone variant H3.3 occupies promoters of regulated genes. Genome Biol, 2014, 15: 2014–2015