Histone variants: Key players of chromatin

Cell and Tissue Research

Volumn 356, Issue 3, 2014, Pages 457-466

  Biterge, Burcu ^a,b,c   Schneider, Robert ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Chromatin; Epigenetic regulation; Function; Histone variant; Transcription

Indexed keywords

CENTROMERE PROTEIN A; HISTONE; HISTONE DBIGH1; HISTONE H1; HISTONE H10; HISTONE H11; HISTONE H12; HISTONE H15; HISTONE H1OO; HISTONE H1T; HISTONE H1T2; HISTONE H1X; HISTONE H2AX; HISTONE H2AZ; HISTONE H33; HISTONE HILS1; MACROH2A; UNCLASSIFIED DRUG; CHROMATIN;

CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CENTROMERE; CHROMATIN; CHROMATIN STRUCTURE; DNA REPAIR; DNA REPLICATION; EPIGENETIC REPRESSION; HETEROCHROMATIN; HISTONE PHOSPHORYLATION; HUMAN; NONHUMAN; NUCLEOSOME; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REVIEW; TELOMERE; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

EUKARYOTA;

ANIMALS; CHROMATIN; DNA REPAIR; GENE EXPRESSION REGULATION; HISTONES; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSCRIPTION, GENETIC;

EID: 84902244816     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-1862-4     Document Type: Review

References (127)

1. Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9(6):1191-1200 (Pubitemid 34722299)
2. Albig W, Doenecke D (1997) The human histone gene cluster at the D6S105 locus. Hum Genet 101:284-294 (Pubitemid 28197522)
3. Amor DJ, Kalitsis P, Sumer H, Choo KH (2004) Building the centromere: fromfoundation proteins to 3D organization. Trends Cell Biol 14(7):359-368 (Pubitemid 38891705)
4. 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)
5. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8(5):532-538
6. Bailey AO, Panchenko T, Sathyan KM, Petkowski JJ, Pai PJ, Bai DL, Russell DH, Macara IG, Shabanowitz J, Hunt DF, Black BE, Foltz DR (2013) Posttranslational modification of CENP-A influences the conformation of centromeric chromatin. Proc Natl Acad Sci USA 110(29):11827-11832
7. Barrero MJ, Sesé B, Kuebler B, Bilic J, Boue S, Martí M, Izpisua Belomonte JC (2013) Macrohistone variants preserve cell identity by preventing the gain of H3K4me2 during reprogramming to pluripotency. Cell Rep S2211-1247, 105-8
8. Binda O, Sevilla A, LeRoy G, Lemischka IR, Garcia BA, Richard S (2013) SETD6 monomethylates H2AZ on lysine 7 and is required for the maintenance of embryonic stem cell self-renewal. Epigenetics 8(2):177-183
9. 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(10):1074-1079
10. Chadwick BP, Willard HF (2001) Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant. Hum Mol Genet 10(10):1101-1113 (Pubitemid 32447788)
11. 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)
12. Chakravarthy S, Luger K (2006) The histone variant macro-H2A preferentially forms "hybrid nucleosomes". J Biol Chem 281:25522-25531 (Pubitemid 44401941)
13. Chan KM, Fang D, Gan H, Hashizume R, Yu C, Schroeder M, Gupta N, Mueller S, James CD, Jenkins R, Sarkaria J, Zhang Z (2013) The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev 27(9):985-990
14. Changolkar LN, Pehrson JR (2002) Reconstitution of nucleosomes with histone macroH2A1.2. Biochemistry 41:179-184 (Pubitemid 34049393)
15. Chen P, Zhao J, Li G (2013a) Histone variants in development and diseases. J Genet Genomics 40(7):355-365
16. Chen P, Zhao J, Wang Y, Wang M, Long H, Liang D, Huang L, Wen Z, Li W, Li X, Feng H, Zhao H, Zhu P, Li M, Wang QF, Li G (2013b) H3.3 actively marks enhancers and primes gene transcription via opening higher-ordered chromatin. Genes Dev 27(19):2109-2124
17. Choi JK, Howe LJ (2009) Histone acetylation: truth of consequences? Biochem Cell Biol 87(1):139-150
18. Choo JH, Kim JD, Chung JH, Stubbs L, Kim J (2006) Allele-specific deposition of macroH2A1 in imprinting control regions. Hum Mol Genet 15:717-724 (Pubitemid 43264696)
19. Chowdhury D, Keogh MC, Ishii H, Peterson CL, Buratowski S, Lieberman J (2005) Gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol Cell 20:801-809 (Pubitemid 41740701)
20. Codomo CA, Furuyama T, Henikoff S (2014) CENP-A octamers do not confer a reduction in nucleosome height by AFM. Nat Struct Mol Biol 21(1):4-5
21. Cook PJ, Ju BG, Telese F, Wang X, Glass CK, Rosenfeld MG (2009) Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458:591-596
22. Corpet A, Olbrich T, Gwerder M, Fink D, Stucki M (2013) Dynamics of histone H3.3 deposition in proliferating and senescent cells reveals a DAXX-dependent targeting to PML-NBs important for pericentromeric heterochromatin organization. Cell Cycle 13(2)
23. Costanzi C, Pehrson JR (1998) Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393:599-601 (Pubitemid 28319252)
24. Creppe C, Janich P, Cantarino N, Noguera M, Valero V, Musulen E, Douet J, Posavec M, Martin-Caballero J, Sumoy L, Di Croce L, Benitah SA, Buschbeck M (2012) MacroH2A1 regulates the balance between self-renewal and differentiation commitment in embryonic and adult stem cells. Mol Cell Biol 32(8):1442-1452
25. Creyghton MP, Markoulaki S, Levine SS, Hanna J, Lodato MA, Sha K, Young RA, Jaenisch R, Boyer LA (2008) H2AZ is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment. Cell 135(4):649-661
26. Dalal Y, Wang H, Lindsay S, Henikoff S (2007) Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol 5(8):e218
27. Dimitriadis EK, Weber C, Gill RK, Diekmann S, Dalal Y (2010) Tetrameric organization of vertebrate centromeric nucleosomes. Proc Natl Acad Sci USA 107(47):20317-20322
28. Doenecke D, Drabent B, Bode C, Bramlage B, Franke K, Gavenis K, Kosciessa U, Witt O (1997) Histone gene expression and chromatin structure during spermatogenesis. Adv Exp Med Biol 424:37
29. Dominski Z, Marzluff WF (1999) Formation of the 3 end of histone mRNA. Gene 239:1-14
30. 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)
31. Drané P, Ouararhni K, Depaux A, Shuaib M, Hamiche A (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24:1253-1265
32. Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray-Gallet D, Nakamura Y, Daigo Y, Nakatani Y, Almouzni-Pettinotti G (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137(3):485-497
33. Elsässer SJ, Allis CD (2010) HIRA and Daxx constitute two independent histone H3.3-containing predeposition complexes. Cold Spring Harb Symp Quant Biol 75:27-34
34. Elsässer SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ (2012) DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 491(7425):560-565
35. Faast R, Thonglairoam V, Schulz TC, Beall J, Wells JR, Taylor H, Matthaei K, Rathjen PD, Tremethick DJ, Lyons I (2001) Histone variant H2A.Z is required for early mammalian development. Curr Biol 11(15):1183-1187 (Pubitemid 32722571)
36. Fan Y, Sirotkin A, Russel IRG, Ayala J, Skoultchi AI (2001) Individual somatic H1 subtypes are dispensable for mouse development even in mice lacking the H1(0) replacement subtype. Mol Cell Biol 21:7933-7943 (Pubitemid 33051786)
37. Fan Y, Nikitina T, Zhao J, Fleury TJ, Bhattacharyya R, Bouhassira EE, Stein A, Woodcock CL, Skoultchi AI (2005) Histone h1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123:1199-1212 (Pubitemid 41821779)
38. Ferbeyre G, de Stanchina E, Querido E, Baptiste N, Prives C, Lowe SW (2000) PML is induced by oncogenic ras and promotes premature senescence. Genes Dev 14:2015-2027 (Pubitemid 30637352)
39. Fink M, Imholz D, Thoma F (2007) Contribution of the serine 129 of histone H2A to chromatin structure. Mol Cell Biol 27:3589-3600 (Pubitemid 46726170)
40. Foltz DR, Jansen LET, Bailey AO, Yates JR, Bassett EA, Wood S, Black BE, Cleveland DW (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137:472-484
41. Funayama R, Saito M, Tanobe H, Ishikawa F (2006) Loss of linker histone H1 in cellular senescence. J Cell Biol 175:869-880 (Pubitemid 44969193)
42. Furuya M, Tanaka M, Teranishi T, Matsumoto K, Hosoi Y, Saeki K, Ishimoto H, Minegishi K, Iritani A, Yoshimura Y (2007) H1foo is indispensable for meiotic maturation of the mouse oocyte. J Reprod Dev 53(4):895-902 (Pubitemid 47397291)
43. 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
44. Gaspar-Maia A, Qadeer ZA, Hasson D, Ratnakumar K, Leu NA, Leroy G, Liu S, Costanzi C, Valle-Garcia D, Schaniel C, Lemischka I, Garcia B, Pehrson JR, Bernstein E (2013) MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nat Commun 4:1565
45. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang C, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D, Allis CD (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678-691
46. Goutte-Gattat D, Shuaib M, Ouararhni K, Gautier T, Skoufias DA, Hamiche A, Dimitrov S (2013) Phosphorylation of the CENP-A amino-terminus in mitotic centromeric chromatin is required for kinetochore function. Proc Natl Acad Sci USA 110(21):8579-8584
47. Greaves IK, Rangasamy D, Ridgway P, Tremethick DJ (2007) H2A.Z contributes to the unique 3D structure of the centromere. Proc Natl Acad Sci USA 104:e525-e530
48. Hake SB, Garcia BA, Kauer M, Baker SP, Shabanowitz J, Hunt DF, Allis CD (2005) Serine 31 phosphorylation of histone variant H3.3 is specific to regions bordering centromeres in metaphase chromosomes. Proc Natl Acad Sci USA 102(18):6344-6349 (Pubitemid 40617445)
49. Hake SB, Allis CD (2006) Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis". Proc Natl Acad Sci USA 103(17):6428-6435
50. Hake SB, Garcia BA, Duncan EM, Kauer M, Dellaire G, Shabanowitz J, Bazett-Jones DP, Allis CD, Hunt DF (2006) Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem 281(1):559-568 (Pubitemid 43671219)
51. Happel N, Schulze E, Doenecke D (2005) Characterization of human histone H1x. Biol Chem 386:541-551
52. Harshman SW, Young NL, Parthun MR, Freitas MA (2013) H1 histones: current perspectives and challenges. Nucleic Acids Res 41(21):9593-9609
53. Hasson D, Panchenko T, Salimian KJ, Salman MU, Sekulic N, Alonso A, Warburton PE, Black BE (2013) The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat Struct Mol Biol 20(6):687-695
54. Hayakawa K, Ohgane J, Tanaka S, Yagi S, Shiota K (2012) Oocyte-specific linker histone H1foo is an epigenomic modulator that decondenses chromatin and impairs pluripotency. Epigenetics 9:1029-1036
55. Hendzel MJ, Lever MA, Crawford E, Th'ng JP (2004) The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J Biol Chem 279(19):20028-20034 (Pubitemid 38623446)
56. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: Stable inheritance with rapidly evolving DNA. Science 293:1098-1102 (Pubitemid 32758083)
57. Heo K, Kim H, Choi SH, Choi J, Kim K, Gu J, Lieber MR, Yang AS, An W (2008) FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell 30(1):86-97 (Pubitemid 351470156)
58. Hill DA (2001) Influence of linker histone H1 on chromatin remodeling. Biochem Cell Biol 79:317-324
59. Hu Y, Chopra V, Chopra R, Locascio JJ, Liao Z, Ding H, Zheng B, Matson WR, Ferrante RJ, Rosas HD, Hersch SM, Scherzer CR (2011) Transcriptional modulator H2A histone family, member Y (H2AFY) marks Huntington disease activity in man and mouse. Proc Natl Acad Sci USA 108(41):17141-17146
60. Ivashkevich A, Redon CE, Nakamura AJ, Martin RF, Martin OA (2012) Use of the γ-H2AX assay to monitor DNA damage and repair in translational cancer research. Cancer Lett 327(1-2):123-133
61. Izzo A, Kamieniarz-Gdula K, Ramírez F, Noureen N, Kind J, Manke T, van Steensel B, Schneider R (2013) The genomic landscape of the somatic linker histone subtypes H1.1 to H1.5 in human cells. Cell Rep 3(6):2142-2154
62. Izzo A, Kamieniarz K, Schneider R (2008) The histone H1 family: specific members, specific functions? Biol Chem 389(4):333-343 (Pubitemid 351773907)
63. Jansen LET, Black BE, Foltz DR, Cleveland DW (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176:795-805 (Pubitemid 46425540)
64. Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K, Felsenfeld G (2009) H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet 41(8):941-945
65. Kamieniarz K, Izzo A, Dundr M, Tropberger P, Ozretic L, Kirfel J, Scheer E, Tropel P, Wisniewski JR, Tora L, Viville S, Buettner R, Schneider R (2012) A dual role of linker histone H1.4 Lys 34 acetylation in transcriptional activation. Genes Dev 26(8):797-802
66. 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 (2006) A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439:497-501 (Pubitemid 43152843)
67. Kouzarides T (2007) Chromatin modifications and their function. Cell 128(4):693-705
68. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication- independent chromatin assembly at telomeres. Proc Natl Acad Sci USA 107(32):14075-14080
69. Lewis PW, Müller MM, Koletsky MS, Cordero F, Lin S, Banaszynski LA, Garcia BA, Muir TW, Becher OJ, Allis CD (2013) Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340(6134):857-861
70. Li A, Yu Y, Lee SC, Ishibashi T, Lees-Miller SP, Ausió J (2010) Phosphorylation of histone H2A.X by DNA-dependent protein kinase is not affected by core histone acetylation, but it alters nucleosome stability and histone H1 binding. J Biol Chem 285(23):17778-17788
71. Li H, Kaminski MS, Li Y, Yildiz M, Ouillette P, Jones S, Fox H, Jacobi K, Saiya-Cork K, Bixby D, Lebovic D, Roulston D, Shedden K, Sabel M, Marentette L, Cimmino V, Chang AE, Malek SN. (2014) Mutations in linker histone genes HIST1H1 B, C, D and E, OCT2 (POU2F2), IRF8 and ARID1A underlying the pathogenesis of follicular lymphoma. Blood. [Epub ahead of print]
72. Li Z, Gadue P, Chen K, Jiao Y, Tuteja G, Schug J, Li W, Kaestner KH (2012) Foxa2 and H2A.Z mediate nucleosome depletion during embryonic stem cell differentiation. Cell 151(7):1608-1616
73. Liu X, Li B, Gorovsky MA (1996) Essential and nonessential histone H2A variants in Tetrahymena thermophila. Mol Cell Biol 16:4305-4311 (Pubitemid 26251232)
74. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389(6648):251-260 (Pubitemid 27406632)
75. Luk E, Ranjan A, Fitzgerald PC, Mizuguchi G, Huang Y, Wei D, Wu C (2010) Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome. Cell 143:725-736
76. Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10:882-891 (Pubitemid 37386096)
77. Martianov I, Brancorsini S, Catena R, Gansmuller A, Kotaja N, Parvinen M, Sassone-Corsi P, Davidson I (2005) Polar nuclear localization of H1T2, a histone H1 variant, required for spermatid elongation and DNA condensation during spermiogenesis. Proc Natl Acad Sci USA 102(8):2808-2813 (Pubitemid 40299874)
78. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ (2002) The human and mouse replication-dependent histone genes. Genomics 80(5):487-498 (Pubitemid 35333791)
79. Meneghini MD, Wu M, Madhani HD (2003) Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112:e725-e736
80. Miell MD, Fuller CJ, Guse A, Barysz HM, Downes A, Owen-Hughes T, Rappsilber J, Straight AF, Allshire RC (2013) CENP-A confers a reduction in height on octameric nucleosomes. Nat Struct Mol Biol 20(6):763-765
81. Misteli T, Gunjan A, Hock R, Bustin M, Brown DT (2000) Dynamic binding of histone H1 to chromatin in living cells. Nature 408:877-881 (Pubitemid 32016100)
82. Mito Y, Henikoff JG, Henikoff S (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37:1090-1097 (Pubitemid 41486661)
83. Mizusawa Y, Kuji N, Tanaka Y, Tanaka M, Ikeda E, Komatsu S, Kato S, Yoshimura Y (2010) Expression of human oocyte-specific linker histone protein and its incorporation into sperm chromatin during fertilization. Fertil Steril 93(4):1134-1141
84. Muthurajan UM, McBryant SJ, Lu X, Hansen JC, Luger K (2011) The linker region of macroH2A promotes self-association of nucleosomal arrays. J Biol Chem 286:23852-23864
85. Nekrasov M, Amrichova J, Parker BJ, Soboleva TA, Jack C, Williams R, Huttley GA, Tremethick DJ (2012) Histone H2A.Z inheritance during the cell cycle and its impact on promoter organization and dynamics. Nat Struct Mol Biol 19:e1076-e1083
86. Ng RK, Gurdon JB (2008) Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol 10:102-109
87. Padeganeh A, Ryan J, Boisvert J, Ladouceur AM, Dorn JF, Maddox PS (2013) Octameric CENP-A nucleosomes are present at human centromeres throughout the cell cycle. Curr Biol 23(9):764-769
88. Pandey NB, Chodchoy N, Liu TJ, Marzluff WF (1990) Introns in histone genes alter the distribution of 3 ends. Nucleic Acids Res 18:3161-3170
89. Papamichos-Chronakis M, Krebs JE, Peterson CL (2006) Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev 20:2437-2449 (Pubitemid 44320391)
90. Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL (2011) Global regulation of H2A.Z localization by the INO80 chromatinremodeling enzyme is essential for genome integrity. Cell 144:200-213
91. Pasque V, Gillich A, Garrett N, Gurdon JB (2011) Histone variant macroH2A confers resistance to nuclear reprogramming. EMBO J 30(12):2373-2387
92. Pérez-Montero S, Carbonell A, Morán T, Vaquero A, Azorín F (2013) The embryonic linker histone H1 variant of Drosophila, dBigH1, regulates zygotic genome activation. Dev Cell 26(6):578-590
93. Qiu JJ, Guo JJ, Lv TJ, Jin HY, Ding JX, Feng WW, Zhang Y, Hua KQ (2013) Prognostic value of centromere protein-A expression in patients with epithelial ovarian cancer. Tumour Biol 34(5):2971-2975
94. Rappa F, Greco A, Podrini C, Cappello F, Foti M, Bourgoin L, Peyrou M, Marino A, Scibetta N, Williams R, Mazzoccoli G, Federici M, Pazienza V, Vinciguerra M (2013) Immunopositivity for histone macroH2A1 isoforms marks steatosis-associated hepatocellular carcinoma. PLoS ONE 8(1):e54458
95. Rasmussen TP, Huang T, Mastrangelo MA, Loring J, Panning B, Jaenisch R (1999) Messenger RNAs encoding mouse histone macroH2A1 isoforms are expressed at similar levels in male and female cells and result from alternative splicing. Nucleic Acids Res 27(18):3685-3689 (Pubitemid 29435748)
96. Ratnakumar K, Duarte LF, LeRoy G, Hasson D, Smeets D, Vardabasso C, Bonisch C, Zeng T, Xiang B, Zhang DY, Li H, Wang X, Hake SB, Schermelleh L, Garcia BA, Bernstein E (2012) ATRX-mediated chromatin association of histone variant macroH2A1 regulates alpha-globin expression. Genes Dev 26:433-438
97. Robinson PJ, Rhodes D (2006) Structure of the '30 nm' chromatin fibre: a key role for the linker histone. Curr Opin Struct Biol 16:e336-e343
98. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA doublestranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858-5868 (Pubitemid 28124064)
99. Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905-916
100. Sancho M, Diani E, Beato M, Jordan A (2008) Depletion of human histone H1 variants uncovers specific roles in gene expression and cell growth. PLoS Genet 4(10):e1000227
101. Sato S, Takahashi S, Asamoto M, Nakanishi M, Wakita T, Ogura Y, Yatabe Y, Shirai T (2012) Histone H1 expression in human prostate cancer tissues and cell lines. Pathol Int 62(2):84-92
102. Schwartz BE, Ahmad K (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19(7):804-814
103. Schwartzentruber J, Korshunov A, Liu XY, Jones DT, Pfaff E et al (2012) Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482(7384):226-231
104. Singh N, Basnet H, Wiltshire TD, Mohammad DH, Thompson JR, Héroux A, Botuyan MV, Yaffe MB, Couch FJ, Rosenfeld MG, Mer G (2012) Dual recognition of phosphoserine and phosphotyrosine in histone variant H2A.X by DNA damage response protein MCPH1. Proc Natl Acad Sci USA 109(36):14381-14386
105. Skene PJ, Henikoff S (2013) Histone variants in pluripotency and disease. Development 140(12):2513-2524
106. 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(38):3423-3428
107. Stoldt S, Wenzel D, Schulze E, Doenecke D, Happel N (2007) G1 phase-dependent nucleolar accumulation of human histone H1x. Biol Cell 99(10):541-552 (Pubitemid 47543312)
108. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403(6765):41-45 (Pubitemid 30038513)
109. Suto RK, Clarkson MJ, Tremethick DJ, Luger K (2000) Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat Struct Biol 7:1121-1124
110. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116(1):51-61 (Pubitemid 38156183)
111. Tanaka H, Iguchi N, Isotani A, Kitamura K, Toyama Y, Matsuoka Y, Onishi M, Masai K, Maekawa M, Toshimori K, Okabe M, Nishimune Y (2005) HANP1/H1T2, a novel histone H1-like protein involved in nuclear formation and sperm fertility. Mol Cell Biol 25(16):7107-7119 (Pubitemid 41105908)
112. Terme JM, Sesé B, Millán-Ariño L, Mayor R, Izpisúa Belmonte JC, Barrero MJ, Jordan A (2011) Histone H1 variants are differentially expressed and incorporated into chromatin during differentiation and reprogramming to pluripotency. J Biol Chem 286(41):35347-35357
113. Thakar A, Gupta P, Ishibashi T, Finn R, Silva-Moreno B, Uchiyama S, Fukui K, Tomschik M, Ausio J, Zlatanova J (2009) H2A.Z and H3.3 histone variants affect nucleosome structure: biochemical and biophysical studies. Biochemistry 48(46):10852-10857
114. Th'ng JPH, Sung R, Ye M, Hendzel MJ (2005) H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. J Biol Chem 280:27809-27814 (Pubitemid 41076896)
115. Till S, Ladurner AG (2009) Sensing NAD metabolites through macro domains. Front Biosci 14:3246-3258
116. Turner BM (1993) Decoding the nucleosome. Cell 75(1):5-8
117. van Attikum H, Fritsch O, Gasser SM (2007) Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J 26:4113-4125 (Pubitemid 47462094)
118. van Daal A, Elgin SCR (1992) A histone variant, H2AvD, is essential in Drosophila melanogaster. Mol Biol Cell 3:593-602
119. Voullaire LE, Slater HR, Petrovic V, Choo KH (1993) A functional marker centromere with no detectable alpha-satellite, satellite III, or CENP-B protein: activation of a latent centromere? Am J Hum Genet 52(6):1153-1163 (Pubitemid 23311357)
120. Walkiewicz MP, Dimitriadis EK, Dalal Y (2014) CENP-A octamers do not confer a reduction in nucleosome height by AFM. Nat Struct Mol Biol 21(1):2-3
121. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191
122. Xiao A, Li H, Shechter D, Ahn SH, Fabrizio LA, Erdjument-Bromage H, Ishibe-Murakami S, Wang B, Tempst P, Hofmann K, Patel DJ, Elledge SJ, Allis CD (2009) WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457:57-62
123. Xu Y, Ayrapetov MK, Xu C, Gursoy-Yuzugullu O, Hu Y, Price BD (2012) Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol Cell 48(5):723-733
124. Yan W, Ma L, Burns KH, Matzuk MM (2003) HILS1 is a spermatid-specific linker histone H1-like protein implicated in chromatin remodeling during mammalian spermiogenesis. Proc Natl Acad Sci USA 100(18):10546-10551 (Pubitemid 37071915)
125. Yang JW, Pendon C, Yang J, Haywood N, Chand A, Brown WR (2000) Human mini-chromosomes with minimal centromeres. Hum Mol Genet 9:1891-1902 (Pubitemid 30608622)
126. Yoda K, Ando S, Morishita S, Houmura K, Hashimoto K, Takeyasu K, Okazaki T (2000) Human centromere protein A (CENP-A) can replace histone H3 in nucleosome reconstitution in vitro. Proc Natl Acad Sci USA 97:7266-7271 (Pubitemid 30431452)
127. Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456:125-129