REVIEW

Histone variants: making structurally and functionally divergent nucleosomes and linkers in chromatin

  • Leilei SHI ,
  • Yuda FANG
Expand
  • National Key Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China

Received date: 07 Dec 2010

Accepted date: 23 Dec 2010

Published date: 01 Apr 2011

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

Abstract

In addition to the post-translational modifications of histone proteins, emerging literature suggests that the mosaic nucleosomes formed by incorporation of various histone variants provide another mechanism for modifying chromatin structure and function. The locally defined chromatin by histone variants is involved in transcriptional regulation, DNA repair, centromere packaging, maintenance of pericentromeric heterochromatin, stress responses, temperature sensing, development, and many other biological processes. Here, we review the universal histone variants in H2A, H3 and H1 families and their roles in epigenetics.

Key words: H2AX; H2AZ; H3.3; CenH3; H1

Cite this article

Leilei SHI , Yuda FANG . Histone variants: making structurally and functionally divergent nucleosomes and linkers in chromatin[J]. Frontiers in Biology, 2011 , 6(2) : 93 -101 . DOI: 10.1007/s11515-011-1127-5

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant No. 91019006 to Y.F.) and the Chinese Academy of Sciences (No. KSCX2-YW-N-099 to Y.F.)
1
Adam M, Robert F, Larochelle M, Gaudreau L (2001). H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol Cell Biol, 21(18): 6270–6279

DOI PMID

2
Ahmad K, Henikoff S (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell, 9(6): 1191–1200

DOI PMID

3
Allis C D, Glover C V C, Bowen J K, Gorovsky M A (1980). Histone variants specific to the transcriptionally active, amitotically dividing macronucleus of the unicellular eucaryote, Tetrahymena thermophila. Cell, 20(3): 609–617

DOI PMID

4
Altaf M, Auger A, Covic M, Côté J (2009). Connection between histone H2A variants and chromatin remodeling complexes. Biochem Cell Biol, 87(1): 35–50

DOI PMID

5
Ascenzi R, Gantt J S (1997). A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants. Plant Mol Biol, 34(4): 629–641

DOI PMID

6
Ascenzi R, Gantt J S (1999). Subnuclear distribution of the entire complement of linker histone variants in Arabidopsis thaliana. Chromosoma, 108(6): 345–355

DOI PMID

7
Ausió J, Abbott D W, Wang X, Moore S C (2001). Histone variants and histone modifications: a structural perspective. Biochem Cell Biol, 79(6): 693–708

DOI PMID

8
Barra J L, Rhounim L, Rossignol J L, Faugeron G (2000). Histone H1 is dispensable for methylation-associated gene silencing in Ascobolus immersus and essential for long life span. Mol Cell Biol, 20(1): 61–69

DOI PMID

8a
Bonnefoy E, OrsiG A, CoubleP, LoppinB(2007). The essential role of Drosophila HIRA for de novo assembly of paternal chromatin at fertilization.PLoS Genet , 3(10): 1991–2006

9
Carr A M, Dorrington S M, Hindley J, Phear G A, Aves S J, Nurse P (1994). Analysis of a histone H2A variant from fission yeast: evidence for a role in chromosome stability. Mol Gen Genet, 245(5): 628–635

DOI PMID

10
Celeste A, Petersen S, Romanienko P J, Fernandez-Capetillo O, Chen H T, Sedelnikova O A, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio M J, Redon C, Pilch D R, Olaru A, Eckhaus M, Camerini-Otero R D, Tessarollo L, Livak F, Manova K, Bonner W M, Nussenzweig M C, Nussenzweig A (2002). Genomic instability in mice lacking histone H2AX. Science, 296(5569): 922–927

DOI PMID

11
Chadwick B P, Willard H F (2001a). Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant. Hum Mol Genet, 10(10): 1101–1113

DOI PMID

12
Chadwick B P, Willard H F (2001b). A novel chromatin protein, distantly related to histone H2A, is largely excluded from the inactive X chromosome. J Cell Biol, 152(2): 375–384

DOI PMID

13
Chen D, Hinkley C S, Henry R W, Huang S (2002). TBP dynamics in living human cells: constitutive association of TBP with mitotic chromosomes. Mol Biol Cell, 13(1): 276–284

DOI PMID

14
Collins K A, Furuyama S, Biggins S (2004). Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol, 14(21): 1968–1972

DOI PMID

15
Cremer C, Münkel C, Granzow M, Jauch A, Dietzel S, Eils R, Guan X Y, Meltzer P S, Trent J M, Langowski J, Cremer T (1996). Nuclear architecture and the induction of chromosomal aberrations. Mutat Res, 366(2): 97–116

PMID

16
Cremer T, Cremer C (2001). Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet, 2(4): 292–301

DOI PMID

17
Csink A K, Henikoff S (1996). Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature, 381(6582): 529–531

DOI PMID

18
Cui B, Gorovsky M A (2006). Centromeric histone H3 is essential for vegetative cell division and for DNA elimination during conjugation in Tetrahymena thermophila. Mol Cell Biol, 26(12): 4499–4510

DOI PMID

19
Cui B, Liu Y, Gorovsky M A (2006). Deposition and function of histone H3 variants in Tetrahymena thermophila. Mol Cell Biol, 26(20): 7719–7730

DOI PMID

20
Dalal Y, Wang H, Lindsay S, Henikoff S (2007). Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol, 5(8): e218

DOI PMID

21
Dawson S C, Sagolla M S, Cande W Z (2007). The cenH3 histone variant defines centromeres in Giardia intestinalis. Chromosoma, 116(2): 175–184

DOI PMID

22
Deal R B, Henikoff J G, Henikoff S (2010). Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science, 328(5982): 1161–1164

DOI PMID

23
Delahodde A, Becam A M, Perea J, Jacq C (1986). A yeast protein HX has homologies with the histone H2AF expressed in chicken embryo. Nucleic Acids Res, 14(22): 9213–9214

DOI PMID

24
Dernburg A F, Broman K W, Fung J C, Marshall W F, Philips J, Agard D A, Sedat J W (1996). Perturbation of nuclear architecture by long-distance chromosome interactions. Cell, 85(5): 745–759

DOI PMID

25
Dhillon N, Oki M, Szyjka S J, Aparicio O M, Kamakaka R T (2006). H2A.Z functions to regulate progression through the cell cycle. Mol Cell Biol, 26(2): 489–501

DOI PMID

26
Dimitriadis E K, Weber C, Gill R K, Diekmann S, Dalal Y (2010). Tetrameric organization of vertebrate centromeric nucleosomes. Proc Natl Acad Sci USA, 107(47): 20317–20322

DOI PMID

28
Earnshaw W C, Rothfield N (1985). Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma, 91(3–4): 313–321

DOI PMID

28a
Erard M S, BelenguerP, Caizergues-FerrerM, PantaloniA, AmalricF(1988). A major nucleolar protein, nucleolin, induces chromatin decondensation by binding to histone H.Eur J Biochem, 175(3): 525–530

29
Faast R, Thonglairoam V, Schulz T C, Beall J, Wells J R, Taylor H, Matthaei K, Rathjen P D, Tremethick D J, Lyons I (2001). Histone variant H2A.Z is required for early mammalian development. Curr Biol, 11(15): 1183–1187

DOI PMID

30
Fan Y, Nikitina T, Morin-Kensicki E M, Zhao J, Magnuson T R, Woodcock C L, Skoultchi A I (2003). H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol Cell Biol, 23(13): 4559–4572

DOI PMID

30a
FangY, SpectorD L(2005). Centromere positioning and dynamics in living Arabidopsis plants.Mol Biol Cell, 16(12): 5710-5718

31
Fang Y, Spector D L (2010). Live Cell Imaging of Plants. Cold Spring Harbor Protocols, pdb top68.

32
Farris S D, Rubio E D, Moon J J, Gombert W M, Nelson B H, Krumm A (2005). Transcription-induced chromatin remodeling at the c-myc gene involves the local exchange of histone H2A.Z. J Biol Chem, 280(26): 25298–25303

DOI PMID

33
Fatemi M, Wade P A (2006). MBD family proteins: reading the epigenetic code. J Cell Sci, 119(Pt 15): 3033–3037

DOI PMID

34
Fernandez-Capetillo O, Mahadevaiah S K, Celeste A, Romanienko P J, Camerini-Otero R D, Bonner W M, Manova K, Burgoyne P, Nussenzweig A (2003). H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell, 4(4): 497–508

DOI PMID

35
Fischle W, Wang Y, Jacobs S A, Kim Y, Allis C D, Khorasanizadeh S (2003). Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev, 17(15): 1870–1881

DOI PMID

36
Gantt J S, Lenvik T R (1991). Arabidopsis thaliana H1 histones. Analysis of two members of a small gene family. Eur J Biochem, 202(3): 1029–1039

DOI PMID

37
Gévry N, Chan H M, Laflamme L, Livingston D M, Gaudreau L (2007). p21 transcription is regulated by differential localization of histone H2A.Z. Genes Dev, 21(15): 1869–1881

DOI PMID

38
Gévry N, Hardy S, Jacques P E, Laflamme L, Svotelis A, Robert F, Gaudreau L (2009). Histone H2A.Z is essential for estrogen receptor signaling. Genes Dev, 23(13): 1522–1533

DOI PMID

38a
Ginisty H, Sicard H, Roger B, Bouvet P(1999). Structure and functions of nucleolin.J Cell Sci, 112 (Pt 6): 761–772

39
Goldberg A D, Banaszynski L A, Noh K M, Lewis P W, Elsaesser S J, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver R C, Miller J C, Lee Y L, Boydston E A, Holmes M C, Gregory P D, Greally J M, Rafii S, Yang C, Scambler P J, Garrick D, Gibbons R J, Higgs D R, Cristea I M, Urnov F D, Zheng D, Allis C D (2010). Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell, 140(5): 678–691

DOI PMID

40
Govin J, Caron C, Rousseaux S, Khochbin S (2005). Testis-specific histone H3 expression in somatic cells. Trends Biochem Sci, 30(7): 357–359

DOI PMID

41
Grove G W, Zweidler A (1984). Regulation of nucleosomal core histone variant levels in differentiating murine erythroleukemia cells. Biochemistry, 23(19): 4436–4443

DOI PMID

42
Hake S B, Garcia B A, Kauer M, Baker S P, Shabanowitz J, Hunt D F, Allis C D (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

DOI PMID

43
Hardy S, Jacques P É, Gévry N, Forest A, Fortin M È, Laflamme L, Gaudreau L, Robert F (2009). The euchromatic and heterochromatic landscapes are shaped by antagonizing effects of transcription on H2A.Z deposition. PLoS Genet, 5(10): e1000687

DOI PMID

44
Hashimoto H, Takami Y, Sonoda E, Iwasaki T, Iwano H, Tachibana M, Takeda S, Nakayama T, Kimura H, Shinkai Y (2010). Histone H1 null vertebrate cells exhibit altered nucleosome architecture. Nucleic Acids Res, 38(11): 3533–3545

DOI PMID

45
Henikoff S (2008). Nucleosome destabilization in the epigenetic regulation of gene expression. Nat Rev Genet, 9(1): 15–26

DOI PMID

46
Henikoff S, Ahmad K (2005). Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol, 21(1): 133–153

DOI PMID

47
Hewawasam G, Shivaraju M, Mattingly M, Venkatesh S, Martin-Brown S, Florens L, Workman J L, Gerton J L (2010). Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol Cell, 40(3): 444–454

DOI PMID

47a
HodlM, BaslerK (2009). Transcription in the absence of histone H3.3. Curr Biol, 19(14): 1221–1226

48
Ho L, Crabtree G R (2010). Chromatin remodelling during development. Nature, 463(7280): 474–484

DOI PMID

49
Ingouff M, Rademacher S, Holec S, Šoljić L, Xin N, Readshaw A, Foo S H, Lahouze B, Sprunck S, Berger F (2010). Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol, 23(20): 2137–2143

50
Jackson J D, Gorovsky M A (2000). Histone H2A.Z has a conserved function that is distinct from that of the major H2A sequence variants. Nucleic Acids Res, 28(19): 3811–3816

DOI PMID

51
Jenuwein T, Allis C D (2001). Translating the histone code. Science, 293(5532): 1074–1080

DOI PMID

52
Kapros T, Robertson A J, Waterborg J H (1995). Histone H3 transcript stability in alfalfa. Plant Mol Biol, 28(5): 901–914

DOI PMID

53
KermekchievM, WorkmanJ L, PikaardC S (1997). Nucleosome binding by the polymerase I transactivator upstream binding factor displaces linker histone H1.Mol Cell Biol, 17(10): 5833-5842

53a
Kojima H, SuzukiT, Kato T, EnomotoK, SatoS, KatoT, TabataS, Sáez-VasquezJ, EcheverríaM, NakagawaT, Ishiguro S, NakamuraK(2007). Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development.Plant J, 49(6):1053–1063

54
Kumar S V, Wigge P A (2010). H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell, 140(1): 136–147

DOI PMID

55
Larochelle M, Gaudreau L (2003). H2A.Z has a function reminiscent of an activator required for preferential binding to intergenic DNA. EMBO J, 22: 4512–4522

56
Leach T J, Mazzeo M, Chotkowski H L, Madigan J P, Wotring M G, Glaser R L (2000). Histone H2A.Z is widely but nonrandomly distributed in chromosomes of Drosophila melanogaster. J Biol Chem, 275(30): 23267–23272

DOI PMID

57
Lever M A, Th’ng J P, Sun X, Hendzel M J (2000). Rapid exchange of histone H1.1 on chromatin in living human cells. Nature, 408(6814): 873–876

DOI PMID

58
Li C, Mueller J E, Elfline M, Bryk M (2008). Linker histone H1 represses recombination at the ribosomal DNA locus in the budding yeast Saccharomyces cerevisiae. Mol Microbiol, 67(4): 906–919

DOI PMID

59
Liu X, Li B, GorovskyMA (1996). Essential and nonessential histone H2A variants in Tetrahymena thermophila. Mol Cell Biol, 16(8): 4305–4311

PMID

60
Loppin B, Bonnefoy E, Anselme C, Laurençon A, Karr T L, Couble P (2005). The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature, 437(7063): 1386–1390

DOI PMID

61
Loyola A (2004). Histone chaperones, a supporting role in the limelight. Biochimica et Biophysica Acta (BBA) -. Gene Structure and Expression, 1677: 3–11

62
Lu X, Wontakal S N, Emelyanov A V, Morcillo P, Konev A Y, Fyodorov D V, Skoultchi A I (2009). Linker histone H1 is essential for Drosophila development, the establishment of pericentric heterochromatin, and a normal polytene chromosome structure. Genes Dev, 23(4): 452–465

DOI PMID

63
Luger K, Mäder A W, Richmond R K, Sargent D F, Richmond T J (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389(6648): 251–260

DOI PMID

64
Mahadevaiah S K, Turner J M, Baudat F, Rogakou E P, de Boer P, Blanco-Rodríguez J, Jasin M, Keeney S, Bonner W M, Burgoyne P S (2001). Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet, 27(3): 271–276

DOI PMID

65
Malik H S, Henikoff S (2001). Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics, 157(3): 1293–1298

PMID

66
Malik H S, Henikoff S (2003). Phylogenomics of the nucleosome. Nat Struct Biol, 10(11): 882–891

DOI PMID

67
March-Díaz R, García-Domínguez M, Lozano-Juste J, León J, Florencio F J, Reyes J C (2008). Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J, 53(3): 475–487

DOI PMID

68
March-Díaz R, Reyes J C (2009). The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Mol Plant, 2(4): 565–577

DOI PMID

69
Meneghini M D, Wu M, Madhani H D (2003). Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell, 112(5): 725–736

DOI PMID

70
Misteli T (2009). Self-organization in the genome. Proc Natl Acad Sci USA, 106(17): 6885–6886

DOI PMID

71
Misteli T, Gunjan A, Hock R, Bustin M, Brown D T (2000). Dynamic binding of histone H1 to chromatin in living cells. Nature, 408(6814): 877–881

DOI PMID

72
Misteli T, Soutoglou E (2009). The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat Rev Mol Cell Biol, 10(4): 243–254

DOI PMID

73
Mizuguchi G, Xiao H, Wisniewski J, Smith M M, Wu C (2007). Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell, 129(6): 1153–1164

DOI PMID

73a
Mongelard F, Bouvet P(2007). Nucleolin: a multiFACeTed protein.Trends Cell Biol, 17(2): 80–86

74
Moore L L, Morrison M, Roth M B (1999). HCP-1, a protein involved in chromosome segregation, is localized to the centromere of mitotic chromosomes in Caenorhabditis elegans. J Cell Biol, 147(3): 471–480

DOI PMID

75
Mousson F, Ochsenbein F, Mann C (2007). The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways. Chromosoma, 116(2): 79–93

DOI PMID

76
Nagaki K, Kashihara K, Murata M (2005). Visualization of diffuse centromeres with centromere-specific histone H3 in the holocentric plant Luzula nivea. Plant Cell, 17(7): 1886–1893

DOI PMID

77
Ng R K, Gurdon J B (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(1): 102–109

DOI PMID

78
Oishi K, Okano H, Sawa H (2007). RMD-1, a novel microtubule-associated protein, functions in chromosome segregation in Caenorhabditis elegans. J Cell Biol, 179(6): 1149–1162

DOI PMID

79
Patterton H G, Landel C C, Landsman D, Peterson C L, Simpson R T (1998). The biochemical and phenotypic characterization of Hho1p, the putative linker histone H1 of Saccharomyces cerevisiae. J Biol Chem, 273(13): 7268–7276

DOI PMID

80
Paull T T, Rogakou E P, Yamazaki V, Kirchgessner C U, Gellert M, Bonner W M (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol, 10(15): 886–895

DOI PMID

81
Pehrson J R, Fried V A (1992). MacroH2A, a core histone containing a large nonhistone region. Science, 257(5075): 1398–1400

DOI PMID

81a
PontvianneF, MatíaI, DouetJ, TourmenteS, MedinaF J, EcheverriaM, Sáez-Vásquez J(2007). Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis.Mol Biol Cell, 18(2): 369–379

82
Ramón A, Muro-Pastor M I, Scazzocchio C, Gonzalez R (2000). Deletion of the unique gene encoding a typical histone H1 has no apparent phenotype in Aspergillus nidulans. Mol Microbiol, 35(1): 223–233

DOI PMID

83
Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W (2002). Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev, 12(2): 162–169

DOI PMID

84
Sakai A, Schwartz B E, Goldstein S, Ahmad K (2009). Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr Biol, 19(21): 1816–1820

DOI PMID

85
Santenard A, Ziegler-Birling C, Koch M, Tora L, Bannister A J, Torres-Padilla M E (2010). Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat Cell Biol, 12(9): 853–862

DOI PMID

86
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 (2010). A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev, 24(2): 159–170

DOI PMID

87
Schäfer G, McEvoy C R, Patterton H G (2008). The Saccharomyces cerevisiae linker histone Hho1p is essential for chromatin compaction in stationary phase and is displaced by transcription. Proc Natl Acad Sci USA, 105(39): 14838–14843

DOI PMID

88
Schwartz B E, Ahmad K (2005). Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev, 19(7): 804–814

DOI PMID

89
Sedelnikova O A, Pilch D R, Redon C, Bonner W M (2003). Histone H2AX in DNA damage and repair. Cancer Biol Ther, 2(3): 233–235

PMID

90
Shen X, Yu L, Weir J W, Gorovsky M A (1995). Linker histones are not essential and affect chromatin condensation in vivo. Cell, 82(1): 47–56

DOI PMID

90a
ShuaibM, OuararhniK, DimitrovS, HamicheA(2010). HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres.Proc Natl Acad Sci U S A, 107(4): 1349–1354

91
Smith M M (2002). Centromeres and variant histones: what, where, when and why? Curr Opin Cell Biol, 14(3): 279–285

DOI PMID

92
Stoler S, Keith K C, Curnick K E, Fitzgerald-Hayes M (1995). 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, 9(5): 573–586

DOI PMID

93
Ström L, Lindroos H B, Shirahige K, Sjögren C (2004). Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell, 16(6): 1003–1015

DOI PMID

94
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

DOI PMID

95
Talbert P B, Henikoff S (2010). Histone variants—ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol, 11(4): 264–275

DOI PMID

96
Talbert P B, Masuelli R, Tyagi A P, Comai L, Henikoff S (2002). Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell, 14(5): 1053–1066

DOI PMID

97
Thiriet C, Hayes J J (2005). Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev, 19(6): 677–682

DOI PMID

98
Ünal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber J E, Koshland D (2004). DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell, 16(6): 991–1002

DOI PMID

99
Ushinsky S C, Bussey H, Ahmed A A, Wang Y, Friesen J, Williams B A, Storms R K (1997). Histone H1 in Saccharomyces cerevisiae. Yeast, 13(2): 151–161

DOI PMID

100
van Attikum H, Gasser S M (2009). Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol, 19(5): 207–217

DOI PMID

101
van Daal A, Elgin S C (1992). A histone variant, H2AvD, is essential in Drosophila melanogaster. Mol Biol Cell, 3(6): 593–602

PMID

102
van der Heijden G W, Derijck A A, Pósfai E, Giele M, Pelczar P, Ramos L, Wansink D G, van der Vlag J, Peters A H, de Boer P (2007). Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat Genet, 39(2): 251–258

DOI PMID

103
Waddington C H (1942). The epigenotype. Endeavour,pp. 18–20.

104
Waddington C H (1968). Towards a Theoretical Biology. In: The Basic Ideas of Biology Edinburgh: Edinburgh University Press,pp. 1–32

105
Walfridsson J, Bjerling P, Thalen M, Yoo E J, Park S D, Ekwall K (2005). The CHD remodeling factor Hrp1 stimulates CENP-A loading to centromeres. Nucleic Acids Res, 33(9): 2868–2879

DOI PMID

106
Waterborg J H (1991). Multiplicity of histone h3 variants in wheat, barley, rice, and maize. Plant Physiol, 96(2): 453–458

DOI PMID

107
West M H, Bonner W M (1980). Histone 2A, a heteromorphous family of eight protein species. Biochemistry, 19(14): 3238–3245

DOI PMID

107a
WierzbickiA T, JerzmanowskiA(2005). Suppression of histone H1 genes in Arabidopsis results in heritable developmental defects and stochastic changes in DNA methylation.Genetics, 169(2): 997–1008

108
Wu Ct, Morris J R (2001). Genes, genetics, and epigenetics: a correspondence. Science, 293(5532): 1103–1105

DOI PMID

109
Zhang Q, Wang Y (2010). HMG modifications and nuclear function. Biochim Biophys Acta, 1799(1–2): 28–36

PMID

110
Zhang X, Germann S, Blus B J, Khorasanizadeh S, Gaudin V, Jacobsen S E (2007). The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol, 14(9): 869–871

DOI PMID

111
Zheng Y, John S, Pesavento J J, Schultz-Norton J R, Schiltz R L, Baek S, Nardulli A M, Hager G L, Kelleher N L, Mizzen C A (2010). Histone H1 phosphorylation is associated with transcription by RNA polymerases I and II. J Cell Biol, 189(3): 407–415

DOI PMID

112
Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008). Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature, 456(7218): 125–129

DOI PMID

Outlines

/