The H1 linker histones: Multifunctional proteins beyond the nucleosomal core particle

EMBO Reports

Volumn 16, Issue 11, 2015, Pages 1439-1453

  Hergeth, Sonja P ^a   Schneider, Robert ^b  

^a Medizinweltenservices GmbH   (Germany)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

chromatin; epigenetics; linker histone; modifications; subtypes

Indexed keywords

DNA; HISTONE H1; CHROMATIN; HETEROCHROMATIN; HISTONE; NUCLEOSOME; PROTEIN BINDING;

BINDING AFFINITY; DNA REPAIR; EMBRYO DEVELOPMENT; GENE EXPRESSION; HETEROCHROMATIN; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE PHOSPHORYLATION; HUMAN; NONHUMAN; NUCLEOSOMAL CORE PARTICLE; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; TRANSCRIPTION REGULATION; ANIMAL; CHEMISTRY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HISTONE CODE; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPAIR; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HETEROCHROMATIN; HISTONE CODE; HISTONES; NUCLEOSOMES; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY;

EID: 84946050981     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201540749     Document Type: Review

References (134)

1. 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: 251-260
2. Woodcock CL, Skoultchi AI, Fan Y, (2006) Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res 14: 17-25
3. Robinson PJ, Rhodes D, (2006) Structure of the "30 nm" chromatin fibre: a key role for the linker histone. Curr Opin Struct Biol 16: 336-343
4. Thoma F, Koller T, Klug A, (1979) Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol 83: 403-427
5. Schlissel MS, Brown DD, (1984) The transcriptional regulation of Xenopus 5s RNA genes in chromatin: the roles of active stable transcription complexes and histone H1. Cell 37: 903-913
6. Lever MA, Th'ng JP, Sun X, Hendzel MJ, (2000) Rapid exchange of histone H1.1 on chromatin in living human cells. Nature 408: 873-876
7. 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
8. Catez F, Ueda T, Bustin M, (2006) Determinants of histone H1 mobility and chromatin binding in living cells. Nat Struct Mol Biol 13: 305-310
9. Shen X, Gorovsky MA, (1996) Linker histone H1 regulates specific gene expression but not global transcription in vivo. Cell 86: 475-483
10. Sirotkin AM, Edelmann W, Cheng G, Klein-Szanto A, Kucherlapati R, Skoultchi AI, (1995) Mice develop normally without the H1(0) linker histone. Proc Natl Acad Sci USA 92: 6434-6438
11. Drabent B, Saftig P, Bode C, Doenecke D, (2000) Spermatogenesis proceeds normally in mice without linker histone H1t. Histochem Cell Biol 113: 433-442
12. Fan Y, Sirotkin A, Russell RG, 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
13. Rabini S, Franke K, Saftig P, Bode C, Doenecke D, Drabent B, (2000) Spermatogenesis in mice is not affected by histone H1.1 deficiency. Exp Cell Res 255: 114-124
14. Fan Y, Nikitina T, Morin-Kensicki EM, Zhao J, Magnuson TR, Woodcock CL, Skoultchi AI, (2003) H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol Cell Biol 23: 4559-4572
15. 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: 3533-3545
16. 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
17. Hellauer K, Sirard E, Turcotte B, (2001) Decreased expression of specific genes in yeast cells lacking histone H1. J Biol Chem 276: 13587-13592
18. Vujatovic O, Zaragoza K, Vaquero A, Reina O, Bernues J, Azorin F, (2012) Drosophila melanogaster linker histone dH1 is required for transposon silencing and to preserve genome integrity. Nucleic Acids Res 40: 5402-5414
19. 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: e1000227
20. Izzo A, Kamieniarz K, Schneider R, (2008) The histone H1 family: specific members, specific functions? Biol Chem 389: 333-343
21. Wis̈niewski JR, Zougman A, Krüger S, Mann M, (2007) Mass spectrometric mapping of linker histone H1 variants reveals multiple acetylations, methylations, and phosphorylation as well as differences between cell culture and tissue. Mol Cell Proteomics 6: 72-87
22. Garcia BA, Busby SA, Barber CM, Shabanowitz J, Allis CD, Hunt DF, (2004) Characterization of phosphorylation sites on histone H1 isoforms by tandem mass spectrometry. J Proteome Res 3: 1219-1227
23. Lu A, Zougman A, Pudełko M, Bębenek M, Ziõłkowski P, Mann M, Wis̈niewski JR, (2009) Mapping of lysine monomethylation of linker histones in human breast and its cancer. J Proteome Res 8: 4207-4215
24. Deterding LJ, Bunger MK, Banks GC, Tomer KB, Archer TK, (2008) Global changes in and characterization of specific sites of phosphorylation in mouse and human histone H1 isoforms upon CDK inhibitor treatment using mass spectrometry. J Proteome Res 7: 2368-2379
25. Villar-Garea A, Imhof A, (2008) Fine mapping of posttranslational modifications of the linker histone H1 from Drosophila melanogaster. PLoS ONE 3: e1553
26. Bonet-Costa C, Vilaseca M, Diema C, Vujatovic O, Vaquero A, Omeñaca N, Castejõn L, Bernués J, Giralt E, Azorín F, (2012) Combined bottom-up and top-down mass spectrometry analyses of the pattern of post-translational modifications of Drosophila melanogaster linker histone H1. J Proteomics 75: 4124-4138
27. Sarg B, Lopez R, Lindner H, Ponte I, Suau P, Roque A, (2015) Identification of novel post-translational modifications of linker histones in chicken erythrocytes. J Proteomics 113: 162-177
28. Happel N, Doenecke D, (2009) Histone H1 and its isoforms: contribution to chromatin structure and function. Gene 431: 1-12
29. McBryant SJ, Lu X, Hansen JC, (2010) Multifunctionality of the linker histones: an emerging role for protein-protein interactions. Cell Res 20: 519-528
30. Harshman SW, Young NL, Parthun MR, Freitas MA, (2013) H1 histones: current perspectives and challenges. Nucleic Acids Res 41: 9593-9609
31. Wood C, Snijders A, Williamson J, Reynolds C, Baldwin J, Dickman M, (2009) Post-translational modifications of the linker histone variants and their association with cell mechanisms. FEBS J 276: 3685-3697
32. Ramakrishnan V, Finch JT, Graziano V, Lee PL, Sweet RM, (1993) Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature 362: 219-223
33. Roque A, Iloro I, Ponte I, Arrondo JLR, Suau P, (2005) DNA-induced secondary structure of the carboxyl-terminal domain of histone H1. J Biol Chem 280: 32141-32147
34. Hayashi T, Hayashi H, Iwai K, (1987) Tetrahymena histone H1. Isolation and amino acid sequence lacking the central hydrophobic domain conserved in other H1 histones. J Biochem 102: 369-376
35. Patterton HG, Landel CC, Landsman D, Peterson CL, Simpson RT, (1998) The biochemical and phenotypic characterization of Hho1p, the putative linker histone H1 of Saccharomyces cerevisiae. J Biol Chem 273: 7268-7276
36. Godde JS, Widom J, (1992) Chromatin structure of Schizosaccharomyces pombe. A nucleosome repeat length that is shorter than the chromatosomal DNA length. J Mol Biol 226: 1009-1025
37. Syed SH, Goutte-Gattat D, Becker N, Meyer S, Shukla MS, Hayes JJ, Everaers R, Angelov D, Bednar J, Dimitrov S, (2010) Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome. Proc Natl Acad Sci USA 107: 9620-9625
38. Song F, Chen P, Sun D, Wang M, Dong L, Liang D, Xu R-M, Zhu P, Li G, (2014) Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science 344: 376-380
39. Zhou B-R, Feng H, Kato H, Dai L, Yang Y, Zhou Y, Bai Y, (2013) Structural insights into the histone H1-nucleosome complex. Proc Natl Acad Sci USA 110: 19390-19395
40. Brown DT, Izard T, Misteli T, (2006) Mapping the interaction surface of linker histone H10 with the nucleosome of native chromatin in vivo. Nat Struct Mol Biol 13: 250-255
41. Marzluff WF, (2005) Metazoan replication-dependent histone mRNAs: a distinct set of RNA polymerase II transcripts. Curr Opin Cell Biol 17: 274-280
42. Albig W, Doenecke D, (1997) The human histone gene cluster at the D6S105 locus. Hum Genet 101: 284-294
43. Wang ZF, Sirotkin AM, Buchold GM, Skoultchi AI, Marzluff WF, (1997) The mouse histone H1 genes: gene organization and differential regulation. J Mol Biol 271: 124-138
44. Kasinsky HE, Lewis JD, Dacks JB, Ausiõ J, (2001) Origin of H1 linker histones. FASEB J 15: 34-42
45. Zlatanova J, Doenecke D, (1994) Histone H1 zero: a major player in cell differentiation? FASEB J 8: 1260-1268
46. Happel N, Schulze E, Doenecke D, (2005) Characterisation of human histone H1x. Biol Chem 386: 541-551
47. Drabent B, Kardalinou E, Doenecke D, (1991) Structure and expression of the human gene encoding testicular H1 histone (H1t). Gene 103: 263-268
48. 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: 2808-2813
49. Tanaka M, Hennebold JD, Macfarlane J, Adashi EY, (2001) A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. Development 128: 655-664
50. 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
51. Hendzel MJ, Lever MA, Crawford E, Th'ng JPH, (2004) The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J Biol Chem 279: 20028-20034
52. Clausell J, Happel N, Hale TK, Doenecke D, Beato M, (2009) Histone H1 subtypes differentially modulate chromatin condensation without preventing ATP-dependent remodeling by SWI/SNF or NURF. PLoS ONE 4: e0007243
53. Öberg C, Izzo A, Schneider R, Wrange Ö, Belikov S, (2012) Linker histone subtypes differ in their effect on nucleosomal spacing in vivo. J Mol Biol 419: 183-197
54. Orrego M, Ponte I, Roque A, Buschati N, Mora X, Suau P, (2007) Differential affinity of mammalian histone H1 somatic subtypes for DNA and chromatin. BMC Biol 5: 22
55. Talasz H, Sapojnikova N, Helliger W, Lindner H, Puschendorf B, (1998) In vitro binding of H1 histone subtypes to nucleosomal organized mouse mammary tumor virus long terminal repeat promotor. J Biol Chem 273: 32236-32243
56. Kinkade JM, Cole RD, (1966) The resolution of four lysine-rich histones derived from calf thymus. J Biol Chem 241: 5790-5797
57. Krishnakumar R, Gamble MJ, Frizzell KM, Berrocal JG, Kininis M, Kraus WL, (2008) Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 319: 819-821
58. Braunschweig U, Hogan GJ, Pagie L, van Steensel B, (2009) Histone H1 binding is inhibited by histone variant H3.3. EMBO J 28: 3635-3645
59. 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: 2142-2154
60. Cao K, Lailler N, Zhang Y, Kumar A, Uppal K, Liu Z, Lee EK, Wu H, Medrzycki M, Pan C, et al, (2013) High-resolution mapping of H1 linker histone variants in embryonic stem cells. PLoS Genet 9: e1003417
61. Nalabothula N, McVicker G, Maiorano J, Martin R, Pritchard JK, Fondufe-Mittendorf YN, (2014) The chromatin architectural proteins HMGD1 and H1 bind reciprocally and have opposite effects on chromatin structure and gene regulation. BMC Genom 15: 1-14
62. Millan-Arino L, Islam ABMMK, Izquierdo-Bouldstridge A, Mayor R, Terme JM, Luque N, Sancho M, Lopez-Bigas N, Jordan A, (2014) Mapping of six somatic linker histone H1 variants in human breast cancer cells uncovers specific features of H1.2. Nucleic Acids Res 42: 4474-4493
63. Chen P, Zhao J, Wang Y, Wang M, Long H, Liang D, Huang L, Wen Z, Li W, Li X, et al, (2013) H3.3 actively marks enhancers and primes gene transcription via opening higher-ordered chromatin. Genes Dev 27: 2109-2124
64. Guenatri M, (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166: 493-505
65. van Steensel B, Delrow J, Henikoff S, (2001) Chromatin profiling using targeted DNA adenine methyltransferase. Nat Genet 27: 304-308
66. Li J-Y, Patterson M, Mikkola HKA, Lowry WE, Kurdistani SK, (2012) Dynamic distribution of linker histone H1.5 in cellular differentiation. PLoS Genet 8: e1002879
67. Mayor R, Izquierdo-Bouldstridge A, Millán-Ariño L, Bustillos A, Sampaio C, Luque N, Jordan A, (2015) Genome distribution of replication-independent histone H1 variants shows H1.0 associated with nucleolar domains and H1X associated with RNA polymerase II-enriched regions. J Biol Chem 290: 7474-7491
68. Lu X, Wontakal SN, Emelyanov AV, Morcillo P, Konev AY, Fyodorov DV, Skoultchi AI, (2009) Linker histone H1 is essential for Drosophila development, the establishment of pericentric heterochromatin, and a normal polytene chromosome structure. Genes Dev 23: 452-465
69. Lu X, Wontakal SN, Kavi H, Kim BJ, Guzzardo PM, Emelyanov AV, Xu N, Hannon GJ, Zavadil J, Fyodorov DV, et al, (2013) Drosophila H1 regulates the genetic activity of heterochromatin by recruitment of Su(var)3-9. Science 340: 78-81
70. Xu N, Emelyanov AV, Fyodorov DV, Skoultchi AI, (2014) Drosophila linker histone H1 coordinates STAT-dependent organization of heterochromatin and suppresses tumorigenesis caused by hyperactive JAK-STAT signaling. Epigenetics Chromatin 7: 16
71. Nielsen AL, Oulad-Abdelghani M, Ortiz JA, Remboutsika E, Chambon P, Losson R, (2001) Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. Mol Cell 7: 729-739
72. Daujat S, Zeissler U, Waldmann T, Happel N, Schneider R, (2005) HP1 binds specifically to Lys26-methylated histone H1.4, whereas simultaneous Ser27 phosphorylation blocks HP1 binding. J Biol Chem 280: 38090-38095
73. Hale TK, Contreras A, Morrison AJ, Herrera RE, (2006) Phosphorylation of the linker histone H1 by CDK regulates its binding to HP1α. Mol Cell 22: 693-699
74. Trojer P, Zhang J, Yonezawa M, Schmidt A, Zheng H, Jenuwein T, Reinberg D, (2009) Dynamic histone H1 isotype 4 methylation and demethylation by histone lysine methyltransferase G9a/KMT1C and the Jumonji domain-containing JMJD2/KDM4 proteins. J Biol Chem 284: 8395-8405
75. Trojer P, Li G, Sims RJ III, Vaquero A, Kalakonda N, Boccuni P, Lee D, Erdjument-Bromage H, Tempst P, Nimer SD, et al, (2007) L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129: 915-928
76. Popova EY, Grigoryev SA, Fan Y, Skoultchi AI, Zhang SS, Barnstable CJ, (2013) Developmentally regulated linker histone H1c promotes heterochromatin condensation and mediates structural integrity of rod photoreceptors in mouse retina. J Biol Chem 288: 17895-17907
77. Alami R, Fan Y, Pack S, Sonbuchner TM, Besse A, Lin Q, Greally JM, Skoultchi AI, Bouhassira EE, (2003) Mammalian linker-histone subtypes differentially affect gene expression in vivo. Proc Natl Acad Sci USA 100: 5920-5925
78. Bresnick EH, Bustin M, Marsaud V, Richard-Foy H, Hager GL, (1992) The transcriptionally-active MMTV promoter is depleted of histone H1. Nucleic Acids Res 20: 273-278
79. Gunjan A, Brown DT, (1999) Overproduction of histone H1 variants in vivo increases basal and induced activity of the mouse mammary tumor virus promoter. Nucleic Acids Res 27: 3355-3363
80. Koop R, Di Croce L, Beato M, (2003) Histone H1 enhances synergistic activation of the MMTV promoter in chromatin. EMBO J 22: 588-599
81. Belikov S, Astrand C, Wrange O, (2007) Mechanism of histone H1-stimulated glucocorticoid receptor DNA binding in vivo. Mol Cell Biol 27: 2398-2410
82. Vicent GP, Nacht AS, Font-Mateu J, Castellano G, Gaveglia L, Ballare C, Beato M, (2011) Four enzymes cooperate to displace histone H1 during the first minute of hormonal gene activation. Genes Dev 25: 845-862
83. Kim K, Lee B, Kim J, Choi J, Kim J-M, Xiong Y, Roeder RG, An W, (2013) Linker histone H1.2 cooperates with Cul4A and PAF1 to drive H4K31 ubiquitylation-mediated transactivation. Cell Rep 5: 1690-1703
84. Kadota S, Nagata K, (2014) Silencing of IFN-stimulated gene transcription is regulated by histone H1 and its chaperone TAF-I. Nucleic Acids Res 42: 7642-7653
85. Lee H, Habas R, Abate-Shen C, (2004) Msx1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 304: 1675-1678
86. Studencka M, Konzer A, Moneron G, Wenzel D, Opitz L, Salinas-Riester G, Bedet C, Kruger M, Hell SW, Wisniewski JR, et al, (2011) Novel roles of Caenorhabditis elegans heterochromatin protein HP1 and linker histone in the regulation of innate immune gene expression. Mol Cell Biol 32: 251-265
87. Kim K, Choi J, Heo K, Kim H, Levens D, Kohno K, Johnson EM, Brock HW, An W, (2008) Isolation and characterization of a novel H1.2 complex that acts as a repressor of p53-mediated transcription. J Biol Chem 283: 9113-9126
88. Ni J-Q, Liu L-P, Hess D, Rietdorf J, Sun F-L, (2006) Drosophila ribosomal proteins are associated with linker histone H1 and suppress gene transcription. Genes Dev 20: 1959-1973
89. Yang S-M, Kim BJ, Norwood Toro L, Skoultchi AI, (2013) H1 linker histone promotes epigenetic silencing by regulating both DNA methylation and histone H3 methylation. Proc Natl Acad Sci USA 110: 1708-1713
90. Medrzycki M, Zhang Y, Zhang W, Cao K, Pan C, Lailler N, McDonald JF, Bouhassira EE, Fan Y, (2014) Histone H1.3 suppresses h19 noncoding RNA expression and cell growth of ovarian cancer cells. Cancer Res 74: 6463-6473
91. Downs JA, Kosmidou E, Morgan A, Jackson SP, (2003) Suppression of homologous recombination by the Saccharomyces cerevisiae linker histone. Mol Cell 11: 1685-1692
92. Hashimoto H, Sonoda E, Takami Y, Kimura H, Nakayama T, Tachibana M, Takeda S, Shinkai Y, (2007) Histone H1 variant, H1R is involved in DNA damage response. DNA Repair 6: 1584-1595
93. Murga M, Jaco I, Fan Y, Soria R, Martinez-Pastor B, Cuadrado M, Yang S-M, Blasco MA, Skoultchi AI, Fernandez-Capetillo O, (2007) Global chromatin compaction limits the strength of the DNA damage response. J Cell Biol 178: 1101-1108
94. Thorslund T, Ripplinger A, Hoffmann S, Wild T, Uckelmann M, Villumsen B, Narita T, Sixma TK, Choudhary C, Bekker-Jensen S, et al, (2015) Histone H1 couples initiation and amplification of ubiquitin signaling after DNA damage. Nature (in press)
95. 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: 578-590
96. Dworkin-Rastl E, Kandolf H, Smith RC, (1994) The maternal histone H1 variant, H1M (B4 protein), is the predominant H1 histone in Xenopus pregastrula embryos. Dev Biol 161: 425-439
97. Saeki H, Ohsumi K, Aihara H, Ito T, Hirose S, Ura K, Kaneda Y, (2005) Linker histone variants control chromatin dynamics during early embryogenesis. Proc Natl Acad Sci USA 102: 5697-5702
98. Jullien J, Astrand C, Halley-Stott RP, Garrett N, Gurdon JB, (2010) Characterization of somatic cell nuclear reprogramming by oocytes in which a linker histone is required for pluripotency gene reactivation. Proc Natl Acad Sci USA 107: 5483-5488
99. Tanaka M, Kihara M, Meczekalski B, King GJ, Adashi EY, (2003) H1oo: a pre-embryonic H1 linker histone in search of a function. Mol Cell Endocrinol 202: 5-9
100. Hayakawa K, Ohgane J, Tanaka S, Yagi S, Shiota K, (2014) Oocyte-specific linker histone H1foo is an epigenomic modulator that decondenses chromatin and impairs pluripotency. Epigenetics 7: 1029-1036
101. Balhorn R, Chalkley R, Granner D, (1972) Lysine-rich histone phosphorylation. A positive correlation with cell replication. Biochemistry 11: 1094-1098
102. Wis̈niewski JR, Zougman A, Mann M, (2008) N(epsilon)-formylation of lysine is a widespread post-translational modification of nuclear proteins occurring at residues involved in regulation of chromatin function. Nucleic Acids Res 36: 570-577
103. Snijders APL, Pongdam S, Lambert SJ, Wood CM, Baldwin JP, Dickman MJ, (2008) Characterization of post-translational modifications of the linker histones H1 and H5 from chicken erythrocytes using mass spectrometry. J Proteome Res 7: 4326-4335
104. Kim MY, Zhang T, Kraus WL, (2005) Poly(ADP-ribosyl)ation by PARP-1: "PAR-laying" NAD+ into a nuclear signal. Genes Dev 19: 1951-1967
105. Poirier GG, Niedergang C, Champagne M, Mazen A, Mandel P, (1982) Adenosine diphosphate ribosylation of chicken-erythrocyte histones H1, H5 and high-mobility-group proteins by purified calf-thymus poly(adenosinediphosphate-ribose) polymerase. Eur J Biochem 127: 437-442
106. Jiang T, Zhou X, Taghizadeh K, Dong M, Dedon PC, (2007) N-formylation of lysine in histone proteins as a secondary modification arising from oxidative DNA damage. Proc Natl Acad Sci USA 104: 60-65
107. Talasz H, Sarg B, Lindner HH, (2009) Site-specifically phosphorylated forms of H1.5 and H1.2 localized at distinct regions of the nucleus are related to different processes during the cell cycle. Chromosoma 118: 693-709
108. Hergeth SP, Dundr M, Tropberger P, Zee BM, Garcia BA, Daujat S, Schneider R, (2011) Isoform-specific phosphorylation of human linker histone H1.4 in mitosis by the kinase Aurora B. J Cell Sci 124: 1623-1628
109. Happel N, Stoldt S, Schmidt B, Doenecke D, (2009) M phase-specific phosphorylation of histone H1.5 at threonine 10 by GSK-3. J Mol Biol 386: 339-350
110. Chu C-S, Hsu P-H, Lo P-W, Scheer E, Tora L, Tsai H-J, Tsai M-D, Juan L-J, (2011) Protein kinase A-mediated serine 35 phosphorylation dissociates histone H1.4 from mitotic chromosome. J Biol Chem 286: 35843-35851
111. Maresca TJ, Freedman B, Heald R, (2005) Histone H1 is essential for mitotic chromosome architecture and segregation in Xenopus laevis egg extracts. J Cell Biol 169: 859-869
112. Gurley LR, Valdez JG, Buchanan JS, (1995) Characterization of the mitotic specific phosphorylation site of histone H1. Absence of a consensus sequence for the p34cdc2/cyclin B kinase. J Biol Chem 270: 27653-27660
113. Th'ng JP, Guo XW, Swank RA, Crissman HA, Bradbury EM, (1994) Inhibition of histone phosphorylation by staurosporine leads to chromosome decondensation. J Biol Chem 269: 9568-9573
114. Alexandrow MG, (2005) Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. J Cell Biol 168: 875-886
115. Bhattacharjee RN, Banks GC, Trotter KW, Lee HL, Archer TK, (2001) Histone H1 phosphorylation by Cdk2 selectively modulates mouse mammary tumor virus transcription through chromatin remodeling. Mol Cell Biol 21: 5417-5425
116. Zheng Y, John S, Pesavento JJ, Schultz-Norton JR, Schiltz RL, Baek S, Nardulli AM, Hager GL, Kelleher NL, Mizzen CA, (2010) Histone H1 phosphorylation is associated with transcription by RNA polymerases I and II. J Cell Biol 189: 407-415
117. Chubb JE, Rea S, (2010) Core and linker histone modifications involved in the DNA damage response. Subcell Biochem 50: 17-42
118. Roque A, Ponte I, Arrondo JLR, Suau P, (2008) Phosphorylation of the carboxy-terminal domain of histone H1: effects on secondary structure and DNA condensation. Nucleic Acids Res 36: 4719-4726
119. Lopez R, Sarg B, Lindner H, Bartolome S, Ponte I, Suau P, Roque A, (2015) Linker histone partial phosphorylation: effects on secondary structure and chromatin condensation. Nucleic Acids Res 43: 4463-4476
120. Weiss T, Hergeth S, Zeissler U, Izzo A, Tropberger P, Zee BM, Dundr M, Garcia BA, Daujat S, Schneider R, (2010) Histone H1 variant-specific lysine methylation by G9a/KMT1C and Glp1/KMT1D. Epigenetics Chromatin 3: 7
121. Kuzmichev A, Jenuwein T, Tempst P, Reinberg D, (2004) Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol Cell 14: 183-193
122. Kamieniarz K, Izzo A, Dundr M, Tropberger P, Ozretic L, Kirfel J, Scheer E, Tropel P, Wisniewski JR, Tora L, et al, (2012) A dual role of linker histone H1.4 Lys 34 acetylation in transcriptional activation. Genes Dev 26: 797-802
123. Vaquero A, Scher M, Lee D, Erdjument-Bromage H, Tempst P, Reinberg D, (2004) Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol Cell 16: 93-105
124. Terme J-M, Millán-Ariño L, Mayor R, Luque N, Izquierdo-Bouldstridge A, Bustillos A, Sampaio C, Canes J, Font I, Sima N, et al, (2014) Dynamics and dispensability of variant-specific histone H1 Lys-26/Ser-27 and Thr-165 post-translational modifications. FEBS Lett 588: 2353-2362
125. Pham AD, Sauer F, (2000) Ubiquitin-activating/conjugating activity of TAFII250, a mediator of activation of gene expression in Drosophila. Science 289: 2357-2360
126. Christophorou MA, Castelo-Branco G, Halley-Stott RP, Oliveira CS, Loos R, Radzisheuskaya A, Mowen KA, Bertone P, Silva JCR, Zernicka-Goetz M, et al, (2014) Citrullination regulates pluripotency and histone H1 binding to chromatin. Nature 507: 104-108
127. Okosun J, Bödör C, Wang J, Araf S, Yang C-Y, Pan C, Boller S, Cittaro D, Bozek M, Iqbal S, et al, (2014) Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat Genet 46: 176-181
128. Takata H, Matsunaga S, Morimoto A, Ono-Maniwa R, Uchiyama S, Fukui K, (2007) H1.X with different properties from other linker histones is required for mitotic progression. FEBS Lett 581: 3783-3788
129. Tanaka Y, Kato S, Tanaka M, Kuji N, Yoshimura Y, (2003) Structure and expression of the human oocyte-specific histone H1 gene elucidated by direct RT-nested PCR of a single oocyte. Biochem Biophys Res Commun 304: 351-357
130. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ, (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191
131. Sarg B, Helliger W, Talasz H, Förg B, Lindner HH, (2006) Histone H1 phosphorylation occurs site-specifically during interphase and mitosis: identification of a novel phosphorylation site on histone H1. J Biol Chem 281: 6573-6580
132. Contreras A, Hale TK, Stenoien DL, Rosen JM, Mancini MA, Herrera RE, (2003) The dynamic mobility of histone H1 is regulated by cyclin/CDK phosphorylation. Mol Cell Biol 23: 8626-8636
133. Baatout S, Derradji H, (2006) About histone H1 phosphorylation during mitosis. Cell Biochem Funct 24: 93-94
134. Kuzmichev A, Margueron R, Vaquero A, Preissner TS, Scher M, Kirmizis A, Ouyang X, Brockdorff N, Abate-Shen C, Farnham P, et al, (2005) Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci USA 102: 1859-1864