Post-translational modifications of the linker histone variants and their association with cell mechanisms

FEBS Journal

Volumn 276, Issue 14, 2009, Pages 3685-3697

  Wood, Christopher ^a   Snijders, Ambrosius ^b   Williamson, James ^b   Reynolds, Colin ^b   Baldwin, John ^c   Dickman, Mark ^b  

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c DARESBURY LABORATORY   (United Kingdom)

Author keywords

Abundance; Acid extraction; Cancer; Cell cycle; Disease; Linker histone; MS; Post translational modification; PTM; PTM function

Indexed keywords

CYCLIN DEPENDENT KINASE; DNA METHYLTRANSFERASE; HISTONE; HISTONE DEACETYLASE; HISTONE H1; LYSINE; MICRORNA;

ACETYLATION; AMINO TERMINAL SEQUENCE; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL STRAIN MCF 7; CELL TYPE; CHICKEN; CHROMATIN STRUCTURE; CPG ISLAND; DISEASE ASSOCIATION; DNA METHYLATION; ENZYME ACTIVE SITE; ENZYME PHOSPHORYLATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENE SILENCING; HELA CELL; HUMAN; MITOSIS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NEOPLASM; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; UBIQUITINATION; ANIMAL; CELL FUNCTION; CHEMISTRY; GENETIC EPIGENESIS; GENETIC VARIABILITY; GENETICS; METABOLISM; PHOSPHORYLATION; SPECIES DIFFERENCE;

ANIMALS; CELL PHYSIOLOGICAL PHENOMENA; EPIGENESIS, GENETIC; GENETIC VARIATION; HISTONES; HUMANS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SPECIES SPECIFICITY;

EID: 67650658841     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07079.x     Document Type: Review

References (69)

1. Bowman RV, Yang IA, Semmler AB Fong KM (2006) Epigenetics of lung cancer. Respirology 11, 355 365. (Pubitemid 43824331)
2. Chuang JC Jones PA (2007) Epigenetics and microRNAs. Pediatr Res 61, 24R 29R. (Pubitemid 46653064)
3. Wood CM (2008) Molecular kinetics and targeting within the nucleus. Curr Chem Biol 2, 229 236.
4. Li LC, Carroll PR Dahiya R (2005) Epigenetic changes in prostate cancer: implication for diagnosis and treatment. J Natl Cancer Inst 97, 103 115. (Pubitemid 40277090)
5. Lohrum M, Stunnenberg HG Logie C (2007) The new frontier in cancer research: deciphering cancer epigenetics. Int J Biochem Cell Biol 39, 1450 1461. (Pubitemid 47031040)
6. Takeshima H, Suetake I Tajima S (2008) Mouse Dnmt3a preferentially methylates linker DNA and is inhibited by histone H1. J Mol Biol 283, 810 821.
7. Li T, Vu TH, Ulaner GA, Littman E, Ling JQ, Chen HL, Hu JF, Behr B, Giudice L Hoffman AR (2005) IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch. Mol Hum Reprod 11, 631 640. (Pubitemid 41672242)
8. Galm O, Herman JG Baylin SB (2006) The fundamental role of epigenetics in hematopoietic malignancies. Blood Rev 20, 1 13. (Pubitemid 43106714)
9. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, Chen WD, Pretlow TP, Yang B, Akiyama Y, Van Engeland M et al. (2004) Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 36, 417 422. (Pubitemid 38437267)
10. Esteller M, Fraga MF, Paz MF, Campo E, Colomer D, Novo FJ, Calasanz MJ, Galm O, Guo M, Benitez J et al. (2002) Cancer epigenetics and methylation. Science 297, 1807 1808.
11. Lu Q, Qiu X, Hu N, Wen H, Su Y Richardson BC (2006) Epigenetics, disease, and therapeutic interventions. Ageing Res Rev 5, 449 467. (Pubitemid 44437040)
12. Baylin SB (2005) DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol 2, S4 S11.
13. Allan J, Hartman PG, Crane-Robinson C Aviles FX (1980) The structure of histone H1 and its location in chromatin. Nature 288, 675 679. (Pubitemid 11168522)
14. Fan L Roberts VA (2006) Complex of linker histone H5 with the nucleosome and its implications for chromatin packing. Proc Natl Acad Sci USA 103, 8384 8389. (Pubitemid 43838464)
15. Brown DT, Izard T Misteli T (2006) Mapping the interaction surface of linker histone H1 with the nucleosome of native chromatin in vivo. Nat Struct Mol Biol 13, 250 255. (Pubitemid 43348511)
16. Routh A, Sandin S Rhodes D (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc Natl Acad Sci USA 105, 8872 8877.
17. Robinson PJ, Fairall L, Huynh VA Rhodes D (2006) EM measurements define the dimensions of the '30-nm' chromatin fiber: evidence for a compact, interdigitated structure. Proc Natl Acad Sci USA 103, 6506 6511.
18. Bordas J, Perez-Grau L, Koch MH, Vega MC Nave C (1986) The superstructure of chromatin and its condensation mechanism. II. Theoretical analysis of the X-ray scattering patterns and model calculations. Eur Biophys J 13, 175 185.
19. Dorigo B, Schalch T, Kulangara A, Duda S, Schroeder RR Richmond TJ (2004) Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science 306, 1571 1573. (Pubitemid 39564956)
20. 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. (Pubitemid 10205723)
21. 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.
22. Khochbin S (2001) Histone H1 diversity: bridging regulatory signals to linker histone function. Gene 271, 1 12. (Pubitemid 32539140)
23. Izzo A, Kamieniarz K Schneider R (2008) The histone H1 family: specific members, specific functions? Biol Chem 389, 333 343. (Pubitemid 351773907)
24. Shen X Gorovsky MA (1996) Linker histone H1 regulates specific gene expression but not global transcription in vivo. Cell 86, 475 483. (Pubitemid 26272087)
25. 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)
26. 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.
27. Gabrilovich DI, Cheng P, Fan Y, Yu B, Nikitina E, Sirotkin A, Shurin M, Oyama T, Adachi Y, Nadaf S et al. (2002) H1(0) histone and differentiation of dendritic cells. A molecular target for tumor-derived factors. J Leukoc Biol 72, 285 296.
28. Th'ng JP, 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)
29. Konishi A, Shimizu S, Hirota J, Takao T, Fan Y, Matsuoka Y, Zhang L, Yoneda Y, Fujii Y, Skoultchi AI et al. (2003) Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 114, 673 688. (Pubitemid 37186764)
30. Gillespie DA Vousden KH (2003) The secret life of histones. Cell 114, 655 656. (Pubitemid 37186759)
31. Yan N Shi Y (2003) Histone H1.2 as a trigger for apoptosis. Nat Struct Biol 10, 983 985. (Pubitemid 37500487)
32. Conn KL, Hendzel MJ Schang LM (2008) Linker histones are mobilized during infection with herpes simplex virus type 1. J Virol 82, 8629 8646.
33. Okamura H, Yoshida K, Amorim BR Haneji T (2008) Histone H1.2 is translocated to mitochondria and associates with Bak in bleomycin-induced apoptotic cells. J Cell Biochem 103, 1488 1496.
34. Sarg B, Gréen A, Söderkvist P, Helliger W, Rundquist I Lindner HH (2005) Characterization of sequence variations in human histone H1.2 and H1.4 subtypes. FEBS J 272, 3673 3683. (Pubitemid 41021179)
35. Clarke HJ, McLay DW Mohamed OA (1998) Linker histone transitions during mammalian oogenesis and embryogenesis. Dev Genet 22, 17 30. (Pubitemid 28114772)
36. Bradbury EM, Inglis RJ Matthews HR (1974) Control of cell division by very lysine rich histone (F1) phosphorylation. Nature 247, 257 261.
37. He J, Yang Q Chang LJ (2005) Dynamic DNA methylation and histone modifications contribute to lentiviral transgene silencing in murine embryonic carcinoma cells. J Virol 79, 13497 13508. (Pubitemid 41508162)
38. Wu J, Wang SH, Potter D, Liu JC, Smith LT, Wu YZ, Huang TH Plass C (2007) Diverse histone modifications on histone 3 lysine 9 and their relation to DNA methylation in specifying gene silencing. BMC Genomics 8, 131, doi :.
39. Gilbert N, Thomson I, Boyle S, Allan J, Ramsahoye B Bickmore WA (2007) DNA methylation affects nuclear organization, histone modifications, and linker histone binding but not chromatin compaction. J Cell Biol 177, 401 411. (Pubitemid 46718270)
40. 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.
41. 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. (Pubitemid 43847591)
42. 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. (Pubitemid 40040376)
43. Wisniewski 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. (Pubitemid 46152693)
44. Snijders AP, 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.
45. Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, Shabanowitz J, Hunt DF White FM (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20, 301 305. (Pubitemid 34205425)
46. Ma M, Kutz-Naber KK Li L (2007) Methyl esterification assisted MALDI FTMS characterization of the orcokinin neuropeptide family. Anal Chem 79, 673 681. (Pubitemid 46106135)
47. 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.
48. 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. (Pubitemid 36576908)
49. 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. (Pubitemid 38515646)
50. 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. (Pubitemid 46067984)
51. Banks GC, Deterding LJ, Tomer KB Archer TK (2001) Hormone-mediated dephosphorylation of specific histone H1 isoforms. J Biol Chem 276, 36467 36473.
52. Villar-Garea A Imhof A (2008) Fine mapping of posttranslational modifications of the linker histone H1 from Drosophila melanogaster. PLoS ONE 3, e1553, doi :.
53. Lelièvre SA, Weaver VM, Nickerson JA, Larabell CA, Bhaumik A, Petersen OW Bissell MJ (1998) Tissue phenotype depends on reciprocal interactions between the extracellular matrix and the structural organization of the nucleus. Proc Natl Acad Sci USA 95, 14711 14716. (Pubitemid 29003695)
54. Zink D, Fischer AH Nickerson JA (2004) Nuclear structure in cancer cells. Nat Rev Cancer 4, 677 687. (Pubitemid 39215066)
55. Gong CX, Liu F, Grundke-Iqbal I Iqbal K (2005) Post-translational modifications of tau protein in Alzheimer's disease. J Neural Transm 112, 813 838. (Pubitemid 40655573)
56. Huq M, Gupta P Wei LN (2008) Post-translational modifications of nuclear co-repressor RIP140: a therapeutic target for metabolic diseases. Curr Med Chem 15, 386 392. (Pubitemid 351266944)
57. Dai B Rasmussen TP (2007) Global epiproteomic signatures distinguish embryonic stem cells from differentiated cells. Stem Cells 25, 2567 2574. (Pubitemid 47582749)
58. Godman CA, Joshi R, Tierney BR, Greenspan E, Rasmussen TP, Wang HW, Shin DG, Rosenberg DW Giardina C (2008) HDAC3 impacts multiple oncogenic pathways in colon cancer cells with effects on Wnt and vitamin D signalling. Cancer Biol Ther 7, 1570 1580.
59. Phanstiel D, Brumbaugh J, Berggren WT, Conard K, Feng X, Levenstein ME, McAlister GC, Thomson JA Coon JJ (2008) Mass spectrometry identifies and quantifies 74 unique histone H4 isoforms in differentiating human embryonic stem cells. Proc Natl Acad Sci USA 105, 4093 4098. (Pubitemid 351754340)
60. 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, doi :.
61. Klumpp S Krieglstein J (2002) Phosphorylation and dephosphorylation of histidine residues in proteins. Eur J Biochem 269, 1067 1071. (Pubitemid 34175364)
62. Auzély-Velty R Rinaudo M (2003) Synthesis of starch derivatives with labile cationic groups. Int J Biol Macromol 31, 123 129. (Pubitemid 36144031)
63. Shechter D, Dormann HL, Allis CD Hake SB (2007) Extraction, purification and analysis of histones. Nat Protoc 2, 1445 1457. (Pubitemid 46952324)
64. Garcia BA, Joshi S, Thomas CE, Chitta RK, Diaz RL, Busby SA, Andrews PC, Ogorzalek Loo RR, Shabanowitz J, Kelleher NL et al. (2006) Comprehensive phosphoprotein analysis of linker histone H1 from Tetrahymena thermophila. Mol Cell Proteomics 5, 1593 1609. (Pubitemid 44480388)
65. Bonaldi T, Imhof A Regula JT (2004) A combination of different mass spectroscopic techniques for the analysis of dynamic changes of histone modifications. Proteomics 4, 1382 1396. (Pubitemid 38648027)
66. Lindner HH (2008) Analysis of histones, histone variants, and their post-translationally modified forms. Electrophoresis 29, 2516 2532. (Pubitemid 351911879)
67. Mizzen CA, Dou Y, Liu Y, Cook RG, Gorovsky MA Allis CD (1999) Identification and mutation of phosphorylation sites in a linker histone. Phosphorylation of macronuclear H1 is not essential for viability in tetrahymena. J Biol Chem 274, 14533 14536.
68. Krueger KE Srivastava S (2006) Posttranslational protein modifications: current implications for cancer detection, prevention and therapeutics. Mol Cell Proteomics 5, 1799 1810. (Pubitemid 44688189)
69. Li H, Coghlan A, Ruan J, Coin LJ, Hériché JK, Osmotherly L, Li R, Liu T, Zhang Z, Bolund L et al. (2006) TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res 34, D572 D580.