A peek into the complex realm of histone phosphorylation

Molecular and Cellular Biology

Volumn 31, Issue 24, 2011, Pages 4858-4873

  Banerjee, Taraswi ^a   Chakravarti, Debabrata ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; HETEROCHROMATIN PROTEIN 1; HISTONE ACETYLTRANSFERASE; HISTONE H1; HISTONE H2A; HISTONE H2AX; HISTONE H2B; HISTONE H3; HISTONE H4; LYSINE; PROTEIN BMAL1; PROTEIN C FOS; PROTEIN P53; SERINE;

APOPTOSIS; CELL CYCLE PROGRESSION; CELL DIVISION; CHROMATIN CONDENSATION; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME CONDENSATION; DNA FRAGMENTATION; DNA REPAIR; EPIGENETICS; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HISTONE PHOSPHORYLATION; HISTONE UBIQUITINATION; HUMAN; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SHORT SURVEY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ANIMALS; CELL CYCLE; CELL DIVISION; CHROMATIN; DNA REPAIR; GENE EXPRESSION REGULATION; HISTONES; HUMANS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 83255192184     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05631-11     Document Type: Short Survey

References (143)

1. Ahn, S. H., et al. 2005. Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae. Cell 120:25-36.
2. Ajiro, K. 2000. Histone H2B phosphorylation in mammalian apoptotic cells. An association with DNA fragmentation. J. Biol. Chem. 275:439-443.
3. Ajiro, K., T. W. Borun, and L. H. Cohen. 1981. Phosphorylation states of different histone 1 subtypes and their relationship to chromatin functions during the HeLa S-3 cell cycle. Biochemistry 20:1445-1454.
4. Anest, V., P. C. Cogswell, and A. S. Baldwin, Jr. 2004. IκB kinase α and p65/RelA contribute to optimal epidermal growth factor-induced c-fos gene expression independent of IκBα degradation. J. Biol. Chem. 279:31183-31189.
5. Baker, S. P., et al. 2010. Histone H3 Thr 45 phosphorylation is a replication-associated post-translational modification in S. cerevisiae. Nat. Cell Biol. 12:294-298.
6. Barber, C. M., et al. 2004. The enhancement of histone H4 and H2A serine 1 phosphorylation during mitosis and S-phase is evolutionarily conserved. Chromosoma 112:360-371.
7. Barlow, C., et al. 1996. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86:159-171.
8. Bassing, C. H., et al. 2003. Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 114:359-370.
9. Bonenfant, D., et al. 2007. Analysis of dynamic changes in post-translational modifications of human histones during cell cycle by mass spectrometry. Mol. Cell. Proteomics 6:1917-1932.
10. Bottomley, M. J. 2004. Structures of protein domains that create or recognize histone modifications. EMBO Rep. 5:464-469.
11. Bradbury, E. M., R. J. Inglis, H. R. Matthews, and T. A. Langan. 1974. Molecular basis of control of mitotic cell division in eukaryotes. Nature 249:553-556.
12. Brittle, A. L., Y. Nanba, T. Ito, and H. Ohkura. 2007. Concerted action of Aurora B, Polo and NHK-1 kinases in centromere-specific histone 2A phosphorylation. Exp. Cell Res. 313:2780-2785.
13. Bungard, D., et al. 2010. Signaling kinase AMPK activates stress-promoted transcription via histone H2B phosphorylation. Science 329:1201-1205.
14. Burma, S., B. P. Chen, M. Murphy, A. Kurimasa, and D. J. Chen. 2001. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276:42462-42467.
15. Celeste, A., et al. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5:675-679.
16. Celeste, A., et al. 2002. Genomic instability in mice lacking histone H2AX. Science 296:922-927.
17. Cerutti, H., and J. A. Casas-Mollano. 2009. Histone H3 phosphorylation: universal code or lineage specific dialects? Epigenetics 4:71-75.
18. Chadee, D. N., et al. 1999. Increased Ser-10 phosphorylation of histone H3 in mitogen-stimulated and oncogene-transformed mouse fibroblasts. J. Biol. Chem. 274:24914-24920.
19. Chadee, D. N., et al. 1995. Increased phosphorylation of histone H1 in mouse fibroblasts transformed with oncogenes or constitutively active mitogen-activated protein kinase kinase. J. Biol. Chem. 270:20098-20105.
20. Cheung, P., C. D. Allis, and P. Sassone-Corsi. 2000. Signaling to chromatin through histone modifications. Cell 103:263-271.
21. Cheung, W. L., et al. 2003. Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113:507-517.
22. Cheung, W. L., et al. 2005. Phosphorylation of histone H4 serine 1 during DNA damage requires casein kinase II in S. cerevisiae. Curr. Biol. 15:656-660.
23. Clements, A., et al. 2003. Structural basis for histone and phosphohistone binding by the GCN5 histone acetyltransferase. Mol. Cell 12:461-473.
24. Cook, P. J., et al. 2009. Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458:591-596.
25. Cruickshank, M. N., P. Besant, and D. Ulgiati. 2010. The impact of histone post-translational modifications on developmental gene regulation. Amino Acids 39:1087-1105.
26. Dawson, M. A., et al. 2009. JAK2 phosphorylates histone H3Y41 and excludes HP1α from chromatin. Nature 461:819-822.
27. Dey, A., F. Chitsaz, A. Abbasi, T. Misteli, and K. Ozato. 2003. The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc. Natl. Acad. Sci. U. S. A. 100:8758-8763.
28. Dhalluin, C., et al. 1999. Structure and ligand of a histone acetyltransferase bromodomain. Nature 399:491-496.
29. Di Croce, L., and R. Shiekhattar. 2008. Thrilling transcription through threonine phosphorylation. Nat. Cell Biol. 10:5-6.
30. Downs, J. A., et al. 2004. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16:979-990.
31. Downs, J. A., N. F. Lowndes, and S. P. Jackson. 2000. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408:1001-1004.
32. Dresser, M. E., and C. N. Giroux. 1988. Meiotic chromosome behavior in spread preparations of yeast. J. Cell Biol. 106:567-573.
33. Drobic, B., K. L. Dunn, P. S. Espino, and J. R. Davie. 2006. Abnormalities of chromatin in tumor cells. EXS 2006:25-47.
34. Duan, Q., H. Chen, M. Costa, and W. Dai. 2008. Phosphorylation of H3S10 blocks the access of H3K9 by specific antibodies and histone methyltransferase. Implication in regulating chromatin dynamics and epigenetic inheritance during mitosis. J. Biol. Chem. 283:33585-33590.
35. Duncan, E. A., V. Anest, P. Cogswell, and A. S. Baldwin. 2006. The kinases MSK1 and MSK2 are required for epidermal growth factor-induced, but not tumor necrosis factor-induced, histone H3 Ser10 phosphorylation. J. Biol. Chem. 281:12521-12525.
36. Elson, A., et al. 1996. Pleiotropic defects in ataxia-telangiectasia proteindeficient mice. Proc. Natl. Acad. Sci. U. S. A. 93:13084-13089.
37. Fink, M., D. Imholz, and F. Thoma. 2007. Contribution of the serine 129 of histone H2A to chromatin structure. Mol. Cell. Biol. 27:3589-3600.
38. Fischle, W., et al. 2005. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438:1116-1122.
39. Fry, C. J., M. A. Shogren-Knaak, and C. L. Peterson. 2004. Histone H3 amino-terminal tail phosphorylation and acetylation: synergistic or independent transcriptional regulatory marks? Cold Spring Harb. Symp. Quant. Biol. 69:219-226.
40. Furumatsu, T., and H. Asahara. 2010. Histone acetylation influences the activity of Sox9-related transcriptional complex. Acta Med. Okayama 64: 351-357.
41. Garcia, B. A., et al. 2005. Modifications of human histone H3 variants during mitosis. Biochemistry 44:13202-13213.
42. Glover, D. M., M. H. Leibowitz, D. A. McLean, and H. Parry. 1995. Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 81:95-105.
43. Goto, H., et al. 1999. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274:25543-25549.
44. Goto, H., Y. Yasui, E. A. Nigg, and M. Inagaki. 2002. Aurora-B phosphorylates Histone H3 at serine28 with regard to the mitotic chromosome condensation. Genes Cells 7:11-17.
45. Grune, T., et al. 2003. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol. Cell 12:449-460.
46. Gu, Y., et al. 1997. Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity 7:653-665.
47. Gurley, L. R., J. A. D'Anna, S. S. Barham, L. L. Deaven, and R. A. Tobey. 1978. Histone phosphorylation and chromatin structure during mitosis in Chinese hamster cells. Eur. J. Biochem. 84:1-15.
48. Gurley, L. R., J. G. Valdez, and J. S. Buchanan. 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.
49. Gurley, L. R., R. A. Walters, S. S. Barham, and L. L. Deaven. 1978. Heterochromatin and histone phosphorylation. Exp. Cell Res. 111:373-383.
50. Hake, S. B., and C. D. Allis. 2006. Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis." Proc. Natl. Acad. Sci. U. S. A. 103:6428-6435.
51. Hale, T. K., A. Contreras, A. J. Morrison, and R. E. Herrera. 2006. Phosphorylation of the linker histone H1 by CDK regulates its binding to HP1α. Mol. Cell 22:693-699.
52. Hendzel, M. J., et al. 1997. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348-360.
53. Houben, A., et al. 2007. Phosphorylation of histone H3 in plants-a dynamic affair. Biochim. Biophys. Acta 1769:308-315.
54. Hsu, J. Y., et al. 2000. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102:279-291.
55. Huang, C. K., and G. R. Laramee. 1991. Stimulation of a histone H4 protein kinase in Triton X-100 lysates of rabbit peritoneal neutrophils pretreated with chemotactic factors: effect of leukotriene B4 and cytochalasin B. J. Leukoc. Biol. 49:158-162.
56. Hunter, T. 2009. Tyrosine phosphorylation: thirty years and counting. Curr. Opin. Cell Biol. 21:140-146.
57. Hurd, P. J., et al. 2009. Phosphorylation of histone H3 Thr-45 is linked to apoptosis. J. Biol. Chem. 284:16575-16583.
58. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293:1074-1080.
59. Jiang, L., et al. 2007. Global assessment of combinatorial post-translational modification of core histones in yeast using contemporary mass spectrometry. LYS4 trimethylation correlates with degree of acetylation on the same H3 tail. J. Biol. Chem. 282:27923-27934.
60. Johansen, K. M., and J. Johansen. 2006. Regulation of chromatin structure by histone H3S10 phosphorylation. Chromosome Res. 14:393-404.
61. Joo, H. Y., et al. 2007. Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 449:1068-1072.
62. Kadam, S., and B. M. Emerson. 2003. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol. Cell 11:377-389.
63. Karam, C. S., W. A. Kellner, N. Takenaka, A. W. Clemmons, and V. G. Corces. 2010. 14-3-3 mediates histone cross-talk during transcription elongation in Drosophila. PLoS Genet. 6:e1000975.
64. Kawashima, S. A., Y. Yamagishi, T. Honda, K. Ishiguro, and Y. Watanabe. 2010. Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327:172-177.
65. Khan, S. N., and A. U. Khan. 2010. Role of histone acetylation in cell physiology and diseases: an update. Clin. Chim. Acta 411:1401-1411.
66. Kobayashi, S., S. Nakagawa, N. Uehara, H. Hamashima, and A. Tanaka. 2002. DNA topology: topological transformation of DNA by reaction of cisplatin-DNA-core histone complexes with human DNA topoisomerase. Nucleic Acids Res. Suppl. 2002:283-284.
67. Kornberg, R. D. 1977. Structure of chromatin. Annu. Rev. Biochem. 46: 931-954.
68. Kotova, E., et al. 2011. Drosophila histone H2A variant (H2Av) controls poly(ADP-ribose) polymerase 1 (PARP1) activation in chromatin. Proc. Natl. Acad. Sci. U. S. A. 108:6205-6210.
69. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128:693-705.
70. Krishnamoorthy, T., et al. 2006. Phosphorylation of histone H4 Ser1 regulates sporulation in yeast and is conserved in fly and mouse spermatogenesis. Genes Dev. 20:2580-2592.
71. Kruger, W., et al. 1995. Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/ SNF complex for transcription. Genes Dev. 9:2770-2779.
72. Kulis, M., and M. Esteller. 2010. DNA methylation and cancer. Adv. Genet. 70:27-56.
73. Kutney, S. N., R. Hong, T. Macfarlan, and D. Chakravarti. 2004. A signaling role of histone-binding proteins and INHAT subunits pp32 and Set/ TAF-Iβ in integrating chromatin hypoacetylation and transcriptional repression. J. Biol. Chem. 279:30850-30855.
74. Lamia, K. A., et al. 2009. AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326:437-440.
75. Langan, T. A., et al. 1989. Mammalian growth-associated H1 histone kinase: a homolog of cdc2+/CDC28 protein kinases controlling mitotic entry in yeast and frog cells. Mol. Cell. Biol. 9:3860-3868.
76. Lau, P. N., and P. Cheung. 2011. Histone code pathway involving H3 S28 phosphorylation and K27 acetylation activates transcription and antagonizes polycomb silencing. Proc. Natl. Acad. Sci. U. S. A. 108:2801-2806.
77. Lau, P. N., and P. Cheung. 2011. Unlocking polycomb silencing through histone H3 phosphorylation. Cell Cycle 10:1514-1515.
78. Li, X. N., et al. 2009. Activation of the AMPK-FOXO3 pathway reduces fatty acid-induced increase in intracellular reactive oxygen species by upregulating thioredoxin. Diabetes 58:2246-2257.
79. Lo, W. S., et al. 2001. Snf1-a histone kinase that works in concert with the histone acetyltransferase Gcn5 to regulate transcription. Science 293:1142-1146.
80. Lo, W. S., et al. 2000. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5:917-926.
81. Loomis, R. J., et al. 2009. Chromatin binding of SRp20 and ASF/SF2 and dissociation from mitotic chromosomes is modulated by histone H3 serine 10 phosphorylation. Mol. Cell 33:450-461.
82. Luger, K., A. W. Mader, R. K. Richmond, D. F. Sargent, and T. J. Richmond. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251-260.
83. Luger, K., T. J. Rechsteiner, A. J. Flaus, M. M. Waye, and T. J. Richmond. 1997. Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 272:301-311.
84. Macdonald, N., et al. 2005. Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3. Mol. Cell 20:199-211.
85. Macurek, L., et al. 2010. Wip1 phosphatase is associated with chromatin and dephosphorylates gammaH2AX to promote checkpoint inhibition. Oncogene 29:2281-2291.
86. Mahadevan, L. C., A. C. Willis, and M. J. Barratt. 1991. Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell 65:775-783.
87. Maile, T., S. Kwoczynski, R. J. Katzenberger, D. A. Wassarman, and F. Sauer. 2004. TAF1 activates transcription by phosphorylation of serine 33 in histone H2B. Science 304:1010-1014.
88. Maruyama, T., et al. 2002. A mammalian bromodomain protein, brd4, interacts with replication factor C and inhibits progression to S phase. Mol. Cell. Biol. 22:6509-6520.
89. Metzger, E., et al. 2010. Phosphorylation of histone H3T6 by PKCβ(I) controls demethylation at histone H3K4. Nature 464:792-796.
90. Metzger, E., et al. 2008. Phosphorylation of histone H3 at threonine 11 establishes a novel chromatin mark for transcriptional regulation. Nat. Cell Biol. 10:53-60.
91. Morrison, A. J., et al. 2004. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119: 767-775.
92. Nelson, C. J., H. Santos-Rosa, and T. Kouzarides. 2006. Proline isomerization of histone H3 regulates lysine methylation and gene expression. Cell 126:905-916.
93. Ng, S. S., et al. 2007. Crystal structures of histone demethylase JMJD2A reveal basis for substrate specificity. Nature 448:87-91.
94. Nishioka, K., et al. 2002. PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell 9:1201-1213.
95. Nussenzweig, A., et al. 1996. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382:551-555.
96. Papamichos-Chronakis, M., J. E. Krebs, and C. L. Peterson. 2006. Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev. 20:2437-2449.
97. Park, E. J., D. W. Chan, J. H. Park, M. A. Oettinger, and J. Kwon. 2003. DNA-PK is activated by nucleosomes and phosphorylates H2AX within the nucleosomes in an acetylation-dependent manner. Nucleic Acids Res. 31: 6819-6827.
98. Park, J. H., M. S. Cosgrove, E. Youngman, C. Wolberger, and J. D. Boeke. 2002. A core nucleosome surface crucial for transcriptional silencing. Nat. Genet. 32:273-279.
99. Preuss, U., G. Landsberg, and K. H. Scheidtmann. 2003. Novel mitosisspecific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res. 31:878-885.
100. Prigent, C., and S. Dimitrov. 2003. Phosphorylation of serine 10 in histone H3, what for? J. Cell Sci. 116:3677-3685.
101. Rogakou, E. P., D. R. Pilch, A. H. Orr, V. S. Ivanova, and W. M. Bonner. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:5858-5868.
102. Roth, S. Y., and C. D. Allis. 1992. Chromatin condensation: does histone H1 dephosphorylation play a role? Trends Biochem. Sci. 17:93-98.
103. Sahin, M., E. Sahin, S. Gumuslu, A. Erdogan, and M. Gultekin. 2010. DNA methylation or histone modification status in metastasis and angiogenesisrelated genes: a new hypothesis on usage of DNMT inhibitors and Sadenosylmethionine for genome stability. Cancer Metastasis Rev. 29:655-676.
104. Sarg, B., W. Helliger, H. Talasz, B. Forg, and H. H. Lindner. 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.
105. Sassone-Corsi, P., et al. 1999. Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. Science 285:886-891.
106. Schneider, R., A. J. Bannister, C. Weise, and T. Kouzarides. 2004. Direct binding of INHAT to H3 tails disrupted by modifications. J. Biol. Chem. 279:23859-23862.
107. Schreiber, S. L., and B. E. Bernstein. 2002. Signaling network model of chromatin. Cell 111:771-778.
108. Selvi, B. R., J. C. Cassel, T. K. Kundu, and A. L. Boutillier. 2010. Tuning acetylation levels with HAT activators: therapeutic strategy in neurodegenerative diseases. Biochim. Biophys. Acta 1799:840-853.
109. Seo, S. B., et al. 2002. Regulation of histone acetylation and transcription by nuclear protein pp32, a subunit of the INHAT complex. J. Biol. Chem. 277:14005-14010.
110. Seo, S. B., et al. 2001. Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the set oncoprotein. Cell 104:119-130.
111. Shimada, M., M. Haruta, H. Niida, K. Sawamoto, and M. Nakanishi. 2010. Protein phosphatase 1gamma is responsible for dephosphorylation of histone H3 at Thr 11 after DNA damage. EMBO Rep. 11:883-889.
112. Shimada, M., et al. 2008. Chk1 is a histone H3 threonine 11 kinase that regulates DNA damage-induced transcriptional repression. Cell 132:221-232.
113. Shoemaker, C. B., and R. Chalkley. 1978. An H3 histone-specific kinase isolated from bovine thymus chromatin. J. Biol. Chem. 253:5802-5807.
114. Shogren-Knaak, M. A., C. J. Fry, and C. L. Peterson. 2003. A native peptide ligation strategy for deciphering nucleosomal histone modifications. J. Biol. Chem. 278:15744-15748.
115. Singh, R. K., and A. Gunjan. 2011. Histone tyrosine phosphorylation comes of age. Epigenetics 6:153-160.
116. Solier, S., and Y. Pommier. 2009. The apoptotic ring: a novel entity with phosphorylated histones H2AX and H2B and activated DNA damage response kinases. Cell Cycle. 8:1853-1859.
117. Soloaga, A., et al. 2003. MSK2 and MSK1 mediate the mitogen-and stressinduced phosphorylation of histone H3 and HMG-14. EMBO J. 22:2788-2797.
118. Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifications. Nature 403:41-45.
119. Stucki, M., and S. P. Jackson. 2006. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amsterdam) 5:534-543.
120. Taverna, S. D., H. Li, A. J. Ruthenburg, C. D. Allis, and D. J. Patel. 2007. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 14:1025-1040.
121. Teperek-Tkacz, M., M. Meglicki, M. Pasternak, J. Z. Kubiak, and E. Borsuk. 2010. Phosphorylation of histone H3 serine 10 in early mouse embryos: active phosphorylation at late S phase and differential effects of ZM447439 on first two embryonic mitoses. Cell Cycle 9:4674-4687.
122. Thiriet, C., and J. J. Hayes. 2005. Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev. 19:677-682.
123. Thomson, S., A. L. Clayton, and L. C. Mahadevan. 2001. Independent dynamic regulation of histone phosphorylation and acetylation during immediate-early gene induction. Mol. Cell 8:1231-1241.
124. Unal, E., et al. 2004. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16:991-1002.
125. van Attikum, H., O. Fritsch, B. Hohn, and S. M. Gasser. 2004. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777-788.
126. Van Hooser, A., D. W. Goodrich, C. D. Allis, B. R. Brinkley, and M. A. Mancini. 1998. Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J. Cell Sci. 111(Pt. 23):3497-3506.
127. Walter, W., et al. 2008. 14-3-3 interaction with histone H3 involves a dual modification pattern of phosphoacetylation. Mol. Cell. Biol. 28:2840-2849.
128. Wang, F., et al. 2010. Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330:231-235.
129. Ward, I. M., and J. Chen. 2001. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276:47759-47762.
130. Wei, Y., L. Yu, J. Bowen, M. A. Gorovsky, and C. D. Allis. 1999. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97:99-109.
131. Wei, Y. F., and H. R. Matthews. 1990. A filter-based protein kinase assay selective for alkali-stable protein phosphorylation and suitable for acidlabile protein phosphorylation. Anal. Biochem. 190:188-192.
132. Wen, W., et al. 2010. MST1 promotes apoptosis through phosphorylation of histone H2AX. J. Biol. Chem. 285:39108-39116.
133. Winter, S., et al. 2008. 14-3-3 proteins recognize a histone code at histone H3 and are required for transcriptional activation. EMBO J. 27:88-99.
134. Xiao, A., et al. 2009. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457:57-62.
135. Yamamoto, Y., U. N. Verma, S. Prajapati, Y. T. Kwak, and R. B. Gaynor. 2003. Histone H3 phosphorylation by IKK-α is critical for cytokine-induced gene expression. Nature 423:655-659.
136. Zhang, Q., Q. Zhong, A. G. Evans, D. Levy, and S. Zhong. 2011. Phosphorylation of histone H3 serine 28 modulates RNA polymerase III-dependent transcription. Oncogene 30:3705-3715.
137. Zhang, Y., K. Griffin, N. Mondal, and J. D. Parvin. 2004. Phosphorylation of histone H2A inhibits transcription on chromatin templates. J. Biol. Chem. 279:21866-21872.
138. Zheng, Y., et al. 2010. Histone H1 phosphorylation is associated with transcription by RNA polymerases I and II. J. Cell Biol. 189:407-415.
139. Zhong, X. Y., P. Wang, J. Han, M. G. Rosenfeld, and X. D. Fu. 2009. SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol. Cell 35:1-10.
140. Zhu, F., et al. 2011. Phosphorylation of H2AX at Ser139 and a new phosphorylation site Ser16 by RSK2 decreases H2AX ubiquitination and inhibits cell transformation. Cancer Res. 71:393-403.
141. Zhu, Q., and A. A. Wani. 2010. Histone modifications: crucial elements for damage response and chromatin restoration. J. Cell Physiol. 223:283-288.
142. Zippo, A., A. De Robertis, R. Serafini, and S. Oliviero. 2007. PIM1-dependent phosphorylation of histone H3 at serine 10 is required for MYCdependent transcriptional activation and oncogenic transformation. Nat. Cell Biol. 9:932-944.
143. Zippo, A., et al. 2009. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138: 1122-1136.