Histone modifications in DNA damage response

Science China Life Sciences

Volumn 59, Issue 3, 2016, Pages 257-270

  Cao, Lin Lin ^a,d   Shen, Changchun ^a   Zhu, Wei Guo ^a,b,c  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b Tsinghua University   (China)

^c Shenzhen University   (China)

^d PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

Author keywords

chromatin; DNA damage response; DNA repair; histone modifications

Indexed keywords

CHROMATIN; HISTONE;

ANIMAL; CHROMATIN; DNA DAMAGE; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING;

ANIMALS; CHROMATIN; DNA DAMAGE; HISTONES; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84959483426     PISSN: 16747305     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11427-016-5011-z     Document Type: Review

References (206)

1. Adamietz, P., and Rudolph, A. (1984). ADP-ribosylation of nuclear proteins in vivo. Identification of histone H2B as a major acceptor for mono- and poly(ADP-ribose) in dimethyl sulfate-treated hepatoma AH7974 cells. J Biol Chem 259, 6841–6846.
2. Arnaudo, A.M., and Garcia, B.A. (2013). Proteomic characterization of novel histone post-translational modifications. Epigenet Chromat 6, 24.
3. Ayoub, N., Jeyasekharan, A.D., Bernal, J.A., and Venkitaraman, A.R. (2008). HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature 453, 682–686.
4. Ayrapetov, M.K., Gursoy-Yuzugullu, O., Xu, C., Xu, Y., and Price, B.D. (2014). DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc Natl Acad Sci USA 111, 9169–9174.
5. Bannister, A.J., and Kouzarides, T. (2011). Regulation of chromatin by histone modifications. Cell Res 21, 381–395.
6. Bassing, C.H., Chua, K.F., Sekiguchi, J., Suh, H., Whitlow, S.R., Fleming, J.C., Monroe, B.C., Ciccone, D.N., Yan, C., Vlasakova, K., Livingston, D.M., Ferguson, D.O., Scully, R., and Alt, F.W. (2002). Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc Natl Acad Sci USA 99, 8173–8178.
7. Bassing, C.H., Suh, H., Ferguson, D.O., Chua, K.F., Manis, J., Eckersdorff, M., Gleason, M., Bronson, R., Lee, C., and Alt, F.W. (2003). Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 114, 359–370.
8. Battu, A., Ray, A., and Wani, A.A. (2011). ASF1A and ATM regulate H3K56-mediated cell-cycle checkpoint recovery in response to UV irradiation. Nucleic Acids Res 39, 7931–7945.
9. Bekker-Jensen, S., Rendtlew Danielsen, J., Fugger, K., Gromova, I., Nerstedt, A., Lukas, C., Bartek, J., Lukas, J., and Mailand, N. (2010). HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat Cell Biol 12, 80–86; sup pp 81–12.
10. Bennett, E.J., and Harper, J.W. (2008). DNA damage: ubiquitin marks the spot. Nat Struct Mol Biol 15, 20–22.
11. Bergink, S., Salomons, F.A., Hoogstraten, D., Groothuis, T.A., de Waard, H., Wu, J., Yuan, L., Citterio, E., Houtsmuller, A.B., Neefjes, J., Hoeijmakers, J.H., Vermeulen, W., and Dantuma, N.P. (2006). DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev 20, 1343–1352.
12. Bhaskara, S., Chyla, B.J., Amann, J.M., Knutson, S.K., Cortez, D., Sun, Z.W., and Hiebert, S.W. (2008). Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 30, 61–72.
13. Bird, A.W., Yu, D.Y., Pray-Grant, M.G., Qiu, Q., Harmon, K.E., Megee, P.C., Grant, P.A., Smith, M.M., and Christman, M.F. (2002). Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419, 411–415.
14. Bohm, L., Schneeweiss, F.A., Sharan, R.N., and Feinendegen, L.E. (1997). Influence of histone acetylation on the modification of cytoplasmic and nuclear proteins by ADP-ribosylation in response to free radicals. Biochim Biophys Acta 1334, 149–154.
15. Bonner, W.M., Redon, C.E., Dickey, J.S., Nakamura, A.J., Sedelnikova, O.A., Solier, S., and Pommier, Y. (2008). GammaH2AX and cancer. Nat Rev Cancer 8, 957–967.
16. Botuyan, M.V., Lee, J., Ward, I.M., Kim, J.E., Thompson, J.R., Chen, J., and Mer, G. (2006). Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361–1373.
17. Campbell, S., Ismail, I.H., Young, L.C., Poirier, G.G., and Hendzel, M.J. (2013). Polycomb repressive complex 2 contributes to DNA double-strand break repair. Cell Cycle 12, 2675–2683.
18. Campbell, S.J., Edwards, R.A., Leung, C.C., Neculai, D., Hodge, C.D., Dhe-Paganon, S., and Glover, J.N. (2012). Molecular insights into the function of RING finger (RNF)-containing proteins hRNF8 and hRNF168 in Ubc13/Mms2-dependent ubiquitylation. J Biol Chem 287, 23900–23910.
19. Camphausen, K., and Tofilon, P.J. (2007). Inhibition of histone deacetylation: a strategy for tumor radiosensitization. J Clin Oncol 25, 4051–4056.
20. Campos, E.I., and Reinberg, D. (2009). Histones: annotating chromatin. Annu Rev Genet 43, 559–599.
21. Cao, J., and Yan, Q. (2012). Histone ubiquitination and deubiquitination in transcription, DNA damage response, and cancer. Front Oncol 2, 26.
22. Cao, L.L., Wei, F., Du, Y., Song, B., Wang, D., Shen, C., Lu, X., Cao, Z., Yang, Q., Gao, Y., Wang, L., Zhao, Y., Wang, H., Yang, Y., and Zhu, W.G. (2015). ATM-mediated KDM2A phosphorylation is required for the DNA damage repair. Oncogene doi: 10.1038/onc.2015.81.
23. Cao, R., Tsukada, Y., and Zhang, Y. (2005). Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 20, 845–854.
24. Celeste, A., Difilippantonio, S., Difilippantonio, M.J., Fernandez-Capetillo, O., Pilch, D.R., Sedelnikova, O.A., Eckhaus, M., Ried, T., Bonner, W.M., and Nussenzweig, A. (2003a). H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114, 371–383.
25. Celeste, A., Fernandez-Capetillo, O., Kruhlak, M.J., Pilch, D.R., Staudt, D.W., Lee, A., Bonner, R.F., Bonner, W.M., and Nussenzweig, A. (2003b). Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5, 675–679.
26. Celeste., A., Petersen., S., Romanienko., P.J., Fernandez-Capetillo., O., Chen., H.T., Sedelnikova., O.A., Reina-San-Martin., B., Coppola., V., Meffre., E., DiÞlippantonio., 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., and Nussenzweig., A. (2002). Genomic instability in mice lacking histone H2AX. Science 296, 922–927.
27. Celic, I., Masumoto, H., Griffith, W.P., Meluh, P., Cotter, R.J., Boeke, J.D., and Verreault, A. (2006). The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr Biol 16, 1280–1289.
28. Chagraoui, J., Hebert, J., Girard, S., and Sauvageau, G. (2011). An anticlastogenic function for the Polycomb Group gene Bmi1. Proc Natl Acad Sci USA 108, 5284–5289.
29. Chaudhuri, S., Wyrick, J.J., and Smerdon, M.J. (2009). Histone H3 Lys79 methylation is required for efficient nucleotide excision repair in a silenced locus of Saccharomyces cerevisiae. Nucleic Acids Res 37, 1690–1700.
30. Chen, C.C., Carson, J.J., Feser, J., Tamburini, B., Zabaronick, S., Linger, J., and Tyler, J.K. (2008). Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134, 231–243.
31. Chen, J., Feng, W., Jiang, J., Deng, Y., and Huen, M.S. (2012). Ring finger protein RNF169 antagonizes the ubiquitin-dependent signaling cascade at sites of DNA damage. J Biol Chem 287, 27715–27722.
32. Cheung, W.L., Ajiro, K., Samejima, K., Kloc, M., Cheung, P., Mizzen, C.A., Beeser, A., Etkin, L.D., Chernoff, J., Earnshaw, W.C., and Allis, C.D. (2003). Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113, 507–517.
33. Cheung, W.L., Turner, F.B., Krishnamoorthy, T., Wolner, B., Ahn, S.H., Foley, M., Dorsey, J.A., Peterson, C.L., Berger, S.L., and Allis, C.D. (2005). Phosphorylation of histone H4 serine 1 during DNA damage requires casein kinase II in S. cerevisiae. Curr Biol 15, 656–660.
34. Chou, D.M., Adamson, B., Dephoure, N.E., Tan, X., Nottke, A.C., Hurov, K.E., Gygi, S.P., Colaiacovo, M.P., and Elledge, S.J. (2010). A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc Natl Acad Sci USA 107, 18475–18480.
35. Chowdhury, D., Keogh, M.C., Ishii, H., Peterson, C.L., Buratowski, S., and Lieberman, J. (2005). gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol Cell 20, 801–809.
36. Chowdhury, D., Xu, X., Zhong, X., Ahmed, F., Zhong, J., Liao, J., Dykxhoorn, D.M., Weinstock, D.M., Pfeifer, G.P., and Lieberman, J. (2008). A PP4-phosphatase complex dephosphorylates gamma-H2AX generated during DNA replication. Mol Cell 31, 33–46.
37. Ciccia, A., and Elledge, S.J. (2010). The DNA damage response: making it safe to play with knives. Mol Cell 40, 179–204.
38. Conde, F., Refolio, E., Cordon-Preciado, V., Cortes-Ledesma, F., Aragon, L., Aguilera, A., and San-Segundo, P.A. (2009). The Dot1 histone methyltransferase and the Rad9 checkpoint adaptor contribute to cohesin-dependent double-strand break repair by sister chromatid recombination in Saccharomyces cerevisiae. Genetics 182, 437–446.
39. Cook, P.J., Ju, B.G., Telese, F., Wang, X., Glass, C.K., and Rosenfeld, M.G. (2009). Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458, 591–596.
40. Dai, L., Peng, C., Montellier, E., Lu, Z., Chen, Y., Ishii, H., Debernardi, A., Buchou, T., Rousseaux, S., Jin, F., Sabari, B.R., Deng, Z., Allis, C.D., Ren, B., Khochbin, S., and Zhao, Y. (2014). Lysine 2-hydroxyisobutyrylation is a widely distributed active histone mark. Nat Chem Biol 10, 365–370.
41. Das, C., Lucia, M.S., Hansen, K.C., and Tyler, J.K. (2009). CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459, 113–117.
42. Delgado-Diaz, M.R., Martin, Y., Berg, A., Freire, R., and Smits, V.A. (2014). Dub3 controls DNA damage signalling by direct deubiquitination of H2AX. Mol Oncol 8, 884–893.
43. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D.H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J., Lukas, J., and Lukas, C. (2009). RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435–446.
44. Douglas, P., Zhong, J., Ye, R., Moorhead, G.B., Xu, X., and Lees-Miller, S.P. (2010). Protein phosphatase 6 interacts with the DNA-dependent protein kinase catalytic subunit and dephosphorylates gamma-H2AX. Mol Cell Biol 30, 1368–1381.
45. Downs, J.A., Allard, S., Jobin-Robitaille, O., Javaheri, A., Auger, A., Bouchard, N., Kron, S.J., Jackson, S.P., and Cote, J. (2004). Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell 16, 979–990.
46. Downs, J.A., Lowndes, N.F., and Jackson, S.P. (2000). A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408, 1001–1004.
47. Driscoll, R., Hudson, A., and Jackson, S.P. (2007). Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315, 649–652.
48. Dulev, S., Tkach, J., Lin, S., and Batada, N.N. (2014). SET8 methyltransferase activity during the DNA double-strand break response is required for recruitment of 53BP1. EMBO Rep 15, 1163–1174.
49. Facchino, S., Abdouh, M., Chatoo, W., and Bernier, G. (2010). BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J Neurosci 30, 10096–10111.
50. Faucher, D., and Wellinger, R.J. (2010). Methylated H3K4, a transcription-associated histone modification, is involved in the DNA damage response pathway. PLoS Genet doi: 10.1371/journal. pgen.1001082.
51. Fernandez-Capetillo, O., Allis, C.D., and Nussenzweig, A. (2004). Phosphorylation of histone H2B at DNA double-strand breaks. J Exp Med 199, 1671–1677.
52. Fierz, B., Chatterjee, C., McGinty, R.K., Bar-Dagan, M., Raleigh, D.P., and Muir, T.W. (2011). Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat Chem Biol 7, 113–119.
53. Fink, M., Imholz, D., and Thoma, F. (2007). Contribution of the serine 129 of histone H2A to chromatin structure. Mol Cell Biol 27, 3589–3600.
54. Fnu, S., Williamson, E.A., De Haro, L.P., Brenneman, M., Wray, J., Shaheen, M., Radhakrishnan, K., Lee, S.H., Nickoloff, J.A., and Hromas, R. (2011). Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining. Proc Natl Acad Sci USA 108, 540–545.
55. Fradet-Turcotte, A., Canny, M.D., Escribano-Diaz, C., Orthwein, A., Leung, C.C., Huang, H., Landry, M.C., Kitevski-LeBlanc, J., Noordermeer, S.M., Sicheri, F., and Durocher, D. (2013). 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499, 50–54.
56. Garcia-Salcedo, J.A., Gijon, P., Nolan, D.P., Tebabi, P., and Pays, E. (2003). A chromosomal SIR2 homologue with both histone NAD-dependent ADP-ribosyltransferase and deacetylase activities is involved in DNA repair in Trypanosoma brucei. EMBO J 22, 5851–5862.
57. Gatti, M., Pinato, S., Maiolica, A., Rocchio, F., Prato, M.G., Aebersold, R., and Penengo, L. (2015). RNF168 promotes noncanonical K27 ubiquitination to signal DNA damage. Cell Rep 10, 226–238.
58. Giannattasio, M., Lazzaro, F., Plevani, P., and Muzi-Falconi, M. (2005). The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J Biol Chem 280, 9879–9886.
59. Ginjala, V., Nacerddine, K., Kulkarni, A., Oza, J., Hill, S.J., Yao, M., Citterio, E., Van Lohuizen, M., and Ganesan, S. (2011). BMI1 is recruited to DNA breaks and contributes to DNA damage-induced H2A ubiquitination and repair. Mol Cell Biol 31, 1972–1982.
60. Greeson, N.T., Sengupta, R., Arida, A.R., Jenuwein, T., and Sanders, S.L. (2008). Di-methyl H4 lysine 20 targets the checkpoint protein Crb2 to sites of DNA damage. J Biol Chem 283, 33168–33174.
61. Grewal, S.I., and Jia, S. (2007). Heterochromatin revisited. Nat Rev Genet 8, 35–46.
62. Grunstein, M. (1997). Histone acetylation in chromatin structure and transcription. Nature 389, 349–352.
63. Guo, R., Chen, J., Mitchell, D.L., and Johnson, D.G. (2011). GCN5 and E2F1 stimulate nucleotide excision repair by promoting H3K9 acetylation at sites of damage. Nucleic Acids Res 39, 1390–1397.
64. Gupta, A., Sharma, G.G., Young, C.S., Agarwal, M., Smith, E.R., Paull, T.T., Lucchesi, J.C., Khanna, K.K., Ludwig, T., and Pandita, T.K. (2005). Involvement of human MOF in ATM function. Mol Cell Biol 25, 5292–5305.
65. Gyorgy, B., Toth, E., Tarcsa, E., Falus, A., and Buzas, E.I. (2006). Citrullination: a posttranslational modification in health and disease. Int J Biochem Cell Biol 38, 1662–1677.
66. Hajdu, I., Ciccia, A., Lewis, S.M., and Elledge, S.J. (2011). Wolf-Hirschhorn syndrome candidate 1 is involved in the cellular response to DNA damage. Proc Natl Acad Sci USA 108, 13130–13134.
67. Han, J., Zhou, H., Horazdovsky, B., Zhang, K., Xu, R.M., and Zhang, Z. (2007). Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315, 653–655.
68. House, N.C., Yang, J.H., Walsh, S.C., Moy, J.M., and Freudenreich, C.H. (2014). NuA4 initiates dynamic histone H4 acetylation to promote high-fidelity sister chromatid recombination at postreplication gaps. Mol Cell 55, 818–828.
69. Hromas, R., Williamson, E.A., Fnu, S., Lee, Y.J., Park, S.J., Beck, B.D., You, J.S., Leitao, A., Nickoloff, J.A., and Lee, S.H. (2012). Chk1 phosphorylation of Metnase enhances DNA repair but inhibits replication fork restart. Oncogene 31, 4245–4254.
70. Hsiao, K.Y., and Mizzen, C.A. (2013). Histone H4 deacetylation facilitates 53BP1 DNA damage signaling and double-strand break repair. J Mol Cell Biol 5, 157–165.
71. Huen, M.S., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M.B., and Chen, J. (2007). RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131, 901–914.
72. Huyen, Y., Zgheib, O., Ditullio, R.A., Jr., Gorgoulis, V.G., Zacharatos, P., Petty, T.J., Sheston, E.A., Mellert, H.S., Stavridi, E.S., and Halazonetis, T.D. (2004). Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432, 406–411.
73. Iacovoni, J.S., Caron, P., Lassadi, I., Nicolas, E., Massip, L., Trouche, D., and Legube, G. (2010). High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J 29, 1446–1457.
74. Ikura, T., Ogryzko, V.V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M., Scully, R., Qin, J., and Nakatani, Y. (2000). Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102, 463–473.
75. Ismail, I.H., Andrin, C., McDonald, D., and Hendzel, M.J. (2010). BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J Cell Biol 191, 45–60.
76. Jackson, S.P., and Bartek, J. (2009). The DNA-damage response in human biology and disease. Nature 461, 1071–1078.
77. Javaheri, A., Wysocki, R., Jobin-Robitaille, O., Altaf, M., Cote, J., and Kron, S.J. (2006). Yeast G1 DNA damage checkpoint regulation by H2A phosphorylation is independent of chromatin remodeling. Proc Natl Acad Sci USA 103, 13771–13776.
78. Jazayeri, A., McAinsh, A.D., and Jackson, S.P. (2004). Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc Natl Acad Sci USA 101, 1644–1649.
79. Jha, D.K., and Strahl, B.D. (2014). An RNA polymerase II-coupled function for histone H3K36 methylation in checkpoint activation and DSB repair. Nat Commun 5, 3965.
80. Jones, B., Su, H., Bhat, A., Lei, H., Bajko, J., Hevi, S., Baltus, G.A., Kadam, S., Zhai, H., Valdez, R., Gonzalo, S., Zhang, Y., Li, E., and Chen, T. (2008). The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet 4, e1000190.
81. Kalocsay, M., Hiller, N.J., and Jentsch, S. (2009). Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell 33, 335–343.
82. Kato, K., Nakajima, K., Ui, A., Muto-Terao, Y., Ogiwara, H., and Nakada, S. (2014). Fine-tuning of DNA damage-dependent ubiquitination by OTUB2 supports the DNA repair pathway choice. Mol Cell 53, 617–630.
83. Keogh, M.C., Kim, J.A., Downey, M., Fillingham, J., Chowdhury, D., Harrison, J.C., Onishi, M., Datta, N., Galicia, S., Emili, A., Lieberman, J., Shen, X., Buratowski, S., Haber, J.E., Durocher, D., Greenblatt, J.F., and Krogan, N.J. (2006). A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439, 497–501.
84. Khoury-Haddad, H., Guttmann-Raviv, N., Ipenberg, I., Huggins, D., Jeyasekharan, A.D., and Ayoub, N. (2014). PARP1-dependent recruitment of KDM4D histone demethylase to DNA damage sites promotes double-strand break repair. Proc Natl Acad Sci USA 111, e728–E737.
85. Kim, J.A., Kruhlak, M., Dotiwala, F., Nussenzweig, A., and Haber, J.E. (2007). Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals. J Cell Biol 178, 209–218.
86. Kolas, N.K., Chapman, J.R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F.D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T.M., Pelletier, L., Jackson, S.P., and Durocher, D. (2007). Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318, 1637–1640.
87. Komander, D. (2009). The emerging complexity of protein ubiquitination. Biochem Soc Trans 37, 937–953.
88. Kouzarides, T. (2000). Acetylation: a regulatory modification to rival phosphorylation? EMBO J 19, 1176–1179.
89. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693–705.
90. Kreimeyer, A., Wielckens, K., Adamietz, P., and Hilz, H. (1984). DNA repair-associated ADP-ribosylation in vivo. Modification of histone H1 differs from that of the principal acceptor proteins. J Biol Chem 259, 890–896.
91. Kusch, T., Florens, L., Macdonald, W.H., Swanson, S.K., Glaser, R.L., Yates, J.R., 3rd, Abmayr, S.M., Washburn, M.P., and Workman, J.L. (2004). Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306, 2084–2087.
92. Lee, H.S., Park, J.H., Kim, S.J., Kwon, S.J., and Kwon, J. (2010a). A cooperative activation loop among SWI/SNF, gamma-H2AX and H3 acetylation for DNA double-strand break repair. EMBO J 29, 1434–1445.
93. Lee, J.S., Smith, E., and Shilatifard, A. (2010b). The language of histone crosstalk. Cell 142, 682–685.
94. Lee, S.H., Oshige, M., Durant, S.T., Rasila, K.K., Williamson, E.A., Ramsey, H., Kwan, L., Nickoloff, J.A., and Hromas, R. (2005). The SET domain protein Metnase mediates foreign DNA integration and links integration to nonhomologous end-joining repair. Proc Natl Acad Sci USA 102, 18075–18080.
95. Li, F., Mao, G., Tong, D., Huang, J., Gu, L., Yang, W., and Li, G.M. (2013). The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha. Cell 153, 590–600.
96. Li, X., Corsa, C.A., Pan, P.W., Wu, L., Ferguson, D., Yu, X., Min, J., and Dou, Y. (2010). MOF and H4 K16 acetylation play important roles in DNA damage repair by modulating recruitment of DNA damage repair protein Mdc1. Mol Cell Biol 30, 5335–5347.
97. Li, X., Liu, L., Yang, S., Song, N., Zhou, X., Gao, J., Yu, N., Shan, L., Wang, Q., Liang, J., Xuan, C., Wang, Y., Shang, Y., and Shi, L. (2014). Histone demethylase KDM5B is a key regulator of genome stability. Proc Natl Acad Sci USA 111, 7096–7101.
98. Liang, C.Y., Hsu, P.H., Chou, D.F., Pan, C.Y., Wang, L.C., Huang, W.C., Tsai, M.D., and Lo, W.S. (2011). The histone H3K36 demethylase Rph1/KDM4 regulates the expression of the photoreactivation gene PHR1. Nucleic Acids Res 39, 4151–4165.
99. Liang, C.Y., Wang, L.C., and Lo, W.S. (2013). Dissociation of the H3K36 demethylase Rph1 from chromatin mediates derepression of environmental stress-response genes under genotoxic stress in Saccharomyces cerevisiae. Mol Biol Cell 24, 3251–3262.
100. Liu, C., Wu, J., Paudyal, S.C., You, Z., and Yu, X. (2013). CHFR is important for the first wave of ubiquitination at DNA damage sites. Nucleic Acids Res 41, 1698–1710.
101. Lord, C.J., and Ashworth, A. (2012). The DNA damage response and cancer therapy. Nature 481, 287–294.
102. Ma, T., Chen, Y., Zhang, F., Yang, C.Y., Wang, S., and Yu, X. (2013). RNF111-dependent neddylation activates DNA damage-induced ubiquitination. Mol Cell 49, 897–907.
103. Maas, N.L., Miller, K.M., DeFazio, L.G., and Toczyski, D.P. (2006). Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 23, 109–119.
104. Macurek, L., Lindqvist, A., Voets, O., Kool, J., Vos, H.R., and Medema, R.H. (2010). Wip1 phosphatase is associated with chromatin and dephosphorylates gammaH2AX to promote checkpoint inhibition. Oncogene 29, 2281–2291.
105. Mah, L.J., El-Osta, A., and Karagiannis, T.C. (2010). gammaH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia 24, 679–686.
106. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C., and Lukas, J. (2007). RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887–900.
107. Mallette, F.A., Mattiroli, F., Cui, G., Young, L.C., Hendzel, M.J., Mer, G., Sixma, T.K., and Richard, S. (2012). RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J 31, 1865–1878.
108. Margueron, R., and Reinberg, D. (2010). Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11, 285–296.
109. Marteijn, J.A., Bekker-Jensen, S., Mailand, N., Lans, H., Schwertman, P., Gourdin, A.M., Dantuma, N.P., Lukas, J., and Vermeulen, W. (2009). Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response. J Cell Biol 186, 835–847.
110. Masumoto, H., Hawke, D., Kobayashi, R., and Verreault, A. (2005). A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436, 294–298.
111. Mattiroli, F., Vissers, J.H., Van Dijk, W.J., Ikpa, P., Citterio, E., Vermeulen, W., Marteijn, J.A., and Sixma, T.K. (2012). RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150, 1182–1195.
112. Messick, T.E., and Greenberg, R.A. (2009). The ubiquitin landscape at DNA double-strand breaks. J Cell Biol 187, 319–326.
113. Miller, K.M., and Jackson, S.P. (2012). Histone marks: repairing DNA breaks within the context of chromatin. Biochem Soc Trans 40, 370–376.
114. Miller, K.M., Tjeertes, J.V., Coates, J., Legube, G., Polo, S.E., Britton, S., and Jackson, S.P. (2010). Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol 17, 1144–1151.
115. Miyamoto, N., Izumi, H., Noguchi, T., Nakajima, Y., Ohmiya, Y., Shiota, M., Kidani, A., Tawara, A., and Kohno, K. (2008). Tip60 is regulated by circadian transcription factor clock and is involved in cisplatin resistance. J Biol Chem 283, 18218–18226.
116. Morrison, A.J., Highland, J., Krogan, N.J., Arbel-Eden, A., Greenblatt, J.F., Haber, J.E., and Shen, X. (2004). INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119, 767–775.
117. Mosammaparast, N., Kim, H., Laurent, B., Zhao, Y., Lim, H.J., Majid, M.C., Dango, S., Luo, Y., Hempel, K., Sowa, M.E., Gygi, S.P., Steen, H., Harper, J.W., Yankner, B., and Shi, Y. (2013). The histone demethylase LSD1/KDM1A promotes the DNA damage response. J Cell Biol 203, 457–470.
118. Mosbech, A., Lukas, C., Bekker-Jensen, S., and Mailand, N. (2013). The deubiquitylating enzyme USP44 counteracts the DNA double-strand break response mediated by the RNF8 and RNF168 ubiquitin ligases. J Biol Chem 288, 16579–16587.
119. Moyal, L., Lerenthal, Y., Gana-Weisz, M., Mass, G., So, S., Wang, S.Y., Eppink, B., Chung, Y.M., Shalev, G., Shema, E., Shkedy, D., Smorodinsky, N.I., Van Vliet, N., Kuster, B., Mann, M., Ciechanover, A., Dahm-Daphi, J., Kanaar, R., Hu, M.C., Chen, D.J., Oren, M., and Shiloh, Y. (2011). Requirement of ATM-dependent monoubiquitylation of histone H2B for timely repair of DNA double-strand breaks. Mol Cell 41, 529–542.
120. Munoz-Galvan, S., Jimeno, S., Rothstein, R., and Aguilera, A. (2013). Histone H3K56 acetylation, Rad52, and non-DNA repair factors control double-strand break repair choice with the sister chromatid. PLoS Genet 9, e1003237.
121. Murr, R., Loizou, J.I., Yang, Y.G., Cuenin, C., Li, H., Wang, Z.Q., and Herceg, Z. (2006). Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 8, 91–99.
122. Nakada, S., Chen, G.I., Gingras, A.C., and Durocher, D. (2008). PP4 is a gamma H2AX phosphatase required for recovery from the DNA damage checkpoint. EMBO Rep 9, 1019–1026.
123. Nakamura, K., Kato, A., Kobayashi, J., Yanagihara, H., Sakamoto, S., Oliveira, D.V., Shimada, M., Tauchi, H., Suzuki, H., Tashiro, S., Zou, L., and Komatsu, K. (2011). Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol Cell 41, 515–528.
124. Nakamura, T.M., Du, L.L., Redon, C., and Russell, P. (2004). Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol Cell Biol 24, 6215–6230.
125. Nottke, A.C., Beese-Sims, S.E., Pantalena, L.F., Reinke, V., Shi, Y., and Colaiacovo, M.P. (2011). SPR-5 is a histone H3K4 demethylase with a role in meiotic double-strand break repair. Proc Natl Acad Sci USA 108, 12805–12810.
126. O’Hagan, H.M., Mohammad, H.P., and Baylin, S.B. (2008). Double strand breaks can initiate gene silencing and SIRT1-dependent onset of DNA methylation in an exogenous promoter CpG island. PLoS Genet 4, e1000155.
127. Oda, H., Hubner, M.R., Beck, D.B., Vermeulen, M., Hurwitz, J., Spector, D.L., and Reinberg, D. (2010). Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol Cell 40, 364–376.
128. Oda, H., Okamoto, I., Murphy, N., Chu, J., Price, S.M., Shen, M.M., Torres-Padilla, M.E., Heard, E., and Reinberg, D. (2009). Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol Cell Biol 29, 2278–2295.
129. Ontoso, D., Acosta, I., van Leeuwen, F., Freire, R., and San-Segundo, P.A. (2013). Dot1-dependent histone H3K79 methylation promotes activation of the Mek1 meiotic checkpoint effector kinase by regulating the Hop1 adaptor. PLoS Genet 9, e1003262.
130. Osley, M.A., Tsukuda, T., and Nickoloff, J.A. (2007). ATP-dependent chromatin remodeling factors and DNA damage repair. Mutat Res 618, 65–80.
131. Pai, C.C., Deegan, R.S., Subramanian, L., Gal, C., Sarkar, S., Blaikley, E.J., Walker, C., Hulme, L., Bernhard, E., Codlin, S., Bahler, J., Allshire, R., Whitehall, S., and Humphrey, T.C. (2014). A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice. Nat Commun 5, 4091.
132. Pan, M.R., Peng, G., Hung, W.C., and Lin, S.Y. (2011). Monoubiquitination of H2AX protein regulates DNA damage response signaling. J Biol Chem 286, 28599–28607.
133. Papamichos-Chronakis, M., Krebs, J.E., and Peterson, C.L. (2006). Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev 20, 2437–2449.
134. Papazyan, R., Voronina, E., Chapman, J.R., Luperchio, T.R., Gilbert, T.M., Meier, E., Mackintosh, S.G., Shabanowitz, J., Tackett, A.J., Reddy, K.L., Coyne, R.S., Hunt, D.F., Liu, Y., and Taverna, S.D. (2014). Methylation of histone H3K23 blocks DNA damage in pericentric heterochromatin during meiosis. Elife 3, e02996.
135. Park, J.H., Park, E.J., Lee, H.S., Kim, S.J., Hur, S.K., Imbalzano, A.N., and Kwon, J. (2006). Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting gamma-H2AX induction. EMBO J 25, 3986–3997.
136. Paull, T.T., Rogakou, E.P., Yamazaki, V., Kirchgessner, C.U., Gellert, M., and Bonner, W.M. (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10, 886–895.
137. Pei, H., Zhang, L., Luo, K., Qin, Y., Chesi, M., Fei, F., Bergsagel, P.L., Wang, L., You, Z., and Lou, Z. (2011). MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470, 124–128.
138. Peng, J.C., and Karpen, G.H. (2009). Heterochromatic genome stability requires regulators of histone H3K9 methylation. PLoS Genet 5, e1000435.
139. Pfister, S.X., Ahrabi, S., Zalmas, L.P., Sarkar, S., Aymard, F., Bachrati, C.Z., Helleday, T., Legube, G., La Thangue, N.B., Porter, A.C., and Humphrey, T.C. (2014). SETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell Rep 7, 2006–2018.
140. Pickart, C.M. (2001). Mechanisms underlying ubiquitination. Annu Rev Biochem 70, 503–533.
141. Polo, S.E., and Jackson, S.P. (2011). Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 25, 409–433.
142. Poulsen, M., Lukas, C., Lukas, J., Bekker-Jensen, S., and Mailand, N. (2012). Human RNF169 is a negative regulator of the ubiquitin-dependent response to DNA double-strand breaks. J Cell Biol 197, 189–199.
143. Qian, M.X., Pang, Y., Liu, C.H., Haratake, K., Du, B.Y., Ji, D.Y., Wang, G.F., Zhu, Q.Q., Song, W., Yu, Y., Zhang, X.X., Huang, H.T., Miao, S., Chen, L.B., Zhang, Z.H., Liang, Y.N., Liu, S., Cha, H., Yang, D., Zhai, Y., Komatsu, T., Tsuruta, F., Li, H., Cao, C., Li, W., Li, G.H., Cheng, Y., Chiba, T., Wang, L., Goldberg, A.L., Shen, Y., and Qiu, X.B. (2013). Acetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis. Cell 153, 1012–1024.
144. Qin, S., and Parthun, M.R. (2002). Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol Cell Biol 22, 8353–8365.
145. Rogakou, E.P., Boon, C., Redon, C., and Bonner, W.M. (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146, 905–916.
146. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S., and Bonner, W.M. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273, 5858–5868.
147. Rossetto, D., Truman, A.W., Kron, S.J., and Cote, J. (2010). Epigenetic modifications in double-strand break DNA damage signaling and repair. Clin Cancer Res 16, 4543–4552.
148. Rossodivita, A.A., Boudoures, A.L., Mecoli, J.P., Steenkiste, E.M., Karl, A.L., Vines, E.M., Cole, A.M., Ansbro, M.R., and Thompson, J.S. (2014). Histone H3 K79 methylation states play distinct roles in UV-induced sister chromatid exchange and cell cycle checkpoint arrest in Saccharomyces cerevisiae. Nucleic Acids Res 42, 6286–6299.
149. Roth, S.Y., Denu, J.M., and Allis, C.D. (2001). Histone acetyltransferases. Annu Rev Biochem 70, 81–120.
150. Sakaguchi, A., and Steward, R. (2007). Aberrant monomethylation of histone H4 lysine 20 activates the DNA damage checkpoint in Drosophila melanogaster. J Cell Biol 176, 155–162.
151. Sancar, A., Lindsey-Boltz, L.A., Unsal-Kacmaz, K., and Linn, S. (2004). Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73, 39–85.
152. Sanders, S.L., Portoso, M., Mata, J., Bahler, J., Allshire, R.C., and Kouzarides, T. (2004). Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119, 603–614.
153. Sasaki, T., Lynch, K.L., Mueller, C.V., Friedman, S., Freitag, M., and Lewis, Z.A. (2014). Heterochromatin controls gammaH2A localization in Neurospora crassa. Eukaryot Cell 13, 990–1000.
154. Savic, V., Yin, B., Maas, N.L., Bredemeyer, A.L., Carpenter, A.C., Helmink, B.A., Yang-Iott, K.S., Sleckman, B.P., and Bassing, C.H. (2009). Formation of dynamic gamma-H2AX domains along broken DNA strands is distinctly regulated by ATM and MDC1 and dependent upon H2AX densities in chromatin. Mol Cell 34, 298–310.
155. Schneider, A.C., Heukamp, L.C., Rogenhofer, S., Fechner, G., Bastian, P.J., von Ruecker, A., Muller, S.C., and Ellinger, J. (2011). Global histone H4K20 trimethylation predicts cancer-specific survival in patients with muscle-invasive bladder cancer. BJU Int 108, e290–E296.
156. Schotta, G., Sengupta, R., Kubicek, S., Malin, S., Kauer, M., Callen, E., Celeste, A., Pagani, M., Opravil, S., De La Rosa-Velazquez, I.A., Espejo, A., Bedford, M.T., Nussenzweig, A., Busslinger, M., and Jenuwein, T. (2008). A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev 22, 2048–2061.
157. Seiler, D.M., Rouquette, J., Schmid, V.J., Strickfaden, H., Ottmann, C., Drexler, G.A., Mazurek, B., Greubel, C., Hable, V., Dollinger, G., Cremer, T., and Friedl, A.A. (2011). Double-strand break-induced transcriptional silencing is associated with loss of tri-methylation at H3K4. Chromosome Res 19, 883–899.
158. Shahbazian, M.D., and Grunstein, M. (2007). Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76, 75–100.
159. Shanbhag, N.M., Rafalska-Metcalf, I.U., Balane-Bolivar, C., Janicki, S.M., and Greenberg, R.A. (2010). ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141, 970–981.
160. Sharma, G.G., So, S., Gupta, A., Kumar, R., Cayrou, C., Avvakumov, N., Bhadra, U., Pandita, R.K., Porteus, M.H., Chen, D.J., Cote, J., and Pandita, T.K. (2010). MOF and histone H4 acetylation at lysine 16 are critical for DNA damage response and double-strand break repair. Mol Cell Biol 30, 3582–3595.
161. Shen, C., Wang, D., Liu, X., Gu, B., Du, Y., Wei, F.Z., Cao, L.L., Song, B., Lu, X., Yang, Q., Zhu, Q., Hou, T., Li, M., Wang, L., Wang, H., Zhao, Y., Yang, Y., and Zhu, W.G. (2015). SET7/9 regulates cancer cell proliferation by influencing beta-catenin stability. FASEB J 29, 4313–1323
162. Shogren-Knaak, M., Ishii, H., Sun, J.M., Pazin, M.J., Davie, J.R., and Peterson, C.L. (2006). Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311, 844–847.
163. Shroff, R., Arbel-Eden, A., Pilch, D., Ira, G., Bonner, W.M., Petrini, J.H., Haber, J.E., and Lichten, M. (2004). Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr Biol 14, 1703–1711.
164. Smith, E.R., Cayrou, C., Huang, R., Lane, W.S., Cote, J., and Lucchesi, J.C. (2005). A human protein complex homologous to the Drosophila MSL complex is responsible for the majority of histone H4 acetylation at lysine 16. Mol Cell Biol 25, 9175–9188.
165. Stewart, G.S., Panier, S., Townsend, K., Al-Hakim, A.K., Kolas, N.K., Miller, E.S., Nakada, S., Ylanko, J., Olivarius, S., Mendez, M., Oldreive, C., Wildenhain, J., Tagliaferro, A., Pelletier, L., Taubenheim, N., Durandy, A., Byrd, P.J., Stankovic, T., Taylor, A.M., and Durocher, D. (2009). The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420–434.
166. Stiff, T., O’Driscoll, M., Rief, N., Iwabuchi, K., Lobrich, M., and Jeggo, P.A. (2004). ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 64, 2390–2396.
167. Strahl, B.D., and Allis, C.D. (2000). The language of covalent histone modifications. Nature 403, 41–45.
168. Stucki, M., Clapperton, J.A., Mohammad, D., Yaffe, M.B., Smerdon, S.J., and Jackson, S.P. (2005). MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213–1226.
169. Suganuma, T., and Workman, J.L. (2008). Crosstalk among histone modifications. Cell 135, 604–607.
170. Sulli, G., Di Micco, R., and d’Adda di Fagagna, F. (2012). Crosstalk between chromatin state and DNA damage response in cellular senescence and cancer. Nat Rev Cancer 12, 709–720.
171. Sun, Y., Jiang, X., and Price, B.D. (2010). Tip60: connecting chromatin to DNA damage signaling. Cell Cycle 9, 930–936.
172. Sun, Y., Jiang, X., Xu, Y., Ayrapetov, M.K., Moreau, L.A., Whetstine, J.R., and Price, B.D. (2009). Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat Cell Biol 11, 1376–1382.
173. Takahashi, A., Imai, Y., Yamakoshi, K., Kuninaka, S., Ohtani, N., Yoshimoto, S., Hori, S., Tachibana, M., Anderton, E., Takeuchi, T., Shinkai, Y., Peters, G., Saya, H., and Hara, E. (2012). DNA damage signaling triggers degradation of histone methyltransferases through APC/C(Cdh1) in senescent cells. Mol Cell 45, 123–131.
174. Talbert, P.B., and Henikoff, S. (2010). Histone variants—ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11, 264–275.
175. Tamburini, B.A., and Tyler, J.K. (2005). Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol 25, 4903–4913.
176. Tan, M., Luo, H., Lee, S., Jin, F., Yang, J.S., Montellier, E., Buchou, T., Cheng, Z., Rousseaux, S., Rajagopal, N., Lu, Z., Ye, Z., Zhu, Q., Wysocka, J., Ye, Y., Khochbin, S., Ren, B., and Zhao, Y. (2011). Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146, 1016–1028.
177. Tang, J., Cho, N.W., Cui, G., Manion, E.M., Shanbhag, N.M., Botuyan, M.V., Mer, G., and Greenberg, R.A. (2013). Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol 20, 317–325.
178. Tateishi, K., Okada, Y., Kallin, E.M., and Zhang, Y. (2009). Role of Jhdm2a in regulating metabolic gene expression and obesity resistance. Nature 458, 757–761.
179. Tatum, D., and Li, S. (2011). Evidence that the histone methyltransferase Dot1 mediates global genomic repair by methylating histone H3 on lysine 79. J Biol Chem 286, 17530–17535.
180. Tjeertes, J.V., Miller, K.M., and Jackson, S.P. (2009). Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J 28, 1878–1889.
181. Turner, B.M., Birley, A.J., and Lavender, J. (1992). Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69, 375–384.
182. Unal, E., Arbel-Eden, A., Sattler, U., Shroff, R., Lichten, M., Haber, J.E., and Koshland, D. (2004). DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 16, 991–1002.
183. Utley, R.T., Lacoste, N., Jobin-Robitaille, O., Allard, S., and Cote, J. (2005). Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol Cell Biol 25, 8179–8190.
184. Van Attikum, H., Fritsch, O., Hohn, B., and Gasser, S.M. (2004). Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119, 777–788.
185. Vempati, R.K., Jayani, R.S., Notani, D., Sengupta, A., Galande, S., and Haldar, D. (2010). p300-mediated acetylation of histone H3 lysine 56 functions in DNA damage response in mammals. J Biol Chem 285, 28553–28564.
186. Voigt, P., Tee, W.W., and Reinberg, D. (2013). A double take on bivalent promoters. Genes Dev 27, 1318–1338.
187. Wagner, K.W., Alam, H., Dhar, S.S., Giri, U., Li, N., Wei, Y., Giri, D., Cascone, T., Kim, J.H., Ye, Y., Multani, A.S., Chan, C.H., Erez, B., Saigal, B., Chung, J., Lin, H.K., Wu, X., Hung, M.C., Heymach, J.V., and Lee, M.G. (2013). KDM2A promotes lung tumorigenesis by epigenetically enhancing ERK1/2 signaling. J Clin Invest 123, 5231–5246.
188. Wakeman, T.P., Wang, Q., Feng, J., and Wang, X.-F. (2012). Bat3 facilitates H3K79 dimethylation by DOT1L and promotes DNA damage-induced 53BP1 foci at G1/G2 cell-cycle phases. EMBO J 31, 2169–2181.
189. Wang, B., and Elledge, S.J. (2007). Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci USA 104, 20759–20763.
190. Wang, D., Zhou, J., Liu, X., Lu, D., Shen, C., Du, Y., Wei, F.Z., Song, B., Lu, X., Yu, Y., Wang, L., Zhao, Y., Wang, H., Yang, Y., Akiyama, Y., Zhang, H., and Zhu, W.G. (2013). Methylation of SUV39H1 by SET7/9 results in heterochromatin relaxation and genome instability. Proc Natl Acad Sci USA 110, 5516–5521.
191. Wang, H., Zhai, L., Xu, J., Joo, H.-Y., Jackson, S., Erdjument-Bromage, H., Tempst, P., Xiong, Y., and Zhang, Y. (2006). Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell 22, 383–394.
192. Ward, I.M., and Chen, J. (2001). Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 276, 47759–47762.
193. Williamson, E.A., Wray, J.W., Bansal, P., and Hromas, R. (2012). Overview for the histone codes for DNA repair. Prog Mol Biol Transl Sci 110, 207–227.
194. Wu, J., Huen, M.S., Lu, L.Y., Ye, L., Dou, Y., Ljungman, M., Chen, J., and Yu, X. (2009). Histone ubiquitination associates with BRCA1-dependent DNA damage response. Mol Cell Biol 29, 849–860.
195. Wu, W., Nishikawa, H., Fukuda, T., Vittal, V., Asano, M., Miyoshi, Y., Klevit, R.E., and Ohta, T. (2015). Interaction of BARD1 and HP1 is required for BRCA1 retention at sites of DNA damage. Cancer Res 75, 1311–1321.
196. Wurtele, H., Kaiser, G.S., Bacal, J., St-Hilaire, E., Lee, E.H., Tsao, S., Dorn, J., Maddox, P., Lisby, M., Pasero, P., and Verreault, A. (2012). Histone H3 lysine 56 acetylation and the response to DNA replication fork damage. Mol Cell Biol 32, 154–172.
197. Wysocki, R., Javaheri, A., Allard, S., Sha, F., Cote, J., and Kron, S.J. (2005). Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol Cell Biol 25, 8430–8443.
198. Xiao, A., Li, H., Shechter, D., Ahn, S.H., Fabrizio, L.A., Erdjument-Bromage, H., Ishibe-Murakami, S., Wang, B., Tempst, P., Hofmann, K., Patel, D.J., Elledge, S.J., and Allis, C.D. (2009). WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457, 57–62.
199. Xie, A., Odate, S., Chandramouly, G., and Scully, R. (2010). H2AX post-translational modifications in the ionizing radiation response and homologous recombination. Cell Cycle 9, 3602–3610.
200. Xie, A., Puget, N., Shim, I., Odate, S., Jarzyna, I., Bassing, C.H., Alt, F.W., and Scully, R. (2004). Control of sister chromatid recombination by histone H2AX. Mol Cell 16, 1017–1025.
201. Xu, Y., Sun, Y., Jiang, X., Ayrapetov, M.K., Moskwa, P., Yang, S., Weinstock, D.M., and Price, B.D. (2010). The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J Cell Biol 191, 31–43.
202. Yan, Q., Dutt, S., Xu, R., Graves, K., Juszczynski, P., Manis, J.P., and Shipp, M.A. (2009). BBAP monoubiquitylates histone H4 at lysine 91 and selectively modulates the DNA damage response. Mol Cell 36, 110–120.
203. Yang, X., Li, L., Liang, J., Shi, L., Yang, J., Yi, X., Zhang, D., Han, X., Yu, N., and Shang, Y. (2013). Histone acetyltransferase 1 promotes homologous recombination in DNA repair by facilitating histone turnover. J Biol Chem 288, 18271–18282.
204. Young, L.C., McDonald, D.W., and Hendzel, M.J. (2013). Kdm4b histone demethylase is a DNA damage response protein and confers a survival advantage following gamma-irradiation. J Biol Chem 288, 21376–21388.
205. Yu, H., Pak, H., Hammond-Martel, I., Ghram, M., Rodrigue, A., Daou, S., Barbour, H., Corbeil, L., Hebert, J., Drobetsky, E., Masson, J.Y., Di Noia, J.M., and Affar el, B. (2014). Tumor suppressor and deubiquitinase BAP1 promotes DNA double-strand break repair. Proc Natl Acad Sci USA 111, 285–290.
206. Yun, M., Wu, J., Workman, J.L., and Li, B. (2011). Readers of histone modifications. Cell Res 21, 564–578.