Targeting DNA damage response: Threshold, chromatin landscape and beyond

Pharmacology and Therapeutics

Volumn 138, Issue 1, 2013, Pages 46-52

  Gonfloni, Stefania ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

H2AX; ATM; c Abl; Chromatin; DNA damage; DNA repair; Histone modifications; Keywords; Tip60

Indexed keywords

HISTONE DEACETYLASE;

CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVATION; GENE STRUCTURE; HISTONE MODIFICATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

CHROMATIN; DNA DAMAGE; DNA REPAIR; HISTONES;

EID: 84875212373     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2012.12.006     Document Type: Review

References (126)

1. A. Al-Hakim, C. Escribano-Diaz, M.C. Landry, L. O'Donnell, S. Panier, and R.K. Szilard The ubiquitous role of ubiquitin in the DNA damage response DNA Repair (Amst) 9 2010 1229 1240
2. K. Aziz, S. Nowsheen, G. Pantelias, G. Iliakis, V.G. Gorgoulis, and A.G. Georgakilas Targeting DNA damage and repair: embracing the pharmacological era for successful cancer therapy Pharmacol Ther 133 2012 334 350
3. C. Baldeyron, G. Soria, D. Roche, A.J. Cook, and G. Almouzni HP1alpha recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair J Cell Biol 193 2011 81 95
4. A.J. Bannister, P. Zegerman, J.F. Partridge, E.A. Miska, J.O. Thomas, and R.C. Allshire Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain Nature 410 2001 120 124
5. Y. Bao Chromatin response to DNA double-strand break damage Epigenomics 3 2011 307 321
6. A. Barski, S. Cuddapah, K. Cui, T.Y. Roh, D.E. Schones, and Z. Wang High-resolution profiling of histone methylations in the human genome Cell 129 2007 823 837
7. S. Bekker-Jensen, J. Rendtlew Danielsen, K. Fugger, I. Gromova, A. Nerstedt, and C. Lukas HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes Nat Cell Biol 12 2010 80 86 (sup pp 81-12)
8. A. Bensimon, R. Aebersold, and Y. Shiloh Beyond ATM: the protein kinase landscape of the DNA damage response FEBS Lett 585 2011 1625 1639
9. J. Boucas, A. Riabinska, M. Jokic, G.S. Herter-Sprie, S. Chen, and K. Hopker Posttranscriptional regulation of gene expression-adding another layer of complexity to the DNA damage response Front Genet 3 2012 159
10. E. Boyarchuk, R. Montes de Oca, and G. Almouzni Cell cycle dynamics of histone variants at the centromere, a model for chromosomal landmarks Curr Opin Cell Biol 23 2011 266 276
11. B.R. Cairns Chromatin remodeling complexes: strength in diversity, precision through specialization Curr Opin Genet Dev 15 2005 185 190
12. E.I. Campos, and D. Reinberg Histones: annotating chromatin Annu Rev Genet 43 2009 559 599
13. K. Cerosaletti, J. Wright, and P. Concannon Active role for nibrin in the kinetics of ATM activation Mol Cell Biol 26 2006 1691 1699
14. J.R. Chapman, A.J. Sossick, S.J. Boulton, and S.P. Jackson BRCA1-associated exclusion of 53BP1 from DNA damage sites underlies temporal control of DNA repair J Cell Sci 125 2012 3529 3534
15. I. Chiolo, A. Minoda, S.U. Colmenares, A. Polyzos, S.V. Costes, and G.H. Karpen Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair Cell 144 2011 732 744
16. D. Chowdhury, M.C. Keogh, H. Ishii, C.L. Peterson, S. Buratowski, and J. Lieberman gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair Mol Cell 20 2005 801 809
17. D. Chowdhury, X. Xu, X. Zhong, F. Ahmed, J. Zhong, and J. Liao A PP4-phosphatase complex dephosphorylates gamma-H2AX generated during DNA replication Mol Cell 31 2008 33 46
18. A. Ciccia, and S.J. Elledge The DNA damage response: Making it safe to play with knives Mol Cell 40 2010 179 204
19. C.R. Clapier, and B.R. Cairns The biology of chromatin remodeling complexes Annu Rev Biochem 78 2009 273 304
20. P.J. Cook, B.G. Ju, F. Telese, X. Wang, C.K. Glass, and M.G. Rosenfeld Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions Nature 458 2009 591 596
21. E. de Wit, F. Greil, and B. van Steensel High-resolution mapping reveals links of HP1 with active and inactive chromatin components PLoS Genet 3 2007 e38
22. D. De Zio, M. Bordi, and F. Cecconi Oxidative DNA damage in neurons: Implication of ku in neuronal homeostasis and survival Int J Cell Biol 2012 2012 752420
23. S. Difilippantonio, A. Celeste, O. Fernandez-Capetillo, H.T. Chen, B. Reina San Martin, and F. Van Laethem Role of Nbs1 in the activation of the ATM kinase revealed in humanized mouse models Nat Cell Biol 7 2005 675 685
24. C. Doil, N. Mailand, S. Bekker-Jensen, P. Menard, D.H. Larsen, and R. Pepperkok RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins Cell 136 2009 435 446
25. J.A. Downs, S. Allard, O. Jobin-Robitaille, A. Javaheri, A. Auger, and N. Bouchard Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites Mol Cell 16 2004 979 990
26. Y.C. Du, S. Gu, J. Zhou, T. Wang, H. Cai, and M.A. Macinnes The dynamic alterations of H2AX complex during DNA repair detected by a proteomic approach reveal the critical roles of Ca(2+)/calmodulin in the ionizing radiation-induced cell cycle arrest Mol Cell Proteomics 5 2006 1033 1044
27. D.D. Dudley, J. Chaudhuri, C.H. Bassing, and F.W. Alt Mechanism and control of V(D)J recombination versus class switch recombination: Similarities and differences Adv Immunol 86 2005 43 112
28. A. Dupre, L. Boyer-Chatenet, and J. Gautier Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex Nat Struct Mol Biol 13 2006 451 457
29. R. Elkon, S. Rashi-Elkeles, Y. Lerenthal, C. Linhart, T. Tenne, and N. Amariglio Dissection of a DNA-damage-induced transcriptional network using a combination of microarrays, RNA interference and computational promoter analysis Genome Biol 6 2005 R43
30. J. Falck, J. Coates, and S.P. Jackson Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage Nature 434 2005 605 611
31. J. Fan, X. Yang, W. Wang, W.H. Wood III, K.G. Becker, and M. Gorospe Global analysis of stress-regulated mRNA turnover by using cDNA arrays Proc Natl Acad Sci U S A 99 2002 10611 10616
32. P. Fei, and W.S. El-Deiry P53 and radiation responses Oncogene 22 2003 5774 5783
33. B. Fierz, C. Chatterjee, R.K. McGinty, M. Bar-Dagan, D.P. Raleigh, and T.W. Muir Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction Nat Chem Biol 7 2011 113 119
34. S. Francia, F. Michelini, A. Saxena, D. Tang, M. de Hoon, and V. Anelli Site-specific DICER and DROSHA RNA products control the DNA-damage response Nature 488 2012 231 235
35. P. Gallinari, S. Di Marco, P. Jones, M. Pallaoro, and C. Steinkuhler HDACs, histone deacetylation and gene transcription: From molecular biology to cancer therapeutics Cell Res 17 2007 195 211
36. A.P. Gasch, M. Huang, S. Metzner, D. Botstein, S.J. Elledge, and P.O. Brown Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p Mol Biol Cell 12 2001 2987 3003
37. S. Gonfloni DNA damage stress response in germ cells: role of c-Abl and clinical implications Oncogene 29 2010 6193 6202
38. S. Gonfloni Modulating c-Abl nuclear activity as a strategy to preserve female fertility Cell Cycle 9 2010 217 218
39. S. Gonfloni, L. Di Tella, S. Caldarola, S.M. Cannata, F.G. Klinger, and C. Di Bartolomeo Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death Nat Med 15 2009 1179 1185
40. S.I. Grewal, and S. Jia Heterochromatin revisited Nat Rev Genet 8 2007 35 46
41. M.G. Guenther, S.S. Levine, L.A. Boyer, R. Jaenisch, and R.A. Young A chromatin landmark and transcription initiation at most promoters in human cells Cell 130 2007 77 88
42. K. Heo, H. Kim, S.H. Choi, J. Choi, and K. Kim FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16 Mol Cell 30 2008 86 97
43. K. Hofmann Ubiquitin-binding domains and their role in the DNA damage response DNA Repair (Amst) 8 2009 544 556
44. M.S. Huen, R. Grant, I. Manke, K. Minn, X. Yu, and M.B. Yaffe RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly Cell 131 2007 901 914
45. T. Ikura, S. Tashiro, A. Kakino, H. Shima, N. Jacob, and R. Amunugama DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics Mol Cell Biol 27 2007 7028 7040
46. S.P. Jackson, and J. Bartek The DNA-damage response in human biology and disease Nature 461 2009 1071 1078
47. B. Jakob, J. Splinter, S. Conrad, K.O. Voss, D. Zink, and M. Durante DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin Nucleic Acids Res 39 2011 6489 6499
48. Z. Jiang, R. Kamath, S. Jin, M. Balasubramani, T.K. Pandita, and B. Rajasekaran Tip60-mediated acetylation activates transcription independent apoptotic activity of Abl Mol Cancer 10 2011 88
49. X. Jiang, Y. Sun, S. Chen, K. Roy, and B.D. Price The FATC domains of PIKK proteins are functionally equivalent and participate in the Tip60-dependent activation of DNA-PKcs and ATM J Biol Chem 281 2006 15741 15746
50. C.A. Johnson, D.A. White, J.S. Lavender, L.P. O'Neill, and B.M. Turner Human class I histone deacetylase complexes show enhanced catalytic activity in the presence of ATP and co-immunoprecipitate with the ATP-dependent chaperone protein Hsp70 J Biol Chem 277 2002 9590 9597
51. S. Keeney, and M.J. Neale Initiation of meiotic recombination by formation of DNA double-strand breaks: Mechanism and regulation Biochem Soc Trans 34 2006 523 525
52. M.C. Keogh, J.A. Kim, M. Downey, J. Fillingham, D. Chowdhury, and J.C. Harrison A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery Nature 439 2006 497 501
53. O. Kerscher, R. Felberbaum, and M. Hochstrasser Modification of proteins by ubiquitin and ubiquitin-like proteins Annu Rev Cell Dev Biol 22 2006 159 180
54. J.A. Kim, M. Kruhlak, F. Dotiwala, A. Nussenzweig, and J.E. Haber Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals J Cell Biol 178 2007 209 218
55. N.K. Kolas, J.R. Chapman, S. Nakada, J. Ylanko, R. Chahwan, and F.D. Sweeney Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase Science 318 2007 1637 1640
56. T. Kouzarides Chromatin modifications and their function Cell 128 2007 693 705
57. J.E. Krebs Moving marks: Dynamic histone modifications in yeast Mol Biosyst 3 2007 590 597
58. T.B. Kryston, A.B. Georgiev, P. Pissis, and A.G. Georgakilas Role of oxidative stress and DNA damage in human carcinogenesis Mutat Res 711 2011 193 201
59. J.H. Lee, and T.T. Paull ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex Science 308 2005 551 554
60. X. Li, C.A. Corsa, P.W. Pan, L. Wu, D. Ferguson, and X. Yu 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 2010 5335 5347
61. M.R. Lieber The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway Annu Rev Biochem 79 2010 181 211
62. M.S. Luijsterburg, and H. van Attikum Chromatin and the DNA damage response: The cancer connection Mol Oncol 5 2011 349 367
63. J. Lukas The interface between the ubiquitin family and the DNA damage response EMBO Rep 11 2010 907 909
64. J. Lukas, C. Lukas, and J. Bartek More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance Nat Cell Biol 13 2011 1161 1169
65. E. Maiani, C. Di Bartolomeo, F.G. Klinger, S.M. Cannata, S. Bernardini, and S. Chateauvieux Reply to: Cisplatin-induced primordial follicle oocyte killing and loss of fertility are not prevented by imatinib Nat Med 18 2012 1172 1174
66. E. Maiani, M. Diederich, and S. Gonfloni DNA damage response: The emerging role of c-Abl as a regulatory switch? Biochem Pharmacol 82 2011 1269 1276
67. N. Mailand, S. Bekker-Jensen, H. Faustrup, F. Melander, J. Bartek, and C. Lukas RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins Cell 131 2007 887 900
68. R. Margueron, and D. Reinberg Chromatin structure and the inheritance of epigenetic information Nat Rev Genet 11 2010 285 296
69. S. Matsuoka, B.A. Ballif, A. Smogorzewska, E.R. McDonald III, K.E. Hurov, and J. Luo ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage Science 316 2007 1160 1166
70. V. Meltser, M. Ben-Yehoyada, and Y. Shaul c-Abl tyrosine kinase in the DNA damage response: Cell death and more Cell Death Differ 18 2011 2 4
71. K.M. Miller, and S.P. Jackson Histone marks: repairing DNA breaks within the context of chromatin Biochem Soc Trans 40 2012 370 376
72. S. Minucci, and P.G. Pelicci Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer Nat Rev Cancer 6 2006 38 51
73. D.H. Mohammad, and M.B. Yaffe 14-3-3 proteins, FHA domains and BRCT domains in the DNA damage response DNA Repair (Amst) 8 2009 1009 1017
74. A.J. Morrison, J. Highland, N.J. Krogan, A. Arbel-Eden, J.F. Greenblatt, and J.E. Haber INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair Cell 119 2004 767 775
75. R. Murr, J.I. Loizou, Y.G. Yang, C. Cuenin, H. Li, and Z.Q. Wang Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks Nat Cell Biol 8 2006 91 99
76. I.B. Nazarov, A.N. Smirnova, R.I. Krutilina, M.P. Svetlova, L.V. Solovjeva, and A.A. Nikiforov Dephosphorylation of histone gamma-H2AX during repair of DNA double-strand breaks in mammalian cells and its inhibition by calyculin A Radiat Res 160 2003 309 317
77. S. Negrini, V.G. Gorgoulis, and T.D. Halazonetis Genomic instability - An evolving hallmark of cancer Nat Rev Mol Cell Biol 11 2010 220 228
78. S. Panier, and D. Durocher Regulatory ubiquitylation in response to DNA double-strand breaks DNA Repair (Amst) 8 2009 436 443
79. M. Papamichos-Chronakis, J.E. Krebs, and C.L. Peterson Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage Genes Dev 20 2006 2437 2449
80. R.D. Paulsen, D.V. Soni, R. Wollman, A.T. Hahn, M.C. Yee, and A. Guan A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability Mol Cell 35 2009 228 239
81. M. Pellegrini, A. Celeste, S. Difilippantonio, R. Guo, W. Wang, and L. Feigenbaum Autophosphorylation at serine 1987 is dispensable for murine ATM activation in vivo Nature 443 2006 222 225
82. J.C. Peng, and G.H. Karpen Epigenetic regulation of heterochromatic DNA stability Curr Opin Genet Dev 18 2008 204 211
83. A.H. Peters, D. O'Carroll, H. Scherthan, K. Mechtler, S. Sauer, and C. Schofer Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability Cell 107 2001 323 337
84. D.K. Pokholok, C.T. Harbison, S. Levine, M. Cole, N.M. Hannett, and T.I. Lee Genome-wide map of nucleosome acetylation and methylation in yeast Cell 122 2005 517 527
85. S.E. Polo, and S.P. Jackson Dynamics of DNA damage response proteins at DNA breaks: A focus on protein modifications Genes Dev 25 2011 409 433
86. J.P. Quivy, D. Roche, D. Kirschner, H. Tagami, Y. Nakatani, and G. Almouzni A CAF-1 dependent pool of HP1 during heterochromatin duplication EMBO J 23 2004 3516 3526
87. C.H. Ramaekers, and B.G. Wouters Regulatory functions of ubiquitin in diverse DNA damage responses Curr Mol Med 11 2011 152 169
88. H.C. Reinhardt, I.G. Cannell, S. Morandell, and M.B. Yaffe Is post-transcriptional stabilization, splicing and translation of selective mRNAs a key to the DNA damage response? Cell Cycle 10 2011 23 27
89. K.E. Rieger, and G. Chu Portrait of transcriptional responses to ultraviolet and ionizing radiation in human cells Nucleic Acids Res 32 2004 4786 4803
90. W.P. Roos, and B. Kaina DNA damage-induced apoptosis: From specific DNA lesions to the DNA damage response and apoptosis Cancer Lett 2012 [Epub ahead of print]. http://www.cancerletters.info/article/S0304-3835(12)00032-8/abstract
91. A.J. Ruthenburg, H. Li, D.J. Patel, and C.D. Allis Multivalent engagement of chromatin modifications by linked binding modules Nat Rev Mol Cell Biol 8 2007 983 994
92. M.D. Shahbazian, and M. Grunstein Functions of site-specific histone acetylation and deacetylation Annu Rev Biochem 76 2007 75 100
93. N.M. Shanbhag, I.U. Rafalska-Metcalf, C. Balane-Bolivar, S.M. Janicki, and R.A. Greenberg ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks Cell 141 2010 970 981
94. G.G. Sharma, S. So, A. Gupta, R. Kumar, C. Cayrou, and N. Avvakumov MOF and histone H4 acetylation at lysine 16 are critical for DNA damage response and double-strand break repair Mol Cell Biol 30 2010 3582 3595
95. M. Shogren-Knaak, and C.L. Peterson Switching on chromatin: Mechanistic role of histone H4-K16 acetylation Cell Cycle 5 2006 1361 1365
96. M. Shrivastav, L.P. De Haro, and J.A. Nickoloff Regulation of DNA double-strand break repair pathway choice Cell Res 18 2008 134 147
97. G. Soria, S.E. Polo, and G. Almouzni Prime, repair, restore: The active role of chromatin in the DNA damage response Mol Cell 46 2012 722 734
98. G.S. Stewart, S. Panier, K. Townsend, A.K. Al-Hakim, N.K. Kolas, and E.S. Miller The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage Cell 136 2009 420 434
99. M. Stucki, J.A. Clapperton, D. Mohammad, M.B. Yaffe, S.J. Smerdon, and S.P. Jackson MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks Cell 123 2005 1213 1226
100. T. Suganuma, and J.L. Workman Signals and combinatorial functions of histone modifications Annu Rev Biochem 80 2011 473 499
101. Y. Sun, X. Jiang, S. Chen, N. Fernandes, and B.D. Price A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM Proc Natl Acad Sci U S A 102 2005 13182 13187
102. Y. Sun, X. Jiang, Y. Xu, M.K. Ayrapetov, L.A. Moreau, and J.R. Whetstine Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60 Nat Cell Biol 11 2009 1376 1382
103. Y. Sun, X. Jiang, and B.D. Price Tip60: connecting chromatin to DNA damage signaling Cell Cycle 9 2010 930 936
104. Y. Sun, Y. Xu, K. Roy, and B.D. Price DNA damage-induced acetylation of lysine 3016 of ATM activates ATM kinase activity Mol Cell Biol 27 2007 8502 8509
105. J.Q. Svejstrup Mechanisms of transcription-coupled DNA repair Nat Rev Mol Cell Biol 3 2002 21 29
106. E. Szenker, D. Ray-Gallet, and G. Almouzni The double face of the histone variant H3.3 Cell Res 21 2011 421 434
107. M. Takata, M.S. Sasaki, E. Sonoda, C. Morrison, M. Hashimoto, and H. Utsumi Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells EMBO J 17 1998 5497 5508
108. P.B. Talbert, and S. Henikoff Histone variants-ancient wrap artists of the epigenome Nat Rev Mol Cell Biol 11 2010 264 275
109. H.D. Ulrich, and H. Walden Ubiquitin signalling in DNA replication and repair Nat Rev Mol Cell Biol 11 2010 479 489
110. T. Uziel, Y. Lerenthal, L. Moyal, Y. Andegeko, L. Mittelman, and Y. Shiloh Requirement of the MRN complex for ATM activation by DNA damage EMBO J 22 2003 5612 5621
111. C.R. Vakoc, M.M. Sachdeva, H. Wang, and G.A. Blobel Profile of histone lysine methylation across transcribed mammalian chromatin Mol Cell Biol 26 2006 9185 9195
112. H. van Attikum, O. Fritsch, B. Hohn, and S.M. Gasser Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair Cell 119 2004 777 788
113. H. van Attikum, and S.M. Gasser The histone code at DNA breaks: A guide to repair? Nat Rev Mol Cell Biol 6 2005 757 765
114. H. van Attikum, and S.M. Gasser Crosstalk between histone modifications during the DNA damage response Trends Cell Biol 19 2009 207 217
115. P. Vichi, F. Coin, J.P. Renaud, W. Vermeulen, J.H. Hoeijmakers, and D. Moras Cisplatin- and UV-damaged DNA lure the basal transcription factor TFIID/TBP EMBO J 16 1997 7444 7456
116. B. Wang, and S.J. Elledge Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage Proc Natl Acad Sci U S A 104 2007 20759 20763
117. X. Wang, L. Zeng, J. Wang, J.F. Chau, K.P. Lai, and D. Jia A positive role for c-Abl in Atm and Atr activation in DNA damage response Cell Death Differ 18 2011 5 15
118. I.M. Ward, and J. Chen Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress J Biol Chem 276 2001 47759 47762
119. J.R. Whetstine, A. Nottke, F. Lan, M. Huarte, S. Smolikov, and Z. Chen Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases Cell 125 2006 467 481
120. A. Xiao, H. Li, D. Shechter, S.H. Ahn, L.A. Fabrizio, and H. Erdjument-Bromage WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity Nature 457 2009 57 62
121. Y. Xu, and B.D. Price Chromatin dynamics and the repair of DNA double strand breaks Cell Cycle 10 2011 261 267
122. K. Yamagata, and I. Kitabayashi Sirt1 physically interacts with Tip60 and negatively regulates Tip60-mediated acetylation of H2AX Biochem Biophys Res Commun 390 2009 1355 1360
123. J. Yuan, R. Adamski, and J. Chen Focus on histone variant H2AX: To be or not to be FEBS Lett 584 2010 3717 3724
124. J. Yuan, and J. Chen MRE11-RAD50-NBS1 complex dictates DNA repair independent of H2AX J Biol Chem 285 2010 1097 1104
125. M. Yun, J. Wu, J.L. Workman, and B. Li Readers of histone modifications Cell Res 21 2011 564 578
126. L. Zou, and S.J. Elledge Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes Science 300 2003 1542 1548