Epigenetic regulation of genomic integrity

Chromosoma

Volumn 121, Issue 2, 2012, Pages 131-151

  Deem, Angela K ^a   Li, Xuan ^a   Tyler, Jessica K ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; BRCA1 PROTEIN; DNA; HISTONE H2A; HISTONE H2AX; HISTONE H2B; HISTONE H3; HISTONE H4; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; RAG1 PROTEIN; RAG2 PROTEIN;

CARCINOGENESIS; CHROMATIN STRUCTURE; CHROMOSOME ABERRATION; DNA DAMAGE; DNA REPAIR; DNA SEQUENCE; EUKARYOTE; EXCISION REPAIR; GENE MUTATION; GENETIC REGULATION; GENETIC STABILITY; HETEROCHROMATIN; HISTONE MODIFICATION; HISTONE UBIQUITINATION; HUMAN; MOLECULAR MECHANICS; NONHUMAN; PROTEIN BINDING; PROTEIN PROCESSING; PROTEIN TRANSPORT; REVIEW;

CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; EPIGENESIS, GENETIC; GENOMIC INSTABILITY; HISTONES; MODELS, BIOLOGICAL;

EUKARYOTA;

EID: 84862799523     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-011-0358-1     Document Type: Review

References (206)

1. Ahel D, Hořejší Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP et al (2009) Poly(ADP-ribose)- dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325:1240-1243
2. Ayoub N, Jeyasekharan AD, Bernal JA, Venkitaraman AR (2008) HP1-[bgr] mobilization promotes chromatin changes that initiate the DNA damage response. Nature 453:682-686
3. Ayoub N, Jeyasekharan AD, Venkitaraman AR (2009) Mobilization and recruitment of HP1β: a bimodal response to DNA breakage. Cell Cycle 8:2946-2951
4. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506 (Pubitemid 36168436)
5. Baldeyron C, Soria G, Roche D, Cook AJL, Almouzni G (2011) HP1αrecruitment to DNA damage by p150CAF-1 promotes homologous recombination repair. J Cell Biol 193:81-95
6. Battu A, Ray A, Wani AA (2011) ASF1A and ATM regulate H3K56- mediated cell-cycle checkpoint recovery in response to UV irradiation. Nucleic Acids Res 39:7931-7945
7. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, Lukas J (2006) Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 173:195-206
8. Bekker-Jensen S, Lukas C, Melander F, Bartek J, Lukas J (2005) Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J Cell Biol 170:201-211 (Pubitemid 41043803)
9. Bergink S, Salomons FA, Hoogstraten D, Groothuis TAM, de Waard H, Wu J, Yuan L, Citterio E, Houtsmuller AB, Neefjes J et al (2006) DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev 20:1343-1352 (Pubitemid 43727594)
10. Berkovich E, Monnat RJ, Kastan MB (2007) Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat Cell Biol 9:683-690 (Pubitemid 47214731)
11. Bewersdorf J, Bennett BT, Knight KL (2006) H2AX chromatin structures and their response to DNA damage revealed by 4Pi microscopy. Proc Natl Acad Sci 103:18137-18142 (Pubitemid 44871625)
12. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, Grant PA, Smith MM, Christman MF (2002) Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419:411-415
13. Borde V, Robine N, Lin W, Bonfils S, Geli V, Nicolas A (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28:99-111
14. Bothmer A, Robbiani DF, Di Virgilio M, Bunting SF, Klein IA, Feldhahn N, Barlow J, Chen H-T, Bosque D, Callen E et al (2011) Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. Mol Cell 42:319-329
15. Bothmer A, Robbiani DF, Feldhahn N, Gazumyan A, Nussenzweig A, Nussenzweig MC (2010) 53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination. J Exp Med 207:855-865
16. Botuyan MV, Lee J, Ward IM, Kim J-E, Thompson JR, Chen J, 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 (Pubitemid 44960409)
17. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, Hiddingh S, Thanasoula M, Kulkarni A, Yang Q et al (2010) 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 17:688-695
18. Bredemeyer AL, Sharma GG, Huang C-Y, Helmink BA, Walker LM, Khor KC, Nuskey B, Sullivan KE, Pandita TK, Bassing CH et al (2006) ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature 442:466-470 (Pubitemid 44264797)
19. Buard J, Barthes P, Grey C, de Massy B (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 28:2616-2624
20. Bunting SF, Callén E, Wong N, Chen H-T, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L et al (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141:243-254
21. Cairns BR (2004) Around the world of DNA damage INO80 days. Cell 119:733-735
22. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5:675-679 (Pubitemid 36818091)
23. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio MJ et al (2002) Genomic instability in mice lacking histone H2AX. Science 296:922-927 (Pubitemid 34464900)
24. Chai B, Huang J, Cairns BR, Laurent BC (2005) Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev 19:1656-1661 (Pubitemid 41058359)
25. Chapman JR, Jackson SP (2008) Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep 9:795-801
26. Chen C-C, Carson JJ, Feser J, Tamburini B, Zabaronick S, Linger J, Tyler JK (2008) Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134:231-243 (Pubitemid 352010334)
27. Cheung WL, Turner FB, Krishnamoorthy T, Wolner B, Ahn S-H, Foley M, Dorsey JA, Peterson CL, Berger SL, Allis CD (2005) Phosphorylation of histone H4 serine 1 during DNA damage requires casein kinase II in S. cerevisiae. Curr Biol 15:656-660
28. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144:732-744
29. Chou DM, Adamson B, Dephoure NE, Tan X, Nottke AC, Hurov KE, Gygi SP, Colaiácovo MP, Elledge SJ (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 107:18475-18480
30. Chowdhury D, Xu X, Zhong X, Ahmed F, Zhong J, Liao J, Dykxhoorn DM, Weinstock DM, Pfeifer GP, Lieberman J (2008) A PP4- phosphatase complex dephosphorylates [gamma]-H2AX generated during DNA replication. Mol Cell 31:33-46 (Pubitemid 351905923)
31. Ciccia A, Elledge SJ (2010) The DNA damage response: making it safe to play with knives. Mol Cell 40:179-204
32. Cleaver JE, Lam ET, Revet I (2009) Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity. Nat Rev Genet 10:756-768
33. Cook PJ, Ju BG, Telese F, Wang X, Glass CK, Rosenfeld MG (2009) Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458:591-596
34. Costa RMA, Chiganças V, da Silva Galhardo R, Carvalho H, Menck CFM (2003) The eukaryotic nucleotide excision repair pathway. Biochimie 85:1083-1099 (Pubitemid 38142363)
35. Cowell IG, Sunter NJ, Singh PB, Austin CA, Durkacz BW, Tilby MJ (2007) γH2AX foci form preferentially in euchromatin after ionising-radiation. PLoS One 2:e1057
36. Das C, Lucia MS, Hansen KC, Tyler JK (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459:113-117
37. Datta A, Bagchi S, Nag A, Shiyanov P, Adami GR, Yoon T, Raychaudhuri P (2001) The p48 subunit of the damaged-DNA binding protein DDB associates with the CBP/p300 family of histone acetyltransferase. Mutat Res/DNA Repair 486:89-97 (Pubitemid 32568410)
38. Dellaire G, Kepkay R, Bazett-Jones DP (2009) High resolution imaging of changes in the structure and spatial organization of chromatin, γ-H2A.X and the MRN complex within etoposide-induced DNA repair foci. Cell Cycle 8:3750-3769
39. Difilippantonio S, Gapud E, Wong N, Huang C-Y, Mahowald G, Chen HT, Kruhlak MJ, Callen E, Livak F, Nussenzweig MC et al (2008) 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature 456:529-533 (Pubitemid 50304846)
40. Dimitrova N, Chen Y-CM, Spector DL, de Lange T (2008) 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456:524-528 (Pubitemid 50304845)
41. Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen DH, Pepperkok R, Ellenberg J, Panier S, Durocher D, Bartek J et al (2009) RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136:435-446
42. Downs JA, Allard S, Jobin-Robitaille O, Javaheri A, Auger A, Bouchard N, Kron SJ, Jackson SP, Côté J (2004) Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell 16:979-990 (Pubitemid 40018407)
43. Duan M-R, Smerdon MJ (2010) UV damage in DNA promotes nucleosome unwrapping. J Biol Chem 285:26295-26303
44. Elsässer SJ, D'Arcy S (2012) Towards a mechanism for histone chaperones. Biochima et Biophysica Acta (BBA) - Gene Regulatory Mechanisms. doi:10.1016/j.bbagrm.2011.07.007
45. Erdel F, Schubert T, Marth C, Längst G, Rippe K (2010) Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites. Proc Natl Acad Sci 107:19873-19878
46. Falk M, Lukasova E, Gabrielova B, Ondrej V, Kozubek S (2007) Chromatin dynamics during DSB repair. Biochimica et Biophysica Acta (BBA) - Molecular. Cell Res 1773:1534-1545
47. Fernandez-Capetillo O, Chen H-T, Celeste A, Ward I, Romanienko PJ, Morales JC, Naka K, Xia Z, Camerini-Otero RD, Motoyama N et al (2002) DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 4:993-997 (Pubitemid 35469431)
48. FitzGerald JE, Grenon M, Lowndes NF (2009) 53BP1: function and mechanisms of focal recruitment. Biochem Soc Trans 37:897-904
49. Fnu S, Williamson EA, De Haro LP, Brenneman M, Wray J, Shaheen M, Radhakrishnan K, Lee S-H, Nickoloff JA, Hromas R (2011) Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining. Proc Natl Acad Sci 108:540-545
50. Fousteri M, Vermeulen W, van Zeeland AA, Mullenders LHF (2006) Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol Cell 23:471-482 (Pubitemid 44226450)
51. Friedberg ECW, Graham C, Siede W, Wood RD, Schultz RA, Ellengberger T (2006) DNA repair and mutagenesis, 2nd edn. ASM, Washington
52. Gale JM, Nissen KA, Smerdon MJ (1987) UV-induced formation of pyrimidine dimers in nucleosome core DNA is strongly modulated with a period of 10.3 bases. Proc Natl Acad Sci 84:6644-6648
53. Giannattasio M, Follonier C, Tourrière H, Puddu F, Lazzaro F, Pasero P, Lopes M, Plevani P, Muzi-Falconi M (2010) Exo1 competes with repair synthesis, converts NER intermediates to long ssDNA gaps, and promotes checkpoint activation. Mol Cell 40:50-62
54. Giannattasio M, Lazzaro F, Plevani P, 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 (Pubitemid 40395835)
55. Ginjala V, Nacerddine K, Kulkarni A, Oza J, Hill SJ, Yao M, Citterio E, van Lohuizen M, 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
56. Gong F, Fahy D, Smerdon MJ (2006) Rad4-Rad23 interaction with SWI/SNF links ATP-dependent chromatin remodeling with nucleotide excision repair. Nat Struct Mol Biol 13:902-907 (Pubitemid 44527372)
57. Goodarzi AA, Kurka T, Jeggo PA (2011) KAP-1 phosphorylation regulates CHD3 nucleosome remodeling during the DNA double-strand break response. Nat Struct Mol Biol 18:831-839
58. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Löbrich M, Jeggo PA (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 31:167-177 (Pubitemid 352001394)
59. Green CM, Almouzni G (2003) Local action of the chromatin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. EMBO J 22:5163-5174
60. Grundy GJ, Yang W, Gellert M (2010) Autoinhibition of DNA cleavage mediated by RAG1 and RAG2 is overcome by an epigenetic signal in V(D)J recombination. Proc Natl Acad Sci 107:22487-22492
61. Guerrero-Santoro J, Kapetanaki MG, Hsieh CL, Gorbachinsky I, Levine AS, Rapić-Otrin V (2008) The cullin 4B-based UV-damaged DNA-binding protein ligase binds to UV-damaged chromatin and ubiquitinates histone H2A. Cancer Res 68:5014-5022
62. Guo R, Chen J, Mitchell DL, Johnson DG (2011) GCN5 and E2F1 stimulate nucleotide excision repair by promoting H3K9 acetylation at sites of damage. Nucleic Acids Res 39:1390-1397
63. Haber JE (2006) Transpositions and translocations induced by site-specific double-strand breaks in budding yeast. DNA Repair 5:998-1009
64. Hara R, Sancar A (2003) Effect of damage type on stimulation of human excision nuclease by SWI/SNF chromatin remodeling factor. Mol Cell Biol 23:4121-4125 (Pubitemid 36666417)
65. Hargreaves DC, Crabtree GR (2011) ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res 21:396-420
66. Helmink BA, Tubbs AT, Dorsett Y, Bednarski JJ, Walker LM, Feng Z, Sharma GG, McKinnon PJ, Zhang J, Bassing CH et al (2011) H2AX prevents CtIP-mediated DNA end resection and aberrant repair in G1-phase lymphocytes. Nature 469:245-249
67. Heo K, Kim H, Choi SH, Choi J, Kim K, Gu J, Lieber MR, Yang AS, An W (2008) FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell 30:86-97 (Pubitemid 351470156)
68. Hiom K (2010) Coping with DNA double strand breaks. DNA Repair 9:1256-1263
69. Holthausen JT, Wyman C, Kanaar R (2010) Regulation of DNA strand exchange in homologous recombination. DNA Repair 9:1264-1272
70. Huber A, Bai P, de Murcia JM, de Murcia G (2004) PARP-1, PARP-2 and ATM in the DNA damage response: functional synergy in mouse development. DNA Repair 3:1103-1108 (Pubitemid 38997953)
71. Huen MSY, Grant R, Manke I, Minn K, Yu X, Yaffe MB, Chen J (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131:901-914 (Pubitemid 350138083)
72. Huen MSY, Huang J, Leung JWC, Sy SMH, Leung KM, Ching Y-P, Tsao SW, Chen J (2010) Regulation of chromatin architecture by the PWWP domain-containing DNA damage-responsive factor EXPAND1/MUM1. Mol Cell 37:854-864
73. Huyen Y, Zgheib O, DiTullio RA Jr, Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES, Halazonetis TD (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406-411 (Pubitemid 39551676)
74. Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L, Trouche D, Legube G (2010) High-resolution profiling of [gamma]H2AX around DNA double strand breaks in the mammalian genome. EMBO J 29:1446-1457
75. Ikura T, Tashiro S, Kakino A, Shima H, Jacob N, Amunugama R, Yoder K, Izumi S, Kuraoka I, Tanaka K et al (2007) DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol Cell Biol 27:7028-7040 (Pubitemid 47549742)
76. Ismail IH, Andrin C, McDonald D, Hendzel MJ (2010) BMI1- mediated histone ubiquitylation promotes DNA double-strand break repair. J Cell Biol 191:45-60
77. Jakob B, Splinter J, Conrad S, Voss K-O, Zink D, Durante M, Löbrich M, Taucher-Scholz G (2011) DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res 39:6489-6499
78. Jiang Y, Wang X, Bao S, Guo R, Johnson DG, Shen X, Li L (2010) INO80 chromatin remodeling complex promotes the removal of UV lesions by the nucleotide excision repair pathway. Proc Natl Acad Sci 107:17274-17279
79. Jungmichel S, Stucki M (2010) MDC1: the art of keeping things in focus. Chromosoma 119:337-349
80. Kalocsay M, Hiller NJ, 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
81. Keogh M-C, Kim J-A, Downey M, Fillingham J, Chowdhury D, Harrison JC, Onishi M, Datta N, Galicia S, Emili A et al (2006) A phosphatase complex that dephosphorylates [gamma]H2AX regulates DNA damage checkpoint recovery. Nature 439:497-501 (Pubitemid 43152843)
82. Kim H, Chen J, Yu X (2007a) Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316:1202-1205 (Pubitemid 46877484)
83. Kim J-A, Kruhlak M, Dotiwala F, Nussenzweig A, Haber JE (2007b) Heterochromatin is refractory to γ-H2AX modification in yeast and mammals. J Cell Biol 178:209-218 (Pubitemid 47076458)
84. Kim J-K, Patel D, Choi B-S (1995) Contrasting structural impacts induced by cis-syn cyclobutane dimer and (6-4) adduct in DNA duplex decamers: implication in mutagenesis and repair activity. Photochem Photobiol 62:44-50
85. Kim Y-C, Gerlitz G, Furusawa T, Catez F, Nussenzweig A, Oh K-S, Kraemer KH, Shiloh Y, Bustin M (2009) Activation of ATM depends on chromatin interactions occurring before induction of DNA damage. Nat Cell Biol 11:92-96
86. Kolas NK, Chapman JR, Nakada S, Ylanko J, Chahwan R, Sweeney FD, Panier S, Mendez M, Wildenhain J, Thomson TM et al (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318:1637-1640 (Pubitemid 350233664)
87. Kruhlak MJ, Celeste A, Dellaire G, Fernandez-Capetillo O, Müller WG, McNally JG, Bazett-Jones DP, Nussenzweig A (2006) Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol 172:823-834
88. Kusch T, Florens L, MacDonald WH, Swanson SK, Glaser RL, Yates JR, Abmayr SM, Washburn MP, Workman JL (2004) Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306:2084-2087 (Pubitemid 40007658)
89. Lan L, Ui A, Nakajima S, Hatakeyama K, Hoshi M, Watanabe R, Janicki SM, Ogiwara H, Kohno T, Kanno S-i et al (2010) The ACF1 complex is required for DNA double-strand break repair in human cells. Mol Cell 40:976-987
90. Larsen DH, Poinsignon C, Gudjonsson T, Dinant C, Payne MR, Hari FJ, Rendtlew Danielsen JM, Menard P, Sand JC, Stucki M et al (2010) The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol 190:731-740
91. Lazzaro F, Giannattasio M, Puddu F, Granata M, Pellicioli A, Plevani P, Muzi-Falconi M (2009) Checkpoint mechanisms at the intersection between DNA damage and repair. DNA Repair 8:1055-1067
92. Lazzaro F, Sapountzi V, Granata M, Pellicioli A, Vaze M, Haber JE, Plevani P, Lydall D, Muzi-Falconi M (2008) Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J 27:1502-1512 (Pubitemid 351733336)
93. Lee H-S, Park J-H, Kim S-J, Kwon S-J, 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
94. Lee J-H, Goodarzi AA, Jeggo PA, Paull TT (2010b) 53BP1 promotes ATM activity through direct interactions with the MRN complex. EMBO J 29:574-585
95. Lee JH, Paull TT (2007) Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26:7741-7748
96. Li G, Reinberg D (2011) Chromatin higher-order structures and gene regulation. Curr Opin Genet Dev 21:175-186
97. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134:244-255
98. Li X, Corsa CAS, Pan PW, Wu L, Ferguson D, Yu X, Min J, 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
99. Liang B, Qiu J, Ratnakumar K, Laurent BC (2007) RSC functions as an early double-strand-break sensor in the cell's response to DNA damage. Curr Biol 17:1432-1437 (Pubitemid 47259384)
100. Lieber MR, Gu J, Lu H, Shimazaki N, Tsai AG (2010) Nonhomologous DNA end joining (NHEJ) and chromosomal translocations in humans. In: Nasheuer H-P (ed) Genome stability and human diseases. Springer, the Netherlands, pp 279-296
101. Lin S-Y, Rai R, Li K, Xu Z-X, Elledge SJ (2005) BRIT1/MCPH1 is a DNA damage responsive protein that regulates the Brca1-Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc Natl Acad Sci U S A 102:15105-15109 (Pubitemid 41513342)
102. Lou Z, Minter-Dykhouse K, Franco S, Gostissa M, Rivera MA, Celeste A, Manis JP, van Deursen J, Nussenzweig A, Paull TT et al (2006) MDC1 Maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol Cell 21:187-200 (Pubitemid 43099935)
103. Lowndes NF (2010) The interplay between BRCA1 and 53BP1 influences death, aging, senescence and cancer. DNA Repair 9:1112-1116
104. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8[thinsp]A resolution. Nature 389:251-260 (Pubitemid 27406632)
105. Luijsterburg MS, Dinant C, Lans H, Stap J, Wiernasz E, Lagerwerf S, Warmerdam DO, Lindh M, Brink MC, Dobrucki JW et al (2009) Heterochromatin protein 1 is recruited to various types of DNA damage. J Cell Biol 185:577-586
106. Luijsterburg MS, van Attikum H (2011) Chromatin and the DNA damage response: the cancer connection. Mol Onc 5:349-267
107. Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, Lukas J (2007) RNF8 ubiquitylates histones at DNA doublestrand breaks and promotes assembly of repair proteins. Cell 131:887-900 (Pubitemid 350138084)
108. Manis JP, Morales JC, Xia Z, Kutok JL, Alt FW, Carpenter PB (2004) 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat Immunol 5:481-487 (Pubitemid 38660459)
109. Manke IA, Lowery DM, Nguyen A, Yaffe MB (2003) BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302:636-639 (Pubitemid 37310918)
110. Marteijn JA, Bekker-Jensen S, Mailand N, Lans H, Schwertman P, Gourdin AM, Dantuma NP, Lukas J, 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
111. Marti TM, Hefner E, Feeney L, Natale V, Cleaver JE (2006) H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc Natl Acad Sci 103:9891-9896 (Pubitemid 43993593)
112. Martinez E, Palhan VB, Tjernberg A, Lymar ES, Gamper AM, Kundu TK, Chait BT, Roeder RG (2001) Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol Cell Biol 21:6782-6795 (Pubitemid 32911240)
113. Matthews AGW, Kuo AJ, Ramon-Maiques S, Han S, Champagne KS, Ivanov D, Gallardo M, Carney D, Cheung P, Ciccone DN et al (2007) RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 450:1106-1110 (Pubitemid 350273622)
114. Mehrotra PV, Ahel D, Ryan DP, Weston R, Wiechens N, Kraehenbuehl R, Owen-Hughes T, Ahel I (2011) DNA repair factor APLF is a histone chaperone. Mol Cell 41:46-55
115. Melander F, Bekker-Jensen S, Falck J, Bartek J, Mailand N, Lukas J (2008) Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J Cell Biol 181:213-226 (Pubitemid 351574548)
116. Messner S, Altmeyer M, Zhao H, Pozivil A, Roschitzki B, Gehrig P, Rutishauser D, Huang D, Caflisch A, Hottiger MO (2010) PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res 38:6350-6362
117. Miller KM, Tjeertes JV, Coates J, Legube G, Polo SE, Britton S, Jackson SP (2010) Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol 17:1144-1151
118. Mochan TA, Venere M, DiTullio RA, Halazonetis TD (2003) 53BP1 and NFBD1/MDC1-Nbs1 function in parallel interacting pathways activating ataxia-telangiectasia mutated (ATM) in response to DNA damage. Cancer Res 63:8586-8591 (Pubitemid 38064030)
119. Morrison AJ, Highland J, Krogan NJ, Arbel-Eden A, Greenblatt JF, Haber JE, Shen X (2004) INO80 and [gamma]-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119:767-775 (Pubitemid 40017684)
120. Morrison AJ, Shen X (2009) Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat Rev Mol Cell Biol 10:373-384
121. Moyal L, Lerenthal Y, Gana-Weisz M, Mass G, So S, Wang S-Y, Eppink B, Chung YM, Shalev G, Shema E et al (2011) Requirement of ATM-dependent monoubiquitylation of histone H2B for timely repair of DNA double-strand breaks. Mol Cell 41:529-542
122. Murr R, Loizou JI, Yang Y-G, Cuenin C, Li H, Wang Z-Q, 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 (Pubitemid 43064802)
123. Nakamura K, Kato A, Kobayashi J, Yanagihara H, Sakamoto S, Oliveira DVNP, Shimada M, Tauchi H, Suzuki H, Tashiro S et al (2011) Regulation of homologous recombination by RNF20- dependent H2B ubiquitination. Mol Cell 41:515-528
124. Oda H, Okamoto I, Murphy N, Chu J, Price SM, Shen MM, Torres- Padilla ME, Heard E, 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
125. Ogiwara H, Ui A, Otsuka A, Satoh H, Yokomi I, Nakajima S, Yasui A, Yokota J, Kohno T (2011) Histone acetylation by CBP and p300 at double-strand break sites facilitates SWI/SNF chromatin remodeling and the recruitment of non-homologous end joining factors. Oncogene 30:2135-2146
126. Oh K-S, Bustin M, Mazur SJ, Appella E, Kraemer KH (2011) UV-induced histone H2AX phosphorylation and DNA damage related proteins accumulate and persist in nucleotide excision repair-deficient XP-B cells. DNA Repair 10:5-15
127. Palomera-Sanchez Z, Bucio-Mendez A, Valadez-Graham V, Reynaud E, Zurita M (2010) Drosophila p53 is required to increase the levels of the dKDM4B demethylase afterUV-induced DNAdamage to demethylate histone H3 lysine 9. J Biol Chem 285:31370-31379
128. Papamichos-Chronakis M, Krebs JE, Peterson CL (2006) Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev 20:2437-2449 (Pubitemid 44320391)
129. Park J-H, Park E-J, Lee H-S, Kim SJ, Hur S-K, Imbalzano AN, Kwon J (2006) Mammalian SWI/SNF complexes facilitate DNA doublestrand break repair by promoting [gamma]-H2AX induction. EMBO J 25:3986-3997 (Pubitemid 44338741)
130. Pavri R, Zhu B, Li G, Trojer P, Mandal S, Shilatifard A, Reinberg D (2006) HistoneH2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125:703-717 (Pubitemid 43732350)
131. Pei H, Zhang L, Luo K, Qin Y, Chesi M, Fei F, Bergsagel PL, Wang L, You Z, Lou Z (2011) MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470:124-128 Peng A, Chen P-L (2003) NFBD1, like 53BP1, is an early and redundant transducer mediating Chk2 phosphorylation in response to DNA damage. J Biol Chem 278:8873-8876
132. Peng G, Lin S-Y (2009) BRIT1/MCPH1 is a multifunctional DNA damage responsive protein mediating DNA repair-associated chromatin remodeling. Cell Cycle 8:3071-3072
133. Pinto DMS, Flaus A (2010) Structure and function of histone H2AX. In: Nasheuer H-P (ed) Genome stability and human diseases. Springer, the Netherlands, pp 55-78
134. Polo SE, Jackson SP (2011) Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 25:409-433
135. Polo SE, Kaidi A, Baskcomb L, Galanty Y, Jackson SP (2010) Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J 29:3130-3139
136. Polo SE, Roche D, Almouzni G (2006) New histone incorporation marks sites of UV repair in human cells. Cell 127:481-493 (Pubitemid 44647423)
137. Postow L, Ghenoiu C, Woo EM, Krutchinsky AN, Chait BT, Funabiki H (2008) Ku80 removal from DNA through double strand break-induced ubiquitylation. J Cell Biol 182:467-479
138. Qing Y, Yamazoe M, Hirota K, Dejsuphong D, Sakai W, Yamamoto KN, Bishop DK, Wu X, Takeda S (2011) The epistatic relationship between BRCA2 and the other RAD51 mediators in homologous recombination. PLoS Genet 7:e1002148
139. Rai R, Dai H, Multani AS, Li K, Chin K, Gray J, Lahad JP, Liang J, Mills GB, Meric-Bernstam F et al (2006) BRIT1 regulates early DNA damage response, chromosomal integrity, and cancer. Cancer Cell 10:145-157 (Pubitemid 44175904)
140. Ramanathan B, Smerdon MJ (1989) Enhanced DNA repair synthesis in hyperacetylated nucleosomes. J Biol Chem 264:11026-11034 (Pubitemid 19168826)
141. Rodrigue A, Lafrance M, Gauthier M-C, McDonald D, Hendzel M, West SC, Jasin M, Masson J-Y (2006) Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J 25:222-231 (Pubitemid 43077310)
142. Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905-916
143. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858-5868 (Pubitemid 28124064)
144. Rouet P, Smih F, Jasin M (1994) Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol Cell Biol 14:8096-8106 (Pubitemid 24373558)
145. Rubbi CP, Milner J (2003) p53 is a chromatin accessibility factor for nucleotide excision repair of DNA damage. EMBO J 22:975-986 (Pubitemid 36227799)
146. Rulten SL, Fisher AEO, Robert I, Zuma MC, Rouleau M, Ju L, Poirier G, Reina-San-Martin B, Caldecott KW (2011) PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol Cell 41:33-45
147. Sánchez-Molina S, Mortusewicz O, Bieber B, Auer S, Eckey M, Leonhardt H, Friedl AA, Becker PB (2011) Role for hACF1 in the G2/M damage checkpoint. Nucleic Acids Res 39:8445-8456
148. Sanders SL, Portoso M, Mata J, Bähler J, Allshire RC, Kouzarides T (2004) Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603-614 (Pubitemid 39535749)
149. Sandhu SK, Yap TA, de Bono JS (2011) The emerging role of poly (ADP-ribose) polymerase inhibitors in cancer treatment. Curr Drug Targets 12:2034-2044
150. Sarkar S, Kiely R, McHugh PJ (2010) The Ino80 chromatin-remodeling complex restores chromatin structure during UV DNA damage repair. J Cell Biol 191:1061-1068
151. Schreiber V, Dantzer F, Ame J-C, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517-528 (Pubitemid 44036457)
152. Sertic S, Pizzi S, Cloney R, Lehmann AR, Marini F, Plevani P, Muzi- Falconi M (2011) Human exonuclease 1 connects nucleotide excision repair (NER) processing with checkpoint activation in response to UV irradiation. Proc Natl Acad Sci 108:13647-13652
153. Sharma GG, So S, Gupta A, Kumar R, Cayrou C, Avvakumov N, Bhadra U, Pandita RK, PorteusMH, Chen DJ et al (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
154. Shim EY, Ma J-L, Oum J-H, Yanez Y, Lee SE (2005) The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol Cell Biol 25:3934-3944 (Pubitemid 40617645)
155. Shimazaki N, Tsai AG, Lieber MR (2009) H3K4me3 stimulates the V (D)J RAG complex for both nicking and hairpinning in trans in addition to tethering in cis: implications for translocations. Mol Cell 34:535-544
156. Shogren-Knaak M, Ishii H, Sun J-M, Pazin MJ, Davie JR, Peterson CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844-847 (Pubitemid 43228847)
157. Smeenk G, Wiegant WW, Vrolijk H, Solari AP, Pastink A, van Attikum H (2010) The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J Cell Biol 190:741-749
158. Smith J, Mun Tho L, Xu N, Gillespie DA (2010) The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. In: George FVW, George K (eds) Advances in cancer research. Academic, New York, pp 73-112
159. Sobhian B, Shao G, Lilli DR, Culhane AC, Moreau LA, Xia B, Livingston DM, Greenberg RA (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316:1198-1202 (Pubitemid 46877483)
160. Spycher C, Miller ES, Townsend K, Pavic L, Morrice NA, Janscak P, Stewart GS, Stucki M (2008) Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J Cell Biol 181:227-240 (Pubitemid 351574549)
161. Stewart GS, Panier S, Townsend K, Al-Hakim AK, Kolas NK, Miller ES, Nakada S, Ylanko J, Olivarius S, Mendez M et al (2009) The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136:420-434
162. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP (2005) MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123:1213-1226 (Pubitemid 41821780)
163. Suganuma T, Workman JL (2011) Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80:473-499
164. Sunavala-Dossabhoy G, De Benedetti A (2009) Tousled homolog, TLK1, binds and phosphorylates Rad9; TLK1 acts as a molecular chaperone in DNA repair. DNA Repair 8:87-102
165. Suquet C, Smerdon MJ (1993) UV damage to DNA strongly influences its rotational setting on the histone surface of reconstituted nucleosomes. J Biol Chem 268:23755-23757 (Pubitemid 23335338)
166. Sy SMH, Huen MSY (2010) The 53BP1-EXPAND connection in chromatin structure regulation. Nucleus 1:3
167. Takedachi A, Saijo M, Tanaka K (2010) DDB2 complex-mediated ubiquitylation around DNA damage is oppositely regulated by XPC and Ku and contributes to the recruitment of XPA. Mol Cell Biol 30:2708-2723
168. Tamburini BA, Tyler JK (2005) Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol 25:4903-4913 (Pubitemid 40781092)
169. Telford DJ, Stewart BW (1989) Micrococcal nuclease: its specificity and use for chromatin analysis. Int J Biochem 21:127-138
170. Tjeertes JV, Miller KM, Jackson SP (2009) Screen for DNA-damage- responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J 28:1878-1889
171. Tsukuda T, Fleming AB, Nickoloff JA, Osley MA (2005) Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438:379-383
172. Utley RT, Lacoste N, Jobin-Robitaille O, Allard S, 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 (Pubitemid 41263009)
173. van Attikum H, Fritsch O, Gasser SM (2007) Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J 26:4113-4125 (Pubitemid 47462094)
174. van Attikum H, Fritsch O, Hohn B, Gasser SM (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777-788 (Pubitemid 40017685)
175. Vempati RK, Jayani RS, Notani D, Sengupta A, Galande S, Haldar D (2010) p300-mediated acetylation of histone H3 lysine 56 functions in DNA damage response in mammals. J Biol Chem 285:28553-28564
176. Vrouwe MG, Pines A, Overmeer RM, Hanada K, Mullenders LHF (2011) UV-induced photolesions elicit ATR-kinase-dependent signaling in non-cycling cells through nucleotide excision repair-dependent and -independent pathways. J Cell Sci 124:435-446
177. Wagner CR, Kuervers L, Baillie DL, Yanowitz JL (2010) xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature 467:839-843
178. Wang B, Matsuoka S, Ballif BA, Zhang D, Smogorzewska A, Gygi SP, Elledge SJ (2007) Abraxas and RAP80 Form a BRCA1 protein complex required for the DNA damage response. Science 316:1194-1198 (Pubitemid 46877482)
179. Wang BSCPES (2002) 53BP1, a medicator of the DNA damage checkpoint. Science 298:1435
180. Wang H, Zhai L, Xu J, Joo H-Y, Jackson S, Erdjument-Bromage H, Tempst P, Xiong Y, 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 (Pubitemid 44308132)
181. Ward IM, Minn K, van Deursen J, Chen J (2003) p53 binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol Cell Biol 23:2556-2563 (Pubitemid 36351034)
182. Ward IM, Reina-San-Martin B, Olaru A, Minn K, Tamada K, Lau JS, CascalhoM, Chen L, Nussenzweig A, Livak F et al (2004) 53BP1 is required for class switch recombination. J Cell Biol 165:459-464 (Pubitemid 38679611)
183. Warmerdam DO, Kanaar R (2010) Dealing with DNA damage: relationships between checkpoint and repair pathways. Mutat Res Rev Mutat Res 704:2-11
184. Wilson KA, Stern DF (2008) NFBD1/MDC1, 53BP1 and BRCA1 have both redundant and unique roles in the ATM pathway. Cell Cycle 7:3584-3594
185. Wood JL, Singh N, Mer G, Chen J (2007) MCPH1 functions in an H2AX-dependent but MDC1-independent pathway in response to DNA damage. J Biol Chem 282:35416-35423 (Pubitemid 350232410)
186. Wu L, Luo K, Lou Z, Chen J (2008) MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc Natl Acad Sci 105:11200-11205
187. Wu S, Shi Y, Mulligan P, Gay F, Landry J, Liu H, Lu J, Qi HH, Wang W, Nickoloff JA et al (2007) A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat Struct Mol Biol 14:1165-1172 (Pubitemid 350223334)
188. Wysocki R, Javaheri A, Allard S, Sha F, Cote J, Kron SJ (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 (Pubitemid 41369165)
189. Xiao A, Li H, Shechter D, Ahn SH, Fabrizio LA, Erdjument-Bromage H, Ishibe-Murakami S, Wang B, Tempst P, Hofmann K et al (2009) WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457:57-62
190. Xie A, Hartlerode A, Stucki M, Odate S, Puget N, Kwok A, Nagaraju G, Yan C, Alt FW, Chen J et al (2007) Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian doublestrand break repair. Mol Cell 28:1045-1057 (Pubitemid 350297033)
191. Xu Y, Sun Y, Jiang X, Ayrapetov MK, Moskwa P, Yang S, Weinstock DM, Price BD (2010) The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J Cell Biol 191:31-43
192. Yan J, Kim Y-S, Yang X-P, Li L-P, Liao G, Xia F, Jetten AM (2007) The ubiquitin-interacting motif-containing protein RAP80 interacts with BRCA1 and functions in DNA damage repair response. Cancer Res 67:6647-6656 (Pubitemid 47105510)
193. Yan Q, Dutt S, Xu R, Graves K, Juszczynski P, Manis JP, Shipp MA (2009) BBAP monoubiquitylates histone H4 at lysine 91 and selectively modulates the DNA damage response. Mol Cell 36:110-120
194. You Z, Bailis JM (2010) DNA damage and decisions: CtIP coordinates DNA repair and cell cycle checkpoints. Trends Cell Biol 20:402-409
195. Yu S, Teng Y, Waters R, Reed SH (2011) How chromatin is remodelled during DNA repair of UV-induced DNA damage in Saccharomyces cerevisiae. PLoS Genet 7:e1002124
196. Yu X, Chen J (2004) DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol Cell Biol 24:9478-9486 (Pubitemid 39391684)
197. Yu X, Chini CCS, He M, Mer G, Chen J (2003) The BRCT domain is a phospho-protein binding domain. Science 302:639-642 (Pubitemid 37310919)
198. Yu Y, Teng Y, Liu H, Reed SH, Waters R (2005) UV irradiation stimulates histone acetylation and chromatin remodeling at a repressed yeast locus. Proc Natl Acad Sci U S A 102:8650-8655 (Pubitemid 40862790)
199. Yuan G, Zhu B (2011) Histone variants and epigenetic inheritance. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms (in press, corrected proof)
200. Yuan J, Adamski R, Chen J (2010) Focus on histone variant H2AX: to be or not to be. FEBS Lett 584:3717-3724
201. Yun MH, Hiom K (2009) CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature 459:460-463
202. Zarebski M, Wiernasz E, Dobrucki JW (2009) Recruitment of heterochromatin protein 1 to DNA repair sites. Cytometry Part A 75A:619-625
203. Zhao GY, Sonoda E, Barber LJ, Oka H, Murakawa Y, Yamada K, Ikura T, Wang X, Kobayashi M, Yamamoto K et al (2007) A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination. Mol Cell 25:663-675 (Pubitemid 46341920)
204. Zhao Q, Wang Q-E, Ray A, Wani G, Han C, Milum K, Wani AA (2009) Modulation of nucleotide excision repair by mammalian SWI/SNF chromatin-remodeling complex. J Biol Chem 284:30424-30432
205. Zhu Q, Wani G, Arab HH, El-Mahdy MA, Ray A, Wani AA (2009) Chromatin restoration following nucleotide excision repair involves the incorporation of ubiquitinated H2A at damaged genomic sites. DNA Repair 8:262-273
206. Ziv Y, Bielopolski D, Galanty Y, Lukas C, Taya Y, Schultz DC, Lukas J, Bekker-Jensen S, Bartek J, Shiloh Y (2006) Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat Cell Biol 8:870-876 (Pubitemid 44151591)