Chromatin dynamics coupled to DNA repair

Epigenetics

Volumn 4, Issue 1, 2009, Pages 31-42

  Huertas, Dori ^a   Sendra, Ramon ^a   Muñoz, Purificación ^a  

^a CATALAN INSTITUTE OF ONCOLOGY   (Spain)

Author keywords

ATP remodeling complexes; Chromatin modifications; DNA damage response; DNA repair; Epigenetics

Indexed keywords

ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; GENOMIC DNA; HISTONE; HISTONE H2AX;

AMINO TERMINAL SEQUENCE; APOPTOSIS; CANCER SUSCEPTIBILITY; CARBOXY TERMINAL SEQUENCE; CELL DAMAGE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CHROMOSOME REARRANGEMENT; DNA DAMAGE; DNA DETERMINATION; DNA FRAGMENTATION; DNA METABOLISM; DNA MODIFICATION; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; DNA SYNTHESIS; EPIGENETICS; EUCHROMATIN; GENE AMPLIFICATION; GENETIC RECOMBINATION; GENETIC REGULATION; HETEROCHROMATIN; HUMAN; MAMMAL CELL; MISMATCH REPAIR; MOLECULAR INTERACTION; NONHUMAN; NUCLEOSOME; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN METHYLATION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; UBIQUITINATION;

EUKARYOTA;

EID: 66349130703     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.4.1.7733     Document Type: Review

References (145)

1. Lindhal T. Instability and decay of the primary structure of DNA. Nature 1993; 362:709-15.
2. Khanna KK, Jackson SP. DNA double-strand breaks: signalling, repair and cancer connection. Nat Genet 2001; 27:247-54.
3. Lieber MR, Ma Y, Pannicke U, Schwarz K. Mechanisms and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol 2003; 4:712-20.
4. Ataian Y, Krebs JE. Five repair pathways in one context: chromatin modification during DNA repair. Biochem Cell Biol 2006; 84:490-504.
5. van Gent D, Hoeijmakers JH, Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat Rev Genet 2001; 2:196-206.
6. Shiloh Y. ATM and related proteins kinases: safeguarding genome integrity. Nat Rev Cancer 2003; 3:155-68.
7. Cahill D, Connor B, Carney JP. Mechanisms of eukaryotic DNA double strand break repair. Front Biosci 2006; 11:1958-76.
8. Kim JS, Krasieva TB, Kurumizaka H, Chen DJ, Taylor AM, Yokomori K. Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells. J Cell Biol 2005; 170:341-7.
9. Arents G, Moudrianakis EN. Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. Proc Natl Acad Sci USA 1993; 90:10489-93.
10. Horn PJ, Peterson CL. Chromatin higher order folding - wrapping up transcription. Science 2002; 297:1824-7.
11. Loyola A, Almouzni G. Parking histone H3 variants: How, when and why?. Trends in Biochem Sci 2007; 32:425-33.
12. Iizuka M, Smith MM. Functional consequences of histone modifications. Curr Opin Genet Dev 2003; 13:154-60.
13. Escargueil AE, Soares DG, Salvador M, Larsen AK, Henriques JA. What histone code for DNA repair? Mut Res 2008; 658:259-70.
14. Saha A, Wittmeyer J, Cairns BR. Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 2006; 7:437-47.
15. Osley MA, Tsukuda T, Nickoloff JA. ATP-dependent chromatin remodelling factors and DNA damage repair. Mut Res 2007; 618:65-80.
16. Smerdon MJ. DNA repair and the role of chromatin structure. Curr Opin Cell Biol 1991; 3:422-8.
17. Groth A, Rocha W, Verreault A, Almouzni G. Chromatin challenges during DNA replication and repair. Cell 2007; 128:721-33.
18. Kanaar R, Wyman C. DNA repair by the MRN complex: break it to make it. Cell 2008; 135:14-6.
19. Williams RS, et al. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand break repair. Cell 2008; 135:97-109.
20. Falk J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005; 434:605-11.
21. Lou Z, et al. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol Cell 2006; 21:187-200.
22. Deng CX. BRCA1: cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res 2006; 34:1416-26.
23. Xie A, et al. Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol Cell 2007; 28:1045-57.
24. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273:5858-68.
25. Downs JA, Lowndes NF, Jackson SP. A role for Saccaromyces cerevisiae histone H2A in DNA repair. Nature 2000; 408:1001-4.
26. Madigan JP, Chotkowski HL, Glaser RL. DNA double-strand break-induced phosphorylation of Drosophila melanogaster histone variant H2Av helps prevent radiation-induced apoptosis. Nucleic Acids Res 2002; 30:3698-705.
27. Czornak K, Chughtai S, Chrzanowska KH. Mystery of DNA repair: the role of the MRN complex and ATM kinase in DNA damage repair. J Appl Genet 2008; 49:383-96.
28. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008; 9:616-27.
29. Stiff T, et al. ATM and DNA-PK function redundantly to phosphorylate H2AX exposure to ionizing radiation. Cancer Res 2004; 64:2390-6.
30. Reitsema T, Klokov D, Banáth JP, Olive PL. DNA-PK is responsible for enhanced phosphorylation of histone H2AX under hypertonic conditions. DNA Repair 2005; 4:1172-81.
31. Mukherjee B, et al. DNA-PK phosphorylates H2AX during apoptotic DNA fragmentation in mammalian cells. DNA Repair 2006; 5:575-90.
32. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506.
33. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001; 276:42462-7.
34. Stucki M, et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNa double-strand breaks. Cell 2005; 123:1213-26.
35. Shroff R, et al. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr Biol 2004; 14:1703-11.
36. Pilch DR, et al. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem Cell Biol 2003; 81:123-9.
37. Manke IA, Lowery DM, Nguyen A, Yaffe MB. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 2003; 302:636-9.
38. Celeste A, et al. Genomic instability in mice lacking histone H2AX. Science 2002; 296:922-7.
39. Fernandez-Capetillo O, Celeste A, Nussenzweig A. Focusing on foci: H2AX and the recruitment of DNA-damage response factors. Cell Cycle 2003; 2:426-7.
40. Celeste A, et al. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 2003; 5:675-9.
41. Tsukuda T, Fleming AB, Nickoloff JA, Olsey MA. Chromatin remodeling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 2005; 438:349-83.
42. Kruhlak MJ, et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol 2006; 172:823-34.
43. Kanu N, Behrens A. ATMIN defines an NBS1-independent pathway of ATM signaling. EMBO J 2007; 26:2933-41.
44. Ziv Y, et al. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat Cell Biol 2006; 8:870-6.
45. Shim EY, Ma JL, Oum JH, Yanez Y, Lee SE. The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol Cell Biol 2005; 25:3934-44.
46. Shim EY, Hong SJ, Oum JH, Yanez Y, Zhang Y, Lee SE. RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol Cell Biol 2007; 27:1602-13.
47. Liang B, Qiu J, Ratnakumar K, Laurent BC. RSC functions as an early double-strand break sensor in the cell's response to DNA damage. Curr Biol 2007; 17:1432-7
48. Park JH, et al. Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting gamma-H2AX induction. EMBO J 2006; 25:3986-97.
49. Sun Y, Jiang X, Chen S, Fernandes N, Price BD. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc Natl Acad Sci USA 2005; 102:13182-7.
50. Jiang X, Sun Y, Chen S, Roy K, Price BD. The FACT domains of PIKK proteins are functionally equivalent and participate in the Tip60-dependent activation of DNA-PKcs and ATM. J Biol Chem 2006; 281:15741-6.
51. Sanders SL, et al. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 2004; 119:603-14.
52. Du LL, Nakamura TM, Russell P. Histone modification-dependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev 2006; 20:1583-96.
53. Nakamura TM, Moser BA, Du LL, Russell P. Cooperative control of Crb2 by ATM family and Cdc2 kinases is essential for the DNA damage checkpoint in fission yeast. Mol Cell Biol 2005; 25:10721-30.
54. Botuyan MV, et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 2006; 127:1361-73.
55. Yang H, et al. Preferential dimethylation of histone H4 lysine 20 by Suv4-20. J Biol Chem 2008; 283:12085-92.
56. Sun ZW, Allis CD. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 2002; 418:104-8.
57. Shahbazian MD, Zhang K, Grunstein M. Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol Cell 2005; 19:271-7.
58. Giannattasio M, Lazzaro F, Plevani P, Muzi-Falconi M. The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J Biol Chem 2005; 280:9879-86.
59. 1 and S phase DNA damage checkpoint functions of Rad9. Mol Cell Biol 2005; 25:8430-43.
60. Grenon M, et al. Docking onto chromatin via the Saccharomyces cerevisiae Rad9 Tudor domain. Yeast 2007; 24:105-19.
61. Puddu F, et al. Phosphorylation of the budding yeast 9-1-1 complex is required for Dpb11 function in the full activation of the UV-induced DNA damage checkpoint. Mol Cell Biol 2008; 28:4782-93.
62. Evans ML, et al. UV sensitive mutations in histone H3 in Saccharomyces cerevisiae that alter specific K79 methylation states genetically act through distinct DNA repair pathways. Curr Genet 2008; 53:259-74.
63. Huyen Y, et al. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 2004; 432:406-11.
64. Bergink S, et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev 2006; 20:1343-52.
65. Wang H, et al. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell 2006; 22:383-94.
66. Wang B, Elledge SJ. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Bcra1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci USA 2007; 104:20759-63.
67. Huen MS, et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007; 131:901-14
68. Sakasai R, Tibbetts R. RNF8-dependent and RNF8-independent regulation of 53BP1 in response to DNA damage. J Biol Chem 2008; 283:13549-55.
69. West SC. Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol 2003; 4:435-45.
70. Wyman C, Kanaar R. DNA double-strand break repair: all's well that ends well. Annu Rev Genet 2006; 40:363-83.
71. San Filippo J, Sung P, Klein H. Mechanism of eukaryotic homologous recombination. Ann Rev Biochem 2008; 77:229-57.
72. Chen S, et al. Accurate in vitro end joining of a DNA double strand break with partially cohesive 3′-overhangs and 3′phosphoglycolate termini: effect of Ku on repair fidelity. J Biol Chem 2001; 276:24323-30.
73. Dip R, Naegeli H. More than just strand breaks: the recognition of structural DNA discontinuities by DNA-dependent protein kinase catalytic subunit. FASEB J 2005; 19:704-15.
74. Buck D, et al. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 2006; 124:287-99.
75. Wu PY, Frit P, Malivert L, Revy P, Blard D, Salles B, Calsou P. Interplay between Cernunnos-XLF and nonhomologous end-joining proteins at DNA ends in the cell. J Biol Chem 2007; 282:31937-43.
76. Dahm K. Role and regulation of human XRCC4-like factor/cernunnos. J Cell Biochem 2008; 104:1534-40.
77. Narlikar GJ, Fan HY, Kingston RE. Cooperation between complexes that regulate chromatin structure and transcription. Cell 2002; 108:475-87.
78. Bird AW, et al. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 2002; 419:411-5.
79. Tamburini BA, Tyler JK. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol 2005; 25:4903-13.
80. Qin S, Parthun MR. Recruitment of the type B histone acetyltransferase Hat1p to chromatin is linked to DNA double-strand breaks. Mol Cell Biol 2006; 26:3649-58.
81. Murr R, et al. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 2006; 8:91-9.
82. Ikura T, et al. DNA damage dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol Cell Biol 2007; 27:7023-40.
83. Downs JA, et al. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell 2004; 16:979-90.
84. Choy JS, Kron SJ. Nu4A subunit Yng2 function in intra-S-phase DNA damage response. Mol Cell Biol 2002; 22:8215-25.
85. Jha S, Shibata E, Dutta A. Human Rvb1/tip49 is required for the histone acetyltransferase activity of Tip60/NuA4 and for the downregulation of phosphorylation on H2AX after DNA damage. Mol Cell Biol 2008; 28:2690-700.
86. Jonsson ZO, Jha S, Wohlschlegel JA, Dutta A. Rcb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodelling complex. Mol Cell 2004; 16:465-77.
87. Jin Y, et al. A mammalian chromatin remodelling complex with similarities to the yeast INO80 complex. J Biol Chem 2005; 280:41207-12.
88. Cai Y, et al. The mammalian YL1 protein is a shared subunit of the TRRAP/ TIP60 histone acetyltransferase and SRCAP complex. J Biol Chem 2005; 280:13665-70.
89. Gribun A, Cheung KL, Huen J, Ortega J, Houry WA. Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex. J Mol Biol 2008; 376:1320-33.
90. Matsuoka S, et al. ATM and ATR substrate analysis reveals extensive protein network responsive to DNA damage. Science 2007; 316:1160-6.
91. Parthun MR. Hat1: the emerging cellular roles of a type B histone acetyltransferase. Oncogene 2007; 26:5319-28.
92. Qin S, Parthun MR. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol Cell Biol 2002; 22:8353-65.
93. Barman HK, et al. Histone acetyltransferase 1 is dispensable for replication-coupled chromatin assembly but contributes to recover DNA damages created following replication blockage in vertebrate cells. Biochem Biophys Res Comm 2006; 354:1547-57.
94. Jazayeri A, McAinsh AD, Jackson SP. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc Natl Acad Sci USA 2004; 101:1644-9.
95. Berkovich E, Monnat RJ, Kastan MB. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat Cell Biol 2007; 9:683-90.
96. Rodrigue A, et al. Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J 2006; 25:222-31.
97. Morrison AJ, et al. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 2004; 119:767-75.
98. Papamichos-Chronakis M, Krebs JE, Peterson CL. Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev 2006; 20:2437-49.
99. van Attikum H, Fritsch O, Hohn B, Gasser SM. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 2004; 119:777-88.
100. Kobor MS, et al. A protein complex containing the conserved Swi2/ Snf2-repeated ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2004; 2:131.
101. Babiarz JE, Halley PD, Rine J. Telomeric heterochromatin boundaries require Nu4A-dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae. Genes Dev 2006; 20:700-10.
102. Keogh MC, et al. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 2006; 439:497-501.
103. Millar CB, Xu F, Zhang K, Grunstein M. Acetylation of H2AZ Lys14 is associated with genome-wide gene activity in yeast. Genes Dev 2006; 20:711-22.
104. Kusch T, et al. Acetylation by Tip60 is required for selective histone variant exchanges at DNA lesions. Science 2004; 306:204-7.
105. van Attikum H, Fritsch O, Gasser S. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J 2007; 26:4113-25.
106. Krogh BO, Symington LS. Recombination proteins in yeast. Annu Rev Genet 2004; 38:233-71.
107. Morrison AJ, et al. Mec1/Tel1 phosphorylation of the INO80 chromatin remodelling complex influences DNA damage checkpoint responses. Cell 2007; 130:499-511.
108. Chai B, Huang J, Cairos BR, Laurent BC. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev 2005; 19:1656-61.
109. Huang J, Hsu JM, Laurent BC. The RSC nucleosome-remodeling complex is required for cohesin's association with chromosome arms. Mol Cell 2004; 13:739-50.
110. Unal E, Arbel-Eden A, Sattler U, Shoroff R, Lichten M, Haer JE, Koshland D. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 2004; 16:991-1002.
111. Strom L, Lindroos HB, Shirahige K, Sjogren C. Postreplicative recruitment of cohesion to double-strand breaks is required for DNA repair. Mol Cell 2004; 16:1003-15.
112. Wolner B, Peterson CL. ATP-dependent and ATP-independent roles for the Rad54 chromatin remodeling enzyme during recombinational repair of a DNA double-strand break. J Biol Chem 2005; 280:10855-60.
113. Thoma NH, Czyzewski BK, Alexeev AA, Mazin AV, Kowalczykowski SC, Pavletich NP. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nat Struct Mol Biol 2005; 12:350-6.
114. Alexeev A, Mazin A, Kowalczykowski SC. Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat Struct Biol 2003; 10:182-6.
115. Shina M, Peterson CL. A Rad51 presynaptic filament is sufficient to capture nucleosomal homology during recombinational repair of a DNA double-strand break. Mol Cell 2008; 30:803-10.
116. Solinger JA, Kiianitsa K, Heyer WF. Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol Cell 2002; 10:1175-88.
117. Kwon Y, Seong C, Chi P, Greene EC, Klein H, Sung P. ATP-dependent chromatin remodelling by the Saccharomyces cerevisiae homologous recombination factor Rdh54. J Biol Chem 2008; 283:10445-52.
118. Hara R, Sancar A. The SWI/SNF chromatin-remodeling factor stimulates repair by human excision nuclease in the mononucleosome core particle. Mol Cell Biol 2002; 22:6779-87.
119. Gaillard H, et al. Chromatin remodelling activities act on UV-damaged nucleosomes and modulate DNA damage accessibility to photolyase. J Biol Chem 2003; 278:17655-63.
120. Yu Y, Teng Y, Liu H, Reed SH, Waters R. UV irradiation stimulates histone acetylation and chromatin remodelling at a repressed yeast locus. Proc Natl Acad Sci USA 2005; 102:8650-5.
121. Teng Y, Yu Y, Ferreiro JA, Waters R. Histone acetylation, chromatin remodeling, transcription and nucleotide excision repair in S. cerevisiae: studies with two model genes. DNA Repair 2005; 4:870-83.
122. Gong F, Fahy D, Smerdon MJ. Rad4-Rad23 interaction with SWI/SNF link is ATP-dependent chromatin remodelling with nucleotide excision repair. Nat Struct Mol Biol 2006; 13:902-7.
123. Gong F, Fahy D, Liu H, Wang W, Smerdon MJ. Role of the mammalian SWI/SNF chromatin remodelling complex in the cellular response to UV damage. Cell Cycle 2008; 7:1067-74.
124. Déry U, Masson J-Y. Twists and turns in the function of DNA damage signalling and repair proteins by post-translational modifications. DNA Repair 2007; 6:561-77.
125. Heo K, et al. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell 2008; 30:86-97.
126. Chowdhury AK, et al. Gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol Cell 2005; 20:801-9.
127. Nakada S, Chen GI, Gingras A-C, Durocher D. PP4 is a γH2AX phosphatase required for recovery from the DNA damage checkpoint. EMBO Rep 2008; 9:1019-26.
128. Utley RT, Lacoste N, Jobin-Robitaille O, Allard S, Côté J. Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol Cell Biol 2005; 25:8179-90.
129. Bhaskara S, et al. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 2008; 30:61-72.
130. Downs JA, Nussenzweig MC, Nussenzweig A. Chromatin dynamics and the preservation of genetic information. Nature 2007; 447:951-8.
131. Ayoub N, Jeyasekharan AD, Bernal JA, Venkitaraman AR. HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature 2008; 453:682-6.
132. Lukas J, Bartek J. DNA damage: a histone-code mediator leaves the stage. Nat Struc Mol Biol 2008; 15:430-3.
133. Polo SE, Roche D, Almouzni G. New histone incorporation marks sites of UV repair in human cells. Cell 2006; 127:481-93.
134. Verreault A. De novo nucleosome assembly: new pieces in an old puzzle. Genes Dev 2000; 14:430-8.
135. Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT. Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev 2004; 18:170-83.
136. Linger JG, Tyler JK. Chromatin disassembly and reassembly during DNA repair. Mutat Res 2007; 618:52-64.
137. Nabatiyan A, Szuüts D, Krude T. Induction of CAF-1 expression in response to DNA strand breaks in quiescent human cells. Mol Cell Biol 2006; 26:1839-49.
138. Balajee AS, Geard CR. Chromatin-bound PCNA complex formation triggered by DNA damage occurs independent of the ATM gene product in human cells. Nucleic Acids Res 2001; 29:1341-51.
139. Pospiech H, Rytkonen AK, Syvaoja JE. The role of DNA polymerase activity in human non-homologous end joining. Nucleic Acids Res 2001; 29:3277-88.
140. Adkins MW, Tyler JK. The histone chaperone Asf1p mediates global chromatin disassembly in vivo. J Biol Chem 2004; 279:52069-74.
141. Schwabish MA, Struhl K. Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol Cell 2006; 22:415-22.
142. Mello JA, et al. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep 2002; 3:329-34.
143. Recht J, et al. Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc Natl Acad Sci USA 2006; 103:6988-93.
144. Chen C-C, et al. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 2008; 134:231-43.
145. Mortusewicz O, Leonhardt H, Cardoso MC. Spatiotemporal dynamics of regulatory protein recruitment at DNA damage sites. J Cell Biochem 2008; 104:562-9.