Histone modifications in response to DNA damage

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 618, Issue 1-2, 2007, Pages 81-90

  Altaf, Mohammed ^a   Saksouk, Nehmé ^a   Côté, Jacques ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

H2AX; H2AZ; Ino80; NuA4; Swr1; Tip60

Indexed keywords

DOUBLE STRANDED DNA; HISTONE;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA REPAIR; GENOME; HUMAN; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION;

ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMES; DNA DAMAGE; DNA PACKAGING; DNA REPAIR; DNA REPLICATION; HISTONES; HUMANS; MODELS, MOLECULAR; NUCLEOSOMES; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 34247172850     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2006.09.009     Document Type: Article

References (86)

1. Peterson C.L., and Laniel M.A. Histones and histone modifications. Curr. Biol. 14 (2004) R546-R551
2. Yap K.L., and Zhou M.M. Structure and function of protein modules in chromatin biology. Results Probl. Cell Differ. 41 (2006) 1-23
3. Vaquero A., Loyola A., and Reinberg D. The constantly changing face of chromatin. Sci. Aging Knowl. Environ. 2003 (2003) RE4
4. Peterson C.L., and Côté J. Cellular machineries for chromosomal DNA repair. Genes Dev. 18 (2004) 602-616
5. Thiriet C., and Hayes J.J. Chromatin in need of a fix: phosphorylation of H2AX connects chromatin to DNA repair. Mol. Cell 18 (2005) 617-622
6. van Attikum H., and Gasser S.M. The histone code at DNA breaks: a guide to repair?. Nat. Rev. Mol. Cell Biol. 6 (2005) 757-765
7. Stiff T., O'Driscoll M., Rief N., Iwabuchi K., Lobrich M., and Jeggo P.A. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64 (2004) 2390-2396
8. Downs J.A., Lowndes N.F., and Jackson S.P. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408 (2000) 1001-1004
9. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273 (1998) 5858-5868
10. Rogakou E.P., Boon C., Redon C., and Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146 (1999) 905-916
11. Downs J.A., Allard S., Jobin-Robitaille O., Javaheri A., Auger A., Bouchard N., Kron S.J., Jackson S.P., and Côté J. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16 (2004) 979-990
12. Shroff R., Arbel-Eden A., Pilch D., Ira G., Bonner W.M., Petrini J.H., Haber J.E., and Lichten M. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14 (2004) 1703-1711
13. Wolner B., van Komen S., Sung P., and Peterson C.L. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12 (2003) 221-232
14. Martin S.G., Laroche T., Suka N., Grunstein M., and Gasser S.M. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell 97 (1999) 621-633
15. Lukas C., Melander F., Stucki M., Falck J., Bekker-Jensen S., Goldberg M., Lerenthal Y., Jackson S.P., Bartek J., and Lukas J. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23 (2004) 2674-2683
16. Stucki M., and Jackson S.P. GammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Rep. (Amst.) 5 (2006) 534-543
17. Wyatt H.R., Liaw H., Green G.R., and Lustig A.J. Multiple roles for Saccharomyces cerevisiae histone H2A in telomere position effect, Spt phenotypes and double-strand-break repair. Genetics 164 (2003) 47-64
18. Harvey A.C., Jackson S.P., and Downs J.A. Saccharomyces cerevisiae histone H2A Ser122 facilitates DNA repair. Genetics 170 (2005) 543-553
19. Celeste A., Petersen S., Romanienko P.J., Fernandez-Capetillo O., Chen H.T., Sedelnikova O.A., Reina-San-Martin B., Coppola V., Meffre E., Difilippantonio 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. Genomic instability in mice lacking histone H2AX. Science 296 (2002) 922-927
20. 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. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 8173-8178
21. Nakamura T.M., Du L.L., Redon C., and Russell P. Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol. Cell Biol. 24 (2004) 6215-6230
22. Kobayashi J., Tauchi H., Sakamoto S., Nakamura A., Morishima K., Matsuura S., Kobayashi T., Tamai K., Tanimoto K., and Komatsu K. NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12 (2002) 1846-1851
23. 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. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5 (2003) 675-679
24. Xie A., Puget N., Shim I., Odate S., Jarzyna I., Bassing C.H., Alt F.W., and Scully R. Control of sister chromatid recombination by histone H2AX. Mol. Cell 16 (2004) 1017-1025
25. Franco S., Gostissa M., Zha S., Lombard D.B., Murphy M.M., Zarrin A.A., Yan C., Tepsuporn S., Morales J.C., Adams M.M., Lou Z., Bassing C.H., Manis J.P., Chen J., Carpenter P.B., and Alt F.W. H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Mol. Cell 21 (2006) 201-214
26. Sweeney F.D., Yang F., Chi A., Shabanowitz J., Hunt D.F., and Durocher D. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr. Biol. 15 (2005) 1364-1375
27. Ward I.M., Minn K., Jorda K.G., and Chen J. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278 (2003) 19579-19582
28. Javaheri A., Wysocki R., Jobin-Robitaille O., Altaf M., Côté J., and Kron S.J. Yeast G1 DNA damage checkpoint regulation by H2A phosphorylation is independent of chromatin remodeling. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13771-13776
29. Toh G.W., O'Shaughnessy A.M., Jimeno S., Dobbie I.M., Grenon M., Maffini S., O'Rorke A., and Lowndes N.F. Histone H2A phosphorylation and H3 methylation are required for a novel Rad9 DSB repair function following checkpoint activation. DNA Rep. (Amst.) 5 (2006) 693-703
30. Strom L., Lindroos H.B., Shirahige K., and Sjogren C. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell 16 (2004) 1003-1015
31. Unal E., Arbel-Eden A., Sattler U., Shroff R., Lichten M., Haber J.E., and Koshland D. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16 (2004) 991-1002
32. Fernandez-Capetillo O., Allis C.D., and Nussenzweig A. Phosphorylation of histone H2B at DNA double-strand breaks. J. Exp. Med. 199 (2004) 1671-1677
33. 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. Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell 113 (2003) 507-517
34. Ahn S.H., Cheung W.L., Hsu J.Y., Diaz R.L., Smith M.M., and Allis C.D. Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae. Cell 120 (2005) 25-36
35. 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. Phosphorylation of histone H4 serine 1 during DNA damage requires casein kinase II in S. cerevisiae. Curr. Biol. 15 (2005) 656-660
36. Utley R.T., Lacoste N., Jobin-Robitaille O., Allard S., and Côté J. Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol. Cell Biol. 25 (2005) 8179-8190
37. Downs J.A., Kosmidou E., Morgan A., and Jackson S.P. Suppression of homologous recombination by the Saccharomyces cerevisiae linker histone. Mol. Cell 11 (2003) 1685-1692
38. Kysela B., Chovanec M., and Jeggo P.A. Phosphorylation of linker histones by DNA-dependent protein kinase is required for DNA ligase IV-dependent ligation in the presence of histone H1. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 1877-1882
39. Morrison A.J., Highland J., Krogan N.J., Arbel-Eden A., Greenblatt J.F., Haber J.E., and Shen X. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119 (2004) 767-775
40. van Attikum H., Fritsch O., Hohn B., and Gasser S.M. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119 (2004) 777-788
41. Doyon Y., and Côté J. The highly conserved and multifunctional NuA4 HAT complex. Curr. Opin. Genet. Dev. 14 (2004) 147-154
42. 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. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419 (2002) 411-415
43. Cairns B.R. Around the world of DNA damage INO80 days. Cell 119 (2004) 733-735
44. Tsukuda T., Fleming A.B., Nickoloff J.A., and Osley M.A. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438 (2005) 379-383
45. van Attikum H., and Gasser S.M. ATP-dependent chromatin remodeling and DNA double-strand break repair. Cell Cycle 4 (2005) 1011-1014
46. Fritsch O., Benvenuto G., Bowler C., Molinier J., and Hohn B. The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol. Cell 16 (2004) 479-485
47. Jin J., Cai Y., Yao T., Gottschalk A.J., Florens L., Swanson S.K., Gutierrez J.L., Coleman M.K., Workman J.L., Mushegian A., Washburn M.P., Conaway R.C., and Conaway J.W. A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J. Biol. Chem. 280 (2005) 41207-41212
48. Muller B., and West S.C. Processing of Holliday junctions by the Escherichia coli RuvA, RuvB, RuvC and RecG proteins. Experientia 50 (1994) 216-222
49. Mizuguchi G., Shen X., Landry J., Wu W.H., Sen S., and Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303 (2004) 343-348
50. Krogan N.J., Keogh M.C., Datta N., Sawa C., Ryan O.W., Ding H., Haw R.A., Pootoolal J., Tong A., Canadien V., Richards D.P., Wu X., Emili A., Hughes T.R., Buratowski S., and Greenblatt J.F. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell 12 (2003) 1565-1576
51. Kobor M.S., Venkatasubrahmanyam S., Meneghini M.D., Gin J.W., Jennings J.L., Link A.J., Madhani H.D., and Rine J. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2 (2004) E131
52. Murr R., Loizou J.I., Yang Y.G., Cuenin C., Li H., Wang Z.Q., and Herceg Z. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 8 (2006) 91-99
53. Squatrito M., Gorrini C., and Amati B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol. (2006)
54. Sun Y., Jiang X., Chen S., Fernandes N., and Price B.D. 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
55. Kusch T., Florens L., Macdonald W.H., Swanson S.K., Glaser R.L., Yates III J.R., Abmayr S.M., Washburn M.P., and Workman J.L. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306 (2004) 2084-2087
56. Keogh M.C., Mennella T.A., Sawa C., Berthelet S., Krogan N.J., Wolek A., Podolny V., Carpenter L.R., Greenblatt J.F., Baetz K., and Buratowski S. The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4. Genes Dev. 20 (2006) 660-665
57. Krogan N.J., Baetz K., Keogh M.C., Datta N., Sawa C., Kwok T.C., Thompson N.J., Davey M.G., Pootoolal J., Hughes T.R., Emili A., Buratowski S., Hieter P., and Greenblatt J.F. Regulation of chromosome stability by the histone H2A variant Htz1, the Swr1 chromatin remodeling complex, and the histone acetyltransferase NuA4. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13513-13518
58. Millar C.B., Xu F., Zhang K., and Grunstein M. Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev. 20 (2006) 711-722
59. Zhang H., Richardson D.O., Roberts D.N., Utley R., Erdjument-Bromage H., Tempst P., Côté J., and Cairns B.R. The Yaf9 component of the SWR1 and NuA4 complexes is required for proper gene expression, histone H4 acetylation, and Htz1 replacement near telomeres. Mol. Cell Biol. 24 (2004) 9424-9436
60. Zhang H., Roberts D.N., and Cairns B.R. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123 (2005) 219-231
61. Raisner R.M., Hartley P.D., Meneghini M.D., Bao M.Z., Liu C.L., Schreiber S.L., Rando O.J., and Madhani H.D. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123 (2005) 233-248
62. Papamichos-Chronakis M., Krebs J.E., and Peterson C.L. Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev. 20 (2006) 2437-2449
63. 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. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439 (2006) 497-501
64. Chowdhury D., Keogh M.C., Ishii H., Peterson C.L., Buratowski S., and Lieberman J. Gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20 (2005) 801-809
65. Downs J.A., and Côté J. Dynamics of chromatin during the repair of DNA double-strand breaks. Cell Cycle 4 (2005) 1373-1376
66. Tamburini B.A., and Tyler J.K. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell Biol. 25 (2005) 4903-4913
67. Jazayeri A., McAinsh A.D., and Jackson S.P. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 1644-1649
68. Martin C., and Zhang Y. The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6 (2005) 838-849
69. Huyen Y., Zgheib O., Ditullio Jr. R.A., Gorgoulis V.G., Zacharatos P., Petty T.J., Sheston E.A., Mellert H.S., Stavridi E.S., and Halazonetis T.D. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432 (2004) 406-411
70. Wysocki R., Javaheri A., Allard S., Sha F., Côté J., and Kron S.J. Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell Biol. 25 (2005) 8430-8443
71. Giannattasio M., Lazzaro F., Plevani P., and Muzi-Falconi M. The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J. Biol. Chem. 280 (2005) 9879-9886
72. Ng H.H., Xu R.M., Zhang Y., and Struhl K. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J. Biol. Chem. 277 (2002) 34655-34657
73. Wood A., Schneider J., Dover J., Johnston M., and Shilatifard A. The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J. Biol. Chem. 278 (2003) 34739-34742
74. Sanders S.L., Portoso M., Mata J., Bahler J., Allshire R.C., and Kouzarides T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119 (2004) 603-614
75. Kao G.D., McKenna W.G., Guenther M.G., Muschel R.J., Lazar M.A., and Yen T.J. Histone deacetylase 4 interacts with 53BP1 to mediate the DNA damage response. J. Cell. Biol. 160 (2003) 1017-1027
76. Qin S., and Parthun M.R. Recruitment of the type B histone acetyltransferase hat1p to chromatin is linked to DNA double-strand breaks. Mol. Cell Biol. 26 (2006) 3649-3658
77. Choy J.S., and Kron S.J. NuA4 subunit Yng2 function in intra-S-phase DNA damage response. Mol. Cell Biol. 22 (2002) 8215-8225
78. Qin S., and Parthun M.R. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol. Cell Biol. 22 (2002) 8353-8365
79. 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. Involvement of human MOF in ATM function. Mol. Cell Biol. 25 (2005) 5292-5305
80. Taipale M., Rea S., Richter K., Vilar A., Lichter P., Imhof A., and Akhtar A. hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells. Mol. Cell Biol. 25 (2005) 6798-6810
81. Smith E.R., Cayrou C., Huang R., Lane W.S., Côté J., and Lucchesi J.C. 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 (2005) 9175-9188
82. Masumoto H., Hawke D., Kobayashi R., and Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436 (2005) 294-298
83. Xu F., Zhang K., and Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121 (2005) 375-385
84. Chai B., Huang J., Cairns B.R., and Laurent B.C. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19 (2005) 1656-1661
85. Shim E.Y., Ma J.L., Oum J.H., Yanez Y., and Lee S.E. The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell Biol. 25 (2005) 3934-3944
86. Park J.H., Park E.J., Lee H.S., Kim S.J., Hur S.K., Imbalzano A.N., and Kwon J. Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting gamma-H2AX induction. EMBO J. 25 (2006) 3986-3997