Acetylated Lysine 56 on Histone H3 Drives Chromatin Assembly after Repair and Signals for the Completion of Repair

Cell

Volumn 134, Issue 2, 2008, Pages 231-243

  Chen, Chin Chuan ^a   Carson, Joshua J ^a   Feser, Jason ^a   Tamburini, Beth ^a   Zabaronick, Susan ^a   Linger, Jeffrey ^a   Tyler, Jessica K ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

CELLBIO; CELLCYCLE; SIGNALING

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; HISTONE CHAPERONE ASF1; HISTONE H3; LYSINE;

ACETYLATION; ARTICLE; CELL CYCLE PROGRESSION; CELL DEATH; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; PRIORITY JOURNAL;

EID: 47549105301     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.06.035     Document Type: Article

References (56)

1. Adkins M.W., Howar S.R., and Tyler J.K. Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol. Cell 14 (2004) 657-666
2. Adkins M.W., Carson J.J., English C.M., Ramey C.J., and Tyler J.K. The histone chaperone anti-silencing function 1 stimulates the acetylation of newly synthesized histone H3 in S-phase. J. Biol. Chem. 282 (2007) 1334-1340
3. Aguilera A., and Gomez-Gonzalez B. Genome instability: a mechanistic view of its causes and consequences. Nat. Rev. Genet. 9 (2008) 204-217
4. Altaf M., Saksouk N., and Cote J. Histone modifications in response to DNA damage. Mutat. Res. 618 (2007) 81-90
5. Bakkenist C.J., and Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 (2003) 499-506
6. Bartek J., and Lukas J. DNA damage checkpoints: from initiation to recovery or adaptation. Curr. Opin. Cell Biol. 19 (2007) 238-245
7. Celic I., Masumoto H., Griffith W.P., Meluh P., Cotter R.J., Boeke J.D., and Verreault A. The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr. Biol. 16 (2006) 1280-1289
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. Driscoll R., Hudson A., and Jackson S.P. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315 (2007) 649-652
10. Dubrana K., van Attikum H., Hediger F., and Gasser S.M. The processing of double-strand breaks and binding of single-strand-binding proteins RPA and Rad51 modulate the formation of ATR-kinase foci in yeast. J. Cell Sci. 120 (2007) 4209-4220
11. Dudasova Z., Dudas A., and Chovanec M. Non-homologous end-joining factors of Saccharomyces cerevisiae. FEMS Microbiol. Rev. 28 (2004) 581-601
12. Emili A., Schieltz D.M., Yates III J.R., and Hartwell L.H. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol. Cell 7 (2001) 13-20
13. Gilbert C.S., Green C.M., and Lowndes N.F. Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol. Cell 8 (2001) 129-136
14. Groth A., Rocha W., Verreault A., and Almouzni G. Chromatin challenges during DNA replication and repair. Cell 128 (2007) 721-733
15. Han J., Zhou H., Horazdovsky B., Zhang K., Xu R.M., and Zhang Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315 (2007) 653-655
16. Hu F., Alcasabas A.A., and Elledge S.J. Asf1 links Rad53 to control of chromatin assembly. Genes Dev. 15 (2001) 1061-1066
17. 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
18. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., Ellenberger T., and Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423 (2003) 305-309
19. Krejci L., Macris M., Li Y., Van Komen S., Villemain J., Ellenberger T., Klein H., and Sung P. Role of ATP hydrolysis in the antirecombinase function of Saccharomyces cerevisiae Srs2 protein. J. Biol. Chem. 279 (2004) 23193-23199
20. Le S., Davis C., Konopka J.B., and Sternglanz R. Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast 13 (1997) 1029-1042
21. Lee S.E., Moore J.K., Holmes A., Umezu K., Kolodner R.D., and Haber J.E. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94 (1998) 399-409
22. Leroy C., Lee S.E., Vaze M.B., Ochsenbien F., Guerois R., Haber J.E., and Marsolier-Kergoat M.C. PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol. Cell 11 (2003) 827-835
23. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 (1997) 251-260
24. Lupardus P.J., and Cimprich K.A. Checkpoint adaptation; molecular mechanisms uncovered. Cell 117 (2004) 555-556
25. Maas N.L., Miller K.M., DeFazio L.G., and Toczyski D.P. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol. Cell 23 (2006) 109-119
26. 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
27. Mello J.A., Sillje H.H., Roche D.M., Kirschner D.B., Nigg E.A., and Almouzni G. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3 (2002) 329-334
28. Melo J., and Toczyski D. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14 (2002) 237-245
29. Myung K., Pennaneach V., Kats E.S., and Kolodner R.D. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc. Natl. Acad. Sci. USA 100 (2003) 6640-6645
30. O'Neill B.M., Szyjka S.J., Lis E.T., Bailey A.O., Yates III J.R., Aparicio O.M., and Romesberg F.E. Pph3-Psy2 is a phosphatase complex required for Rad53 dephosphorylation and replication fork restart during recovery from DNA damage. Proc. Natl. Acad. Sci. USA 104 (2007) 9290-9295
31. Osley M.A., Tsukuda T., and Nickoloff J.A. ATP-dependent chromatin remodeling factors and DNA damage repair. Mutat. Res. 618 (2007) 65-80
32. Pasero P., Shimada K., and Duncker B.P. Multiple roles of replication forks in S phase checkpoints: sensors, effectors and targets. Cell Cycle 2 (2003) 568-572
33. Pellicioli A., Lee S.E., Lucca C., Foiani M., and Haber J.E. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol. Cell 7 (2001) 293-300
34. Prado F., Cortes-Ledesma F., Huertas P., and Aguilera A. Mitotic recombination in Saccharomyces cerevisiae. Curr. Genet. 42 (2003) 185-198
35. Prado F., Cortes-Ledesma F., and Aguilera A. The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep. 5 (2004) 497-502
36. Qin J., and Li L. Molecular anatomy of the DNA damage and replication checkpoints. Radiat. Res. 159 (2003) 139-148
37. Ramey C.J., Howar S., Adkins M., Linger J., Spicer J., and Tyler J.K. Activation of the DNA damage checkpoint in yeast lacking the histone chaperone anti-silencing function 1. Mol. Cell. Biol. 24 (2004) 10313-10327
38. Recht J., Tsubota T., Tanny J.C., Diaz R.L., Berger J.M., Zhang X., Garcia B.A., Shabanowitz J., Burlingame A.L., Hunt D.F., 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 103 (2006) 6988-6993
39. 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
40. Schwabish M.A., and Struhl K. Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol. Cell 22 (2006) 415-422
41. Schwartz M.F., Lee S.J., Duong J.K., Eminaga S., and Stern D.F. FHA domain-mediated DNA checkpoint regulation of Rad53. Cell Cycle 2 (2003) 384-396
42. Shim E.Y., Hong S.J., Oum J.H., Yanez Y., Zhang Y., and Lee S.E. RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol. 27 (2007) 1602-1613
43. 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
44. 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
45. Thaminy S., Newcomb B., Kim J., Gatbonton T., Foss E., Simon J., and Bedalov A. HST3 is regulated by MEC1-dependent proteolysis and controls the S phase checkpoint and sister chromatid cohesion by deacetylating histone H3 at lysine 56. J. Biol. Chem. 282 (2007) 3705-3714
46. Tsubota T., Berndsen C.E., Erkmann J.A., Smith C.L., Yang L., Freitas M.A., Denu J.M., and Kaufman P.D. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol. Cell 25 (2007) 703-712
47. Tsubouchi H., and Ogawa H. A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol. Cell. Biol. 18 (1998) 260-268
48. 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
49. Tyler J.K., Adams C.R., Chen S.R., Kobayashi R., Kamakaka R.T., and Kadonaga J.T. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402 (1999) 555-560
50. 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
51. van Attikum H., Fritsch O., and Gasser S.M. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26 (2007) 4113-4125
52. van Vugt M.A., and Medema R.H. Checkpoint adaptation and recovery: back with Polo after the break. Cell Cycle 3 (2004) 1383-1386
53. van Vugt M.A., and Medema R.H. Getting in and out of mitosis with Polo-like kinase-1. Oncogene 24 (2005) 2844-2859
54. Vaze M.B., Pellicioli A., Lee S.E., Ira G., Liberi G., Arbel-Eden A., Foiani M., and Haber J.E. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol. Cell 10 (2002) 373-385
55. Williams R.S., Williams J.S., and Tainer J.A. Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem. Cell Biol. 85 (2007) 509-520
56. Zabaronick S.R., and Tyler J.K. The histone chaperone anti-silencing function 1 is a global regulator of transcription independent of passage through S phase. Mol. Cell. Biol. 25 (2005) 652-660