Histone H3K56 Acetylation, Rad52, and Non-DNA Repair Factors Control Double-Strand Break Repair Choice with the Sister Chromatid

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Muñoz Galván, Sandra ^a   Jimeno, Sonia ^a   Rothstein, Rodney ^b   Aguilera, Andrés ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE ADA2; HISTONE ACETYLTRANSFERASE AHC1; HISTONE ACETYLTRANSFERASE RTT109; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE H3; LYSINE; NON DNA REPAIR FACTOR; PROTEIN BUD27; PROTEIN PDR10; PROTEN WSS1; RAD52 PROTEIN; SUMO PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DEACETYLATION; DNA DETERMINATION; DNA REPAIR; DNA REPLICATION; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENETIC RECOMBINATION; GENOMIC INSTABILITY; HISTONE ACETYLATION; HOMOLOGOUS RECOMBINATION; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; PROTEIN TARGETING; RAD52 GENE; REGULATORY MECHANISM; SISTER CHROMATID;

ACETYLATION; CHROMATIDS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; GENOMIC INSTABILITY; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SISTER CHROMATID EXCHANGE; SUMO-1 PROTEIN; UBIQUITIN;

EID: 84873494530     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003237     Document Type: Article

References (49)

1. Kadyk LC, Hartwell LH, (1992) Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132: 387-402.
2. Johnson RD, Jasin M, (2000) Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J 19: 3398-3407.
3. Gonzalez-Barrera S, Cortes-Ledesma F, Wellinger RE, Aguilera A, (2003) Equal sister chromatid exchange is a major mechanism of double-strand break repair in yeast. Mol Cell 11: 1661-1671.
4. Cortes-Ledesma F, Aguilera A, (2006) Double-strand breaks arising by replication through a nick are repaired by cohesin-dependent sister-chromatid exchange. EMBO Rep 7: 919-926.
5. Gunjan A, Paik J, Verreault A, (2005) Regulation of histone synthesis and nucleosome assembly. Biochimie 87: 625-635.
6. Masumoto H, Hawke D, Kobayashi R, Verreault A, (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436: 294-298.
7. Maas NL, Miller KM, DeFazio LG, Toczyski DP, (2006) Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 23: 109-119.
8. Chen CC, Carson JJ, Feser J, Tamburini B, Zabaronick S, et al. (2008) Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134: 231-243.
9. Das C, Lucia MS, Hansen KC, Tyler JK, (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459: 113-117.
10. 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.
11. Yuan J, Pu M, Zhang Z, Lou Z, (2009) Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 8: 1747-1753.
12. Ozdemir A, Spicuglia S, Lasonder E, Vermeulen M, Campsteijn C, et al. (2005) Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J Biol Chem 280: 25949-25952.
13. Alvaro D, Lisby M, Rothstein R, (2007) Genome-wide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet 3: e228 doi:10.1371/journal.pgen.0030228.
14. Malone RE, Montelone BA, Edwards C, Carney K, Hoekstra MF, (1988) A reexamination of the role of the RAD52 gene in spontaneous mitotic recombination. Curr Genet 14: 211-223.
15. Lettier G, Feng Q, de Mayolo AA, Erdeniz N, Reid RJ, et al. (2006) The role of DNA double-strand breaks in spontaneous homologous recombination in S. cerevisiae. PLoS Genet 2: e194 doi:10.1371/journal.pgen.0030194.
16. Mullen JR, Chen CF, Brill SJ, (2010) Wss1 is a SUMO-dependent isopeptidase that interacts genetically with the Slx5-Slx8 SUMO-targeted ubiquitin ligase. Mol Cell Biol 30: 3737-3748.
17. Eberharter A, Sterner DE, Schieltz D, Hassan A, Yates JR 3rd, et al. (1999) The ADA complex is a distinct histone acetyltransferase complex in Saccharomyces cerevisiae. Mol Cell Biol 19: 6621-6631.
18. Cortes-Ledesma F, Tous C, Aguilera A, (2007) Different genetic requirements for repair of replication-born double-strand breaks by sister-chromatid recombination and break-induced replication. Nucleic Acids Res 35: 6560-6570.
19. Deplazes A, Mockli N, Luke B, Auerbach D, Peter M, (2009) Yeast Uri1p promotes translation initiation and may provide a link to cotranslational quality control. EMBO J 28: 1429-1441.
20. Rockwell NC, Wolfger H, Kuchler K, Thorner J, (2009) ABC transporter Pdr10 regulates the membrane microenvironment of Pdr12 in Saccharomyces cerevisiae. J Membr Biol 229: 27-52.
21. Horiuchi J, Silverman N, Marcus GA, Guarente L, (1995) ADA3, a putative transcriptional adaptor, consists of two separable domains and interacts with ADA2 and GCN5 in a trimeric complex. Mol Cell Biol 15: 1203-1209.
22. Xu F, Zhang K, Grunstein M, (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121: 375-385.
23. Fasullo MT, Davis RW, (1987) Recombinational substrates designed to study recombination between unique and repetitive sequences in vivo. Proc Natl Acad Sci U S A 84: 6215-6219.
24. Celic I, Verreault A, Boeke JD, (2008) Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics 179: 1769-1784.
25. Moriel-Carretero M, Aguilera A, (2010a) A postincision-deficient TFIIH causes replication fork breakage and uncovers alternative Rad51- or Pol32-mediated restart mechanisms. Mol Cell 37: 690-701.
26. Lydeard JR, Jain S, Yamaguchi M, Haber JE, (2007) Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448: 820-823.
27. Torres-Rosell J, Sunjevaric I, De Piccoli G, Sacher M, Eckert-Boulet N, et al. (2007) The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat Cell Biol 9: 923-931.
28. Palancade B, Doye V, (2008) Sumoylating and desumoylating enzymes at nuclear pores: underpinning their unexpected duties? Trends Cell Biol 18: 174-183.
29. Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller KM, et al. (2009) Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462: 935-939.
30. 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.
31. De Piccoli G, Cortes-Ledesma F, Ira G, Torres-Rosell J, Uhle S, et al. (2006) Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat Cell Biol 8: 1032-1034.
32. Potts PR, Porteus MH, Yu H, (2006) Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J 25: 3377-3388.
33. Sacher M, Pfander B, Hoege C, Jentsch S, (2006) Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat Cell Biol 8: 1284-1290.
34. Altmannova V, Eckert-Boulet N, Arneric M, Kolesar P, Chaloupkova R, et al. Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res 38: 4708-4721.
35. Suganuma T, Workman JL, Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80: 473-499.
36. Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, et al. (2006) 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 U S A 103: 6988-6993.
37. Garcia BA, Hake SB, Diaz RL, Kauer M, Morris SA, et al. (2007) Organismal differences in post-translational modifications in histones H3 and H4. J Biol Chem 282: 7641-7655.
38. Wurtele H, Kaiser GS, Bacal J, St-Hilaire E, Lee EH, et al. (2012) Histone H3 lysine 56 acetylation and the response to DNA replication fork damage. Mol Cell Biol 32: 154-72.
39. Aguilera A, Gomez-Gonzalez B, (2008) Genome instability: a mechanistic view of its causes and consequences. Nat Rev Genet 9: 204-217.
40. Prado F, Cortes-Ledesma F, Aguilera A, (2004) The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep 5: 497-502.
41. Emili A, Schieltz DM, Yates JR 3rd, Hartwell LH, (2001) Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol Cell 7: 13-20.
42. Driscoll R, Hudson A, Jackson SP, (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649-652.
43. Yang B, Miller A, Kirchmaier AL, (2008) HST3/HST4-dependent deacetylation of lysine 56 of histone H3 in silent chromatin. Mol Biol Cell 19: 4993-5005.
44. de Mayolo AA, Sunjevaric I, Reid R, Mortensen UH, Rothstein R, et al. The rad52-Y66A allele alters the choice of donor template during spontaneous chromosomal recombination. DNA Repair (Amst) 9: 23-32.
45. Moriel-Carretero M, Aguilera A, (2010b) Replication fork breakage and re-start: New insights into Rad3/XPD-associated deficiencies. Cell Cycle 9: 2958-2962.
46. Gonzalez-Barrera S, Garcia-Rubio M, Aguilera A, (2002) Transcription and double-strand breaks induce similar mitotic recombination events in Saccharomyces cerevisiae. Genetics 162: 603-614.
47. Lisby M, Rothstein R, Mortensen UH, (2001) Rad52 forms DNA repair and recombination centers during S phase. Proc Natl Acad Sci U S A 98: 8276-8282.
48. Garcia-Rubio M, Huertas P, Gonzalez-Barrera S, Aguilera A, (2003) Recombinogenic effects of DNA-damaging agents are synergistically increased by transcription in Saccharomyces cerevisiae. New insights into transcription-associated recombination. Genetics 165: 457-466.
49. Lisby M, Mortensen UH, Rothstein R, (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 5: 572-577.