The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation

Molecular and Cellular Biology

Volumn 32, Issue 22, 2012, Pages 4727-4740

  Eapen, Vinay V ^a   Sugawara, Neal ^a   Tsabar, Michael ^a   Wu, Wei Hua ^b   Haber, James E ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2A; HISTONE H2AX; PROTEIN FUN30; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE CHECKPOINT; DOUBLE STRANDED DNA BREAK; HISTONE PHOSPHORYLATION; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ADAPTATION, PHYSIOLOGICAL; CELL CYCLE CHECKPOINTS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA BREAKS, DOUBLE-STRANDED; DNA, FUNGAL; EXODEOXYRIBONUCLEASES; HISTONES; HOMOLOGOUS RECOMBINATION; NUCLEOSOMES; PHOSPHORYLATION; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 84868694661     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00566-12     Document Type: Article

References (72)

1. Awad S, Ryan D, Prochasson P, Owen-Hughes T, Hassan AH. 2010. The Snf2 homolog Fun30 acts as a homodimeric ATP-dependent chromatinremodeling enzyme. J. Biol. Chem. 285:9477-9484.
2. Aylon Y, Kupiec M. 2005. Cell cycle-dependent regulation of doublestrand break repair: a role for the CDK. Cell Cycle 4:259-261.
3. Bassing CH, et al. 2002. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. U. S. A. 99:8173-8178.
4. Bitterman KJ, Anderson RM, Cohen HY, Latorre-Esteves M, Sinclair DA. 2002. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J. Biol. Chem. 277:45099-45107.
5. Costelloe T, et al. 2012. The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489:581-584.
6. Chai B, Huang J, Cairns BR, Laurent BC. 2005. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA doublestrand break repair. Genes Dev. 19:1656-1661.
7. Chen SH, Albuquerque CP, Liang J, Suhandynata RT, Zhou H. 2010. A proteome-wide analysis of kinase-substrate network in the DNA damage response. J. Biol. Chem. 285:12803-12812.
8. Chen X, et al. 2012. The Fun30 nucleosome remodeler promotes resection of DNA double-strand break ends. Nature 489:576-580.
9. Chen X, et al. 2011. Cell cycle regulation ofDNAdouble-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat. Struct. Mol. Biol. 18:1015-1019.
10. Chi P, et al. 2011. Analyses of the yeast Rad51 recombinase A265V mutant reveal different in vivo roles of Swi2-like factors. Nucleic Acids Res. 39:6511-6522.
11. Chung WH, Zhu Z, Papusha A, Malkova A, Ira G. 2010. Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet. 6:e1000948. doi:10.1371/ journal.pgen.1000948.
12. Clerici M, Mantiero D, Lucchini G, Longhese MP. 2006. The Saccharomyces cerevisiae Sae2 protein negatively regulates DNA damage checkpoint signalling. EMBO Rep. 7:212-218.
13. Clerici M, Mantiero D, Lucchini G, Longhese MP. 2005. The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J. Biol. Chem. 280:38631-38638.
14. Costanzo M, Baryshnikova A, Myers CL, Andrews B, Boone C. 2011. Charting the genetic interaction map of a cell. Curr. Opin. Biotechnol. 22:66-74.
15. Daley JM, Palmbos PL, Wu D, Wilson TE. 2005. Nonhomologous end joining in yeast. Annu. Rev. Genet. 39:431-451.
16. Daley JM, Wilson TE. 2005. Rejoining of DNA double-strand breaks as a function of overhang length. Mol. Cell. Biol. 25:896-906.
17. Dotiwala F, Haase J, Arbel-Eden A, Bloom K, Haber JE. 2007. The yeast DNAdamage checkpoint proteins control a cytoplasmic response toDNA damage. Proc. Natl. Acad. Sci. U. S. A. 104:11358-11363.
18. Dotiwala F, Harrison JC, Jain S, Sugawara N, Haber JE. 2010. Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromere-dependent mechanism. Curr. Biol. 20:328-332.
19. Durand-Dubief M, et al. 2012. SWI/SNF-like chromatin remodeling factor Fun30 supports point centromere function in S. cerevisiae. PLoS Genet. 8:e1002974. doi:10.1371/journal.pgen.1002974.
20. Fernandez-Capetillo O, et al. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:993-997.
21. Fishman-Lobell J, Rudin N, Haber JE. 1992. Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol. Cell. Biol. 12:1292-1303.
22. Gravel S, Chapman JR, Magill C, Jackson SP. 2008. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22: 2767-2772.
23. Guillemain G, et al. 2007. Mechanisms of checkpoint kinase Rad53 inactivation after a double-strand break in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:3378-3389.
24. Harrison JC, Haber JE. 2006. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40:209-235.
25. Hicks WM, Yamaguchi M, Haber JE. 2011. Real-time analysis of doublestrand DNA break repair by homologous recombination. Proc. Natl. Acad. Sci. U. S. A. 108:3108-3115.
26. Ira G, et al. 2004. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431:1011-1017.
27. Jain S, et al. 2009. A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA doublestrand break repair. Genes Dev. 23:291-303.
28. Jazayeri A, Balestrini A, Garner E, Haber JE, Costanzo V. 2008. Mre11-Rad50-Nbs1-dependent processing of DNA breaks generates oligonucleotides that stimulate ATM activity. EMBO J. 27:1953-1962.
29. Keogh MC, et al. 2006. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439: 497-501.
30. Kim JA, Haber JE. 2009. Chromatin assembly factors Asf1 and CAF-1 have overlapping roles in deactivating the DNA damage checkpoint when DNA repair is complete. Proc. Natl. Acad. Sci. U. S. A. 106:1151-1156.
31. Kim JA, Kruhlak M, Dotiwala F, Nussenzweig A, Haber JE. 2007. Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals. J. Cell Biol. 178:209-218.
32. Kramer KM, Brock JA, Bloom K, Moore JK, Haber JE. 1994. Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol. Cell. Biol. 14:1293-1301.
33. Lee JH, Paull TT. 2004. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304:93-96.
34. Lee K, Lee SE. 2007. Saccharomyces cerevisiae Sae2-and Tel1-dependent single-strand DNA formation at DNA break promotes microhomologymediated end joining. Genetics 176:2003-2014.
35. Lee SE, Bressan DA, Petrini JH, Haber JE. 2002. Complementation between N-terminal Saccharomyces cerevisiae mre11 alleles in DNA repair and telomere length maintenance. DNA Repair (Amst.) 1:27-40.
36. Lee SE, et al. 1998. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94:399-409.
37. Lee SE, Pellicioli A, Malkova A, Foiani M, Haber JE. 2001. The Saccharomyces recombination protein Tid1p is required for adaptation from G2/M arrest induced by a double-strand break. Curr. Biol. 11:1053-1057.
38. Leroy C, et al. 2003. PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol. Cell 11: 827-835.
39. Lydeard JR, Jain S, Yamaguchi M, Haber JE. 2007. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448:820-823.
40. Lydeard JR, Lipkin-Moore Z, Jain S, Eapen VV, Haber JE. 2010. Sgs1 and exo1 redundantly inhibit break-induced replication and de novo telomere addition at broken chromosome ends. PLoS Genet. 6:e1000973. doi: 10.1371/journal.pgen.1000973.
41. Lydeard JR, et al. 2010. Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes Dev. 24:1133-1144.
42. Ma JL, Kim EM, Haber JE, Lee SE. 2003. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 23:8820-8828.
43. Majka J, Burgers PM. 2007. Clamping the Mec1/ATR checkpoint kinase into action. Cell Cycle 6:1157-1160.
44. Majka J, Burgers PM. 2003. Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc. Natl. Acad. Sci. U. S. A. 100:2249-2254.
45. Makovets S, Blackburn EH. 2009. DNA damage signalling prevents deleterious telomere addition at DNA breaks. Nat. Cell Biol. 11:1383-1386.
46. Matsuoka S, et al. 2007. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316:1160-1166.
47. Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770-774.
48. Mizuguchi G, et al. 2004. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:343-348.
49. Moore JK, Haber JE. 1996. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2164-2173.
50. Myung K, Pennaneach V, Kats ES, Kolodner RD. 2003. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc. Natl. Acad. Sci. U. S. A. 100:6640-6645.
51. Neves-Costa A, Will WR, Vetter AT, Miller JR, Varga-Weisz P. 2009. The SNF2-family member Fun30 promotes gene silencing in heterochromatic loci. PLoS One 4:e8111. doi:10.1371/journal.pone.0008111.
52. Oum JH, et al. 2011. RSC facilitates Rad59-dependent homologous recombination between sister chromatids by promoting cohesin loading at DNA double-strand breaks. Mol. Cell. Biol. 31:3924-3937.
53. 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.
54. Pellicioli A, Lee SE, Lucca C, Foiani M, Haber JE. 2001. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol. Cell 7:293-300.
55. Rowbotham SP, et al. 2011. Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol. Cell 42:285-296.
56. Shim EY, Ma JL, Oum JH, Yanez Y, Lee SE. 2005. The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA doublestrand breaks. Mol. Cell. Biol. 25:3934-3944.
57. Shroff R, et al. 2004. Distribution and dynamics of chromatin modification induced by a definedDNAdouble-strand break. Curr. Biol. 14:1703-1711.
58. Stralfors A, Walfridsson J, Bhuiyan H, Ekwall K. 2011. The FUN30 chromatin remodeler, Fft3, protects centromeric and subtelomeric domains from euchromatin formation. PLoS Genet. 7:e1001334.
59. Strom L, Lindroos HB, Shirahige K, Sjogren C. 2004. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell 16:1003-1015.
60. Sugawara N, Wang X, Haber JE. 2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12:209-219.
61. Thompson JS, Johnson LM, Grunstein M. 1994. Specific repression of the yeast silent mating locusHMRby an adjacent telomere. Mol. Cell. Biol. 14:446-455.
62. Toczyski DP, Galgoczy DJ, Hartwell LH. 1997. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90:1097-1106.
63. Unal E, et al. 2004. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16:991-1002.
64. Usui T, Ogawa H, Petrini JH. 2001. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol. Cell 7:1255-1266.
65. Vaze M, et al. 2002. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires srs2 helicase. Mol. Cell 10:373.
66. Wach A, Brachat A, Pohlmann R, Philippsen P. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793-1808.
67. Wu WH, et al. 2005. Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat. Struct. Mol. Biol. 12:1064-1071.
68. Yeung M, Durocher D. 2011. Srs2 enables checkpoint recovery by promoting disassembly of DNA damage foci from chromatin. DNA Repair 10:1213-1222.
69. Yu Q, Zhang X, Bi X. 2011. Roles of chromatin remodeling factors in the formation and maintenance of heterochromatin structure. J. Biol. Chem. 286:14659-14669.
70. Yuan J, Adamski R, Chen J. 2010. Focus on histone variant H2AX: to be or not to be. FEBS Lett. 584:3717-3724.
71. Zhou J, Monson EK, Teng S, Schulz VP, Zakian VA. 2000. Pif1p helicase, a catalytic inhibitor of telomerase in yeast. Science 289:771-774.
72. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134: 981-994.