The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks

Molecular and Cellular Biology

Volumn 25, Issue 10, 2005, Pages 3934-3944

  Eun, Yong Shim ^a   Ma, Jia Lin ^a   Oum, Ji Hyun ^a   Yanez, Yvonne ^a   Sang, Eun Lee ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; ENDONUCLEASE; KU ANTIGEN; MRE11 PROTEIN; PROTEIN SUBUNIT;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CELL REGENERATION; CELL SURVIVAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPAIR; DNA STRAND BREAKAGE; FUNGAL GENE; GENE DELETION; GENE IDENTIFICATION; GENE INTERACTION; GENETIC SCREENING; GENOME; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; RSC 30 GENE; RSC 8 GENE; SACCHAROMYCES CEREVISIAE; YEAST CELL;

AMINO ACID SEQUENCE; CELL CYCLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; PHENOTYPE; PROTEIN BINDING; PROTEIN SUBUNITS; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 18144423533     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.10.3934-3944.2005     Document Type: Article

References (75)

1. Ai, X., and M. R. Parthun. 2004. The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol. Cell 14:195-205.
2. Alexiadis, V., and J. T. Kadonaga. 2002. Strand pairing by Rad54 and Rad51 is enhanced by chromatin. Genes Dev. 16:2767-2771.
3. Angus-Hill, M. L., A. Schlichter, D. Roberts, H. Erdjument-Bromage, P. Tempst, and B. R. Cairns. 2001. A Rsc3/Rsc30 zinc cluster dimer reveals novel roles for the chromatin remodeler RSC in gene expression and cell cycle control. Mol. Cell 7:741-751.
4. Askree, S. H., T. Yehuda, S. Smolikov, R. Gurevich, J. Hawk, C. Coker, A. Krauskopf, M. Kupiec, and M. J. McEachern. 2004. A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl. Acad. Sci. USA 101:8658-8663.
5. Baetz, K. K., N. J. Krogan, A. Emili, J. Greenblatt, and P. Hieter. 2004. The ctf13-30/CTF13 genomic haploinsufficiency modifier screen identifies the yeast chromatin remodeling complex RSC, which is required for the establishment of sister chromatid cohesion. Mol. Cell. Biol. 24:1232-1244.
6. Barlev, N. A., V. Poltoratsky, T. Owen-Hughes, C. Ying, L. Liu, J. L. Workman, and S. L. Berger. 1998. Repression of GCN5 histone acetyltransferase activity via bromodomain-mediated binding and phosphorylation by the Ku-DNA-dependent protein kinase complex. Mol. Cell. Biol. 18:1349-1358.
7. Bassing, C. H., and F. W. Alt. 2004. The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amsterdam) 3:781-796.
8. Bassing, C. H., K. F. Chua, J. Sekiguchi, H. Suh, S. R. Whitlow, J. C. Fleming, B. C. Monroe, D. N. Ciccone, C. Yan, K. Vlasakova, D. M. Livingston, D. O. Ferguson, R. Scully, and F. W. Alt. 2002. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. USA 99:8173-8178.
9. Bennett, C. B., L. K. Lewis, G. Karthikeyan, K. S. Lobachev, Y. H. Jin, J. F. Sterling, J. R. Snipe, and M. A. Resnick. 2001. Genes required for ionizing radiation resistance in yeast. Nat. Genet. 29:426-434.
10. Bird, A. W., D. Y. Yu, M. G. Pray-Grant, Q. Qiu, K. E. Harmon, P. C. Megee, P. A. Grant, M. M. Smith, and M. F. Christman. 2002. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419:411-415.
11. Boulton, S. J., and S. P. Jackson. 1998. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17:1819-1828.
12. Boulton, S. J., and S. P. Jackson. 1996. Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res. 24:4639-4648.
13. Boyer, L. A., M. R. Langer, K. A. Crowley, S. Tan, J. M. Denu, and C. L. Peterson. 2002. Essential role for the SANT domain in the functioning of multiple chromatin remodeling enzymes. Mol. Cell 10:935-942.
14. Cairns, B. R., Y. Lorch, Y. Li, M. Zhang, L. Lacomis, H. Erdjument-Bromage, P. Tempst, J. Du, B. Laurent, and R. D. Kornberg. 1996. RSC, an essential, abundant chromatin-remodeling complex. Cell 87:1249-1260.
15. Cairns, B. R., A. Schlichter, H. Erdjument-Bromage, P. Tempst, R. D. Kornberg, and F. Winston. 1999. Two functionally distinct forms of the RSC nucleosome-remodeling complex, containing essential AT hook, BAH, and bromodomains. Mol. Cell 4:715-723.
16. Celeste, A., S. Difilippantonio, M. J. Difilippantonio, O. Fernandez-Capetillo, D. R. Pilch, O. A. Sedelnikova, M. Eckhaus, T. Ried, W. M. Bonner, and A. Nussenzweig. 2003. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114:371-383.
17. Chen, L., K. Trujillo, W. Ramos, P. Sung, and A. E. Tomkinson. 2001. Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol. Cell 8:1105-1115.
18. Critchlow, S. E., and S. P. Jackson. 1998. DNA end-joining: from yeast to man. Trends Biochem. Sci. 23:394-398.
19. Dhalluin, C., J. E. Carlson, L. Zeng, C. He, A. K. Aggarwal, and M. M. Zhou. 1999. Structure and ligand of a histone acetyltransferase bromodomain. Nature 399:491-496.
20. Downs, J. A., S. Allard, O. Jobin-Robitaille, A. Javaheri, A. Auger, N. Bouchard, S. J. Kron, S. P. Jackson, and J. Cote. 2004. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16:979-990.
21. Downs, J. A., and S. P. Jackson. 2004. A means to a DNA end: the many roles of Ku. Nat. Rev. Mol. Cell Biol. 5:367-378.
22. Downs, J. A., N. F. Lowndes, and S. P. Jackson. 2000. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408:1001-1004.
23. Fritsch, O., G. Benvenuto, C. Bowler, J. Molinier, B. Hohn, Z. O. Jonsson, S. Jha, J. A. Wohlschlegel, A. Dutta. 2004. The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol. Cell 16:479-485.
24. Fyodorov, D. V., and J. T. Kadonaga. 2001. The many faces of chromatin remodeling: SWItching beyond transcription. Cell 106:523-525.
25. Green, C. M., and G. Almouzni. 2002. When repair meets chromatin. First in series on chromatin dynamics. EMBO Rep. 3:28-33.
26. Haber, J. E. 2000. Lucky breaks: analysis of recombination in Saccharomyces. Mutat Res. 451:53-69.
27. Haber, J. E. 1998. Mating-type gene switching in Saccharomyces cerevisiae. Annu. Rev. Genet. 32:561-599.
28. Huang, J., J. M. Hsu, and B. C. Laurent. 2004. The RSC nucleosome-remodeling complex is required for cohesin's association with chromosome arms. Mol. Cell 13:739-750.
29. Jazayeri, A., A. D. McAinsh, and S. P. Jackson. 2004. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 101:1644-1649.
30. Jonsson, Z. O., S. Jha, J. A. Wohlschlegel, and A. Dutta. 2004. Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. Mol. Cell 16:465-477.
31. Kasten, M., H. Szerlong, H. Erdjument-Bromage, P. Tempst, M. Werner, and B. R. Cairns. 2004. Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J. 23:1348-1359.
32. Kegel, A., J. O. Sjostrand, and S. U. Astrom. 2001. Nej1p, a cell type-specific regulator of nonhomologous end joining in yeast. Curr. Biol. 11:1611-1617.
33. Kim, J. S., T. B. Krasieva, V. LaMorte, A. M. Taylor, and K. Yokomori. 2002. Specific recruitment of human cohesin to laser-induced DNA damage. J. Biol. Chem. 277:45149-45153.
34. Kobor, M. S., S. Venkatasubrahmanyam, M. D. Meneghini, J. W. Gin, J. L. Jennings, A. J. Link, H. D. Madhani, and J. Rine. 2004. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol. 2:E131.
35. Koyama, H., M. Itoh, K. Miyahara, and E. Tsuchiya. 2002. Abundance of the RSC nucleosome-remodeling complex is important for the cells to tolerate DNA damage in Saccharomyces cerevisiae. FEBS Lett. 531:215-221.
36. Krejci, L., L. Chen, S. Van Komen, P. Sung, and A. Tomkinson. 2003. Mending the break: two DNA double-strand break repair machines in eukaryotes. Prog. Nucleic Acid Res. Mol. Biol. 74:159-201.
37. Krejci, L., J. Damborsky, B. Thomsen, M. Duno, and C. Bendixen. 2001. Molecular dissection of interactions between Rad51 and members of the recombination-repair group. Mol. Cell. Biol. 21:966-976.
38. Krogan, N. J., M. C. Keogh, N. Datta, C. Sawa, O. W. Ryan, H. Ding, R. A. Haw, J. Pootoolal, A. Tong, V. Canadien, D. P. Richards, X. Wu, A. Emili, T. R. Hughes, S. Buratowski, and J. F. Greenblatt. 2003. A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol. Cell 12:1565-1576.
39. 2/M arrest after DNA damage. Cell 94:399-409.
40. Lee, S. E., F. Paques, J. Sylvan, and J. E. Haber. 1999. Role of yeast SIR genes and mating type in directing DNA double-strand breaks to homologous and non-homologous repair paths. Curr. Biol. 9:767-770.
41. Lisby, M., J. H. Barlow, R. C. Burgess, and R. Rothstein. 2004. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118:699-713.
42. Martens, J. A., and F. Winston. 2003. Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev. 13:136-142.
43. Mizuguchi, G., X. Shen, J. Landry, W. H. Wu, S. Sen, and C. Wu. 2004. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:343-348.
44. Moore, J. K., and J. E. Haber. 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.
45. Moreau, S., J. R. Ferguson, and L. S. Symington. 1999. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19:556-566.
46. Morrison, A. J., J. Highland, N. J. Krogan, A. Arbel-Eden, J. F. Greenblatt, J. E. Haber, and X. Shen. 2004. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119:767-775.
47. Nugent, C. I., G. Bosco, L. O. Ross, S. K. Evans, A. P. Salinger, J. K. Moore, J. E. Haber, and V. Lundblad. 1998. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol. 8:657-660.
48. Ooi, S. L., D. D. Shoemaker, and J. D. Boeke. 2001. A DNA microarray-based genetic screen for nonhomologous end-joining mutants in Saccharomyces cerevisiae. Science 294:2552-2556.
49. Paques, F., and J. E. Haber. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63:349-404.
50. Peterson, C. L., and J. Cote. 2004. Cellular machineries for chromosomal DNA repair. Genes Dev. 18:602-616.
51. Petrini, J. H. 1999. The mammalian Mre11-Rad50-nbs1 protein complex: integration of functions in the cellular DNA-damage response. Am. J. Hum. Genet. 64:1264-1269.
52. Pierce, A. J., J. M. Stark, F. D. Araujo, M. E. Moynahan, M. Berwick, and M. Jasin. 2001. Double-strand breaks and tumorigenesis. Trends Cell Biol. 11:S52-S59.
53. Redon, C., D. R. Pilch, E. P. Rogakou, A. H. Orr, N. F. Lowndes, and W. M. Bonner. 2003. Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint-blind DNA damage. EMBO Rep. 4:1-7.
54. Ross-Macdonald, P., P. S. Coelho, T. Roemer, S. Agarwal, A. Kumar, R. Jansen, K. H. Cheung, A. Sheehan, D. Symoniatis, L. Umansky, M. Heidtman, F. K. Nelson, H. Iwasaki, K. Hager, M. Gerstein, P. Miller, G. S. Roeder, and M. Snyder. 1999. Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature 402:413-418.
55. Saha, A., J. Wittmeyer, and B. R. Cairns. 2002. Chromatin remodeling by RSC involves ATP-dependent DNA translocation. Genes Dev. 16:2120-2134.
56. Schar, P., M. Fasi, and R. Jessberger. 2004. SMC1 coordinates DNA double-strand break repair pathways. Nucleic Acids Res. 32:3921-3929.
57. Shen, X., G. Mizuguchi, A. Hamiche, and C. Wu. 2000. A chromatin remodelling complex involved in transcription and DNA processing. Nature 406:541-544.
58. Shroff, R., A. Arbel-Eden, D. Pilch, G. Ira, W. M. Bonner, J. H. Petrini, J. E. Haber, and M. Lichten. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14:1703-1711.
59. Siede, W., A. A. Friedl, I. Dianova, F. Eckardt-Schupp, and E. C. Friedberg. 1996. The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics 142:91-102.
60. Sjogren, C., and K. Nasmyth. 2001. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol. 11:991-995.
61. Strom, L., H. B. Lindroos, K. Shirahige, and C. Sjogren. 2004. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell 16:1003-1015.
62. Sugawara, N., X. Wang, and J. E. Haber. 2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12:209-219.
63. Treich, I., L. Ho, and M. Carlson. 1998. Direct interaction between Rsc6 and Rsc8/Swh3, two proteins that are conserved in SWI/SNF-related complexes. Nucleic Acids Res. 26:3739-3745.
64. Trujillo, K. M., and P. Sung. 2001. DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50*Mre11 complex. J. Biol. Chem. 276:35458-35464.
65. Tseng, H. M., and A. E. Tomkinson. 2002. A physical and functional interaction between yeast Pol4 and Dnl4-Lif1 links DNA synthesis and ligation in nonhomologous end joining. J. Biol. Chem. 277:45630-45637.
66. Unal, E., A. Arbel-Eden, U. Sattler, R. Shroff, M. Lichten, J. E. Haber, and D. Koshland. 2004. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16:991-1002.
67. Valencia, M., M. Bentele, M. B. Vaze, G. Herrmann, E. Kraus, S. E. Lee, P. Schar, and J. E. Haber. 2001. NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae. Nature 414:666-669.
68. van Attikum, H., O. Fritsch, B. Hohn, and S. M. Gasser. 2004. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777-788.
69. Van Komen, S., G. Petukhova, S. Sigurdsson, S. Stratton, and P. Sung. 2000. Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell 6:563-572.
70. Wang, W. 2003. The SWI/SNF family of ATP-dependent chromatin remodelers: similar mechanisms for diverse functions. Curr. Top. Microbiol. Immunol. 274:143-169.
71. Wilson, T. E., U. Grawunder, and M. R. Lieber. 1997. Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 388:495-498.
72. Wilson, T. E., and M. R. Lieber. 1999. Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway. J. Biol. Chem. 274:23599-23609.
73. Wong, M. C., S. R. Scott-Drew, M. J. Hayes, P. J. Howard, and J. A. Murray. 2002. RSC2, encoding a component of the RSC nucleosome remodeling complex, is essential for 2μm plasmid maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol. 22:4218-4229.
74. Wu, C., T. Tsukiyama, D. Gdula, P. Georgel, M. Martinez-Balbas, G. Mizuguchi, V. Ossipow, R. Sandaltzopoulos, and H. M. Wang. 1998. ATP-dependent remodeling of chromatin. Cold Spring Harbor Symp. Quant. Biol. 63:525-534.
75. Wu, X., T. E. Wilson, and M. R. Lieber. 1999. A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Proc. Natl. Acad. Sci. USA 96:1303-1308.