The Yeast Chromatin Remodeler RSC Complex Facilitates End Joining Repair of DNA Double-strand Breaks

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2005 May 5

PMID 15870268

Citations 79

Authors

Eun Yong Shim

Jia-Lin Ma

Ji-Hyun Oum

Yvonne Yanez

Sang Eun Lee

Affiliations

Soon will be listed here.

Abstract

Repair of chromosome double-strand breaks (DSBs) is central to cell survival and genome integrity. Nonhomologous end joining (NHEJ) is the major cellular repair pathway that eliminates chromosome DSBs. Here we report our genetic screen that identified Rsc8 and Rsc30, subunits of the Saccharomyces cerevisiae chromatin remodeling complex RSC, as novel NHEJ factors. Deletion of RSC30 gene or the C-terminal truncation of RSC8 impairs NHEJ of a chromosome DSB created by HO endonuclease in vivo. rsc30Delta maintains a robust level of homologous recombination and the damage-induced cell cycle checkpoints. By chromatin immunoprecipitation, we show recruitment of RSC to a chromosome DSB with kinetics congruent with its involvement in NHEJ. Recruitment of RSC to a DSB depends on Mre11, Rsc30, and yKu70 proteins. Rsc1p and Rsc2p, two other RSC subunits, physically interact with yKu80p and Mre11p. The interaction of Rsc1p with Mre11p appears to be vital for survival from genotoxic stress. These results suggest that chromatin remodeling by RSC is important for NHEJ.

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References

Petrini J . The mammalian Mre11-Rad50-nbs1 protein complex: integration of functions in the cellular DNA-damage response. Am J Hum Genet. 1999; 64(5):1264-9. PMC: 1377860. DOI: 10.1086/302391. View

Paques F, Haber J . Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1999; 63(2):349-404. PMC: 98970. DOI: 10.1128/MMBR.63.2.349-404.1999. View

Dhalluin C, Carlson J, Zeng L, He C, Aggarwal A, Zhou M . Structure and ligand of a histone acetyltransferase bromodomain. Nature. 1999; 399(6735):491-6. DOI: 10.1038/20974. View

Wu C, Tsukiyama T, Gdula D, Georgel P, Mizuguchi G, Ossipow V . ATP-dependent remodeling of chromatin. Cold Spring Harb Symp Quant Biol. 1999; 63:525-34. DOI: 10.1101/sqb.1998.63.525. View

Lee S, Paques F, Sylvan J, Haber J . Role of yeast SIR genes and mating type in directing DNA double-strand breaks to homologous and non-homologous repair paths. Curr Biol. 1999; 9(14):767-70. DOI: 10.1016/s0960-9822(99)80339-x. View

Wilson T, Lieber M . Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway. J Biol Chem. 1999; 274(33):23599-609. DOI: 10.1074/jbc.274.33.23599. View

Jonsson Z, Jha S, Wohlschlegel J, Dutta A . Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. Mol Cell. 2004; 16(3):465-77. DOI: 10.1016/j.molcel.2004.09.033. View

Fritsch O, Benvenuto G, Bowler C, Molinier J, Hohn B . The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol Cell. 2004; 16(3):479-85. DOI: 10.1016/j.molcel.2004.09.034. View

Morrison A, Highland J, Krogan N, Arbel-Eden A, Greenblatt J, Haber J . INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell. 2004; 119(6):767-75. DOI: 10.1016/j.cell.2004.11.037. View

10.

van Attikum H, Fritsch O, Hohn B, Gasser S . Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell. 2004; 119(6):777-88. DOI: 10.1016/j.cell.2004.11.033. View

11.

Downs J, Allard S, Jobin-Robitaille O, Javaheri A, Auger A, Bouchard N . Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell. 2004; 16(6):979-90. DOI: 10.1016/j.molcel.2004.12.003. View

12.

Kim J, Krasieva T, LaMorte V, Taylor A, Yokomori K . Specific recruitment of human cohesin to laser-induced DNA damage. J Biol Chem. 2002; 277(47):45149-53. DOI: 10.1074/jbc.M209123200. View

13.

Tseng H, Tomkinson A . A physical and functional interaction between yeast Pol4 and Dnl4-Lif1 links DNA synthesis and ligation in nonhomologous end joining. J Biol Chem. 2002; 277(47):45630-7. DOI: 10.1074/jbc.M206861200. View

14.

Wang W . The SWI/SNF family of ATP-dependent chromatin remodelers: similar mechanisms for diverse functions. Curr Top Microbiol Immunol. 2003; 274:143-69. DOI: 10.1007/978-3-642-55747-7_6. View

15.

Ross-Macdonald P, Coelho P, Roemer T, Agarwal S, Kumar A, Jansen R . Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature. 1999; 402(6760):413-8. DOI: 10.1038/46558. View

16.

Cairns B, Schlichter A, Erdjument-Bromage H, Tempst P, Kornberg R, Winston F . Two functionally distinct forms of the RSC nucleosome-remodeling complex, containing essential AT hook, BAH, and bromodomains. Mol Cell. 2000; 4(5):715-23. DOI: 10.1016/s1097-2765(00)80382-2. View

17.

Haber J . Lucky breaks: analysis of recombination in Saccharomyces. Mutat Res. 2000; 451(1-2):53-69. DOI: 10.1016/s0027-5107(00)00040-3. View

18.

Shen X, Mizuguchi G, Hamiche A, Wu C . A chromatin remodelling complex involved in transcription and DNA processing. Nature. 2000; 406(6795):541-4. DOI: 10.1038/35020123. View

19.

Van Komen S, Petukhova G, Sigurdsson S, Stratton S, Sung P . Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol Cell. 2000; 6(3):563-72. DOI: 10.1016/s1097-2765(00)00055-1. View

20.

Krejci L, Damborsky J, Thomsen B, Duno M, Bendixen C . Molecular dissection of interactions between Rad51 and members of the recombination-repair group. Mol Cell Biol. 2001; 21(3):966-76. PMC: 86686. DOI: 10.1128/MCB.21.3.966-976.2001. View