Synergistic action of the Saccharomyces cerevisiae homologous recombination factors Rad54 and Rad51 in chromatin remodeling

DNA Repair

Volumn 6, Issue 10, 2007, Pages 1496-1506

  Kwon, YoungHo ^a   Chi, Peter ^a   Roh, Dong Hyun ^b   Klein, Hannah ^c   Sung, Patrick ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Chungbuk National University   (South Korea)

^c Kaplan Cancer Center   (United States)

Author keywords

Chromatin remodeling; D loop; Homologous recombination; Rad51; Rad54

Indexed keywords

DNA; HISTONE; RAD51 PROTEIN; RAD54 PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DNA REPAIR; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SACCHAROMYCES CEREVISIAE;

CHROMATIN; DNA REPAIR ENZYMES; MUTATION; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 34548522658     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.04.012     Document Type: Article

References (53)

1. Bezzubova O., Silbergleit A., Yamaguchi-Iwai Y., Takeda S., and Buerstedde J.M. Reduced X-ray resistance and homologous recombination frequencies in a RAD54-/- mutant of the chicken DT40 cell line. Cell 89 (1997) 185-193
2. Essers J., Hendriks R.W., Swagemakers S.M., Troelstra C., de Wit J., Bootsma D., Hoeijmakers J.H., and Kanaar R. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89 (1997) 195-204
3. Schmuckli-Maurer J., Rolfsmeier M., Nguyen H., and Heyer W.D. Genome instability in rad54 mutants of Saccharomyces cerevisiae. Nucleic Acids Res. 31 (2003) 1013-1023
4. Matsuda M., Miyagawa K., Takahashi M., Fukuda T., Kataoka T., Asahara T., Inui H., Watatani M., Yasutomi M., Kamada N., Dohi K., and Kamiya K. Mutations in the RAD54 recombination gene in primary cancers. Oncogene 18 (1999) 3427-3430
5. Smirnova M., Van Komen S., Sung P., and Klein H.L. Effects of tumor-associated mutations on Rad54 functions. J. Biol. Chem. 279 (2004) 24081-24088
6. Swagemakers S.M., Essers J., de Wit J., Hoeijmakers J.H., and Kanaar R. The human RAD54 recombinational DNA repair protein is a double-stranded DNA-dependent ATPase. J. Biol. Chem. 273 (1998) 28292-28297
7. Petukhova G., Stratton S., and Sung P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393 (1998) 91-94
8. Amitani I., Baskin R.J., and Kowalczykowski S.C. Visualization of Rad54, a chromatin remodeling protein, translocating on single DNA molecules. Mol. Cell. 23 (2006) 143-148
9. Van Komen S., Petukhova G., Sigurdsson S., Stratton S., and Sung P. Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell. 6 (2000) 563-572
10. Ristic D., Wyman C., Paulusma C., and Kanaar R. The architecture of the human Rad54-DNA complex provides evidence for protein translocation along DNA. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 8454-8460
11. Sigurdsson S., Van Komen S., Petukhova G., and Sung P. Homologous DNA pairing by human recombination factors Rad51 and Rad54. J. Biol. Chem. 277 (2002) 42790-42794
12. Jaskelioff M., Van Komen S., Krebs J.E., Sung P., and Peterson C.L. Rad54p is a chromatin remodeling enzyme required for heteroduplex DNA joint formation with chromatin. J. Biol. Chem. 278 (2003) 9212-9218
13. Alexeev A., Mazin A., and Kowalczykowski S.C. Rad54 protein possesses chromatin-remo deling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat. Struct. Biol. 10 (2003) 182-186
14. Alexiadis V., and Kadonaga J.T. Strand pairing by Rad54 and Rad51 is enhanced by chromatin. Genes Dev. 16 (2002) 2767-2771
15. Solinger J.A., and Heyer W.D. Rad54 protein stimulates the postsynaptic phase of Rad51 protein-mediated DNA strand exchange. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 8447-8453
16. Bugreev D.V., Mazina O.M., and Mazin A.V. Rad54 protein promotes branch migration of Holliday junctions. Nature 442 (2006) 590-593
17. Symington L.S. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66 (2002) 630-670
18. Sung P., and Klein H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell. Biol. 7 (2006) 739-750
19. Bianco P.R., Tracy R.B., and Kowalczykowski S.C. DNA strand exchange proteins: a biochemical and physical comparison. Front. Biosci. 3 (1998) D570-D603
20. Sung P., Krejci L., Van Komen S., and Sehorn M.G. Rad51 recombinase and recombination mediators. J. Biol. Chem. 278 (2003) 42729-42732
21. 2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 9988-9993
22. Chi P., Van Komen S., Sehorn M.G., Sigurdsson S., and Sung P. Roles of ATP binding and ATP hydrolysis in human Rad51 recombinase function. DNA Repair (Amst.) 5 (2006) 381-391
23. Cox M.M. The bacterial RecA protein as a motor protein. Annu. Rev. Microbiol. 57 (2003) 551-577
24. Ristic D., Modesti M., van der Heijden T., van Noort J., Dekker C., Kanaar R., and Wyman C. Human Rad51 filaments on double- and single-stranded DNA: correlating regular and irregular forms with recombination function. Nucleic Acids Res. 33 (2005) 3292-3302
25. Jiang H., Xie Y., Houston P., Stemke-Hale K., Mortensen U.H., Rothstein R., and Kodadek T. Direct association between the yeast Rad51 and Rad54 recombination proteins. J. Biol. Chem. 271 (1996) 33181-33186
26. Clever B., Interthal H., Schmuckli-Maurer J., King J., Sigrist M., and Heyer W.D. Recombinational repair in yeast: functional interactions between Rad51 and Rad54 proteins. EMBO J. 16 (1997) 2535-2544
27. Petukhova G., Van Komen S., Vergano S., Klein H., and Sung P. Yeast Rad54 promotes Rad51-dependent homologous DNA pairing via ATP hydrolysis-driven change in DNA double helix conformation. J. Biol. Chem. 274 (1999) 29453-29462
28. Raschle M., Van Komen S., Chi P., Ellenberger T., and Sung P. Multiple interactions with the Rad51 recombinase govern the homologous recombination function of Rad54. J. Biol. Chem. 279 (2004) 51973-51980
29. Alexiadis V., Lusser A., and Kadonaga J.T. A conserved N-terminal motif in Rad54 is important for chromatin remodeling and homologous strand pairing. J. Biol. Chem. 279 (2004) 27824-27829
30. Solinger J.A., Kiianitsa K., and Heyer W.D. Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol. Cell. 10 (2002) 1175-1188
31. Wolner B., van Komen S., Sung P., and Peterson C.L. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell. 12 (2003) 221-232
32. Mazin A.V., Alexeev A.A., and Kowalczykowski S.C. A novel function of Rad54 protein. Stabilization of the Rad51 nucleoprotein filament. J. Biol. Chem. 278 (2003) 14029-14036
33. Sugawara N., Wang X., and Haber J.E. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell. 12 (2003) 209-219
34. Wolner B., and Peterson C.L. ATP-dependent and ATP-independent roles for the Rad54 chromatin remodeling enzyme during recombinational repair of a DNA double strand break. J. Biol. Chem. 280 (2005) 10855-10860
35. Mazin A.V., Bornarth C.J., Solinger J.A., Heyer W.D., and Kowalczykowski S.C. Rad54 protein is targeted to pairing loci by the Rad51 nucleoprotein filament. Mol. Cell. 6 (2000) 583-592
36. Houston P.L., and Broach J.R. The dynamics of homologous pairing during mating type interconversion in budding yeast. PLoS Genet. 2 (2006) e98
37. Sung P., and Stratton S.A. Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J. Biol. Chem. 271 (1996) 27983-27986
38. Stein A. Reconstitution of chromatin from purified components. Methods Enzymol. 170 (1989) 585-603
39. Jeong S.W., Lauderdale J.D., and Stein A. Chromatin assembly on plasmid DNA in vitro. Apparent spreading of nucleosome alignment from one region of pBR327 by histone H5. J. Mol. Biol. 222 (1991) 1131-1147
40. Lusser A., and Kadonaga J.T. Strategies for the reconstitution of chromatin. Nat. Methods 1 (2004) 19-26
41. Sung P., and Robberson D.L. DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82 (1995) 453-461
42. Krejci L., Damborsky J., Thomsen B., Duno M., and Bendixen C. Molecular dissection of interactions between Rad51 and members of the recombination-repair group. Mol. Cell. Biol. 21 (2001) 966-976
43. Zhang X.P., Lee K.I., Solinger J.A., Kiianitsa K., and Heyer W.D. Gly-103 in the N-terminal domain of Saccharomyces cerevisiae Rad51 protein is critical for DNA binding. J. Biol. Chem. 280 (2005) 26303-26311
44. Galkin V.E., Wu Y., Zhang X.P., Qian X., He Y., Yu X., Heyer W.D., Luo Y., and Egelman E.H. The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity. Structure 14 (2006) 983-992
45. Becker P.B., and Horz W. ATP-dependent nucleosome remodeling. Annu. Rev. Biochem. 71 (2002) 247-273
46. Hecht A., Laroche T., Strahl-Bolsinger S., Gasser S.M., and Grunstein M. HistoneH3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80 (1995) 583-592
47. 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
48. Boyer L.A., Latek R.R., and Peterson C.L. The SANT domain: a unique histone-tail-binding module?. Nat. Rev. Mol. Cell. Biol. 5 (2004) 158-163
49. Clapier C.R., Langst G., Corona D.F., Becker P.B., and Nightingale K.P. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 21 (2001) 875-883
50. Dang W., Kagalwala M.N., and Bartholomew B. Regulation of ISW2 by concerted action of histone H4 tail and extranucleosomal DNA. Mol. Cell. Biol. 26 (2006) 7388-7396
51. Kasten M., Szerlong H., Erdjument-Bromage H., Tempst P., Werner M., and Cairns B.R. Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J. 23 (2004) 1348-1359
52. Georgel P.T., Palacios DeBeer M.A., Pietz G., Fox C.A., and Hansen J.C. Sir3-dependent assembly of supramolecular chromatin structures in vitro. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 8584-8589
53. Georgel P.T., Tsukiyama T., and Wu C. Role of histone tails in nucleosome remodeling by Drosophila NURF. EMBO J. 16 (1997) 4717-4726