A Rad51 Presynaptic Filament Is Sufficient to Capture Nucleosomal Homology during Recombinational Repair of a DNA Double-Strand Break

Molecular Cell

Volumn 30, Issue 6, 2008, Pages 803-810

  Sinha, Manisha ^a   Peterson, Craig L ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

DNA

Indexed keywords

BIOTIN; DOUBLE STRANDED DNA; RAD51 PROTEIN; RAD54 PROTEIN; STREPTAVIDIN;

ARTICLE; CELL SURVIVAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; EUKARYOTIC CELL; GENE SEQUENCE; GENOMIC INSTABILITY; MINICHROMOSOME; MOLECULAR RECOGNITION; NUCLEOSOME;

BINDING SITES; CHROMATIN; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; HISTONES; HUMANS; KINETICS; NUCLEOSOMES; PEPTIDE FRAGMENTS; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 44949091416     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2008.04.015     Document Type: Article

References (39)

1. Adzuma K. No sliding during homology search by RecA protein. J. Biol. Chem. 273 (1998) 31565-31573
2. Alexeev A., Mazin A., and Kowalczykowski S.C. Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat. Struct. Biol. 10 (2003) 182-186
3. Alexiadis V., and Kadonaga J.T. Strand pairing by Rad54 and Rad51 is enhanced by chromatin. Genes Dev. 16 (2002) 2767-2771
4. Allard S., Masson J.Y., and Cote J. Chromatin remodeling and the maintenance of genome integrity. Biochim. Biophys. Acta 1677 (2004) 158-164
5. 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
6. Carruthers L.M., Tse C., Walker III K.P., and Hansen J.C. Assembly of defined nucleosomal and chromatin arrays from pure components. Methods Enzymol. 304 (1999) 19-35
7. Chai B., Huang J., Cairns B.R., and Laurent B.C. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19 (2005) 1656-1661
8. 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
9. Christiansen G., and Griffith J. Visualization of the paranemic joining of homologous DNA molecules catalyzed by the RecA protein of Escherichia coli. Proc. Natl. Acad. Sci. USA 83 (1986) 2066-2070
10. Cox M.M. The bacterial RecA protein as a motor protein. Annu. Rev. Microbiol. 57 (2003) 551-577
11. Folta-Stogniew E., O'Malley S., Gupta R., Anderson K.S., and Radding C.M. Exchange of DNA base pairs that coincides with recognition of homology promoted by E. coli RecA protein. Mol. Cell 15 (2004) 965-975
12. Gonda D.K., and Radding C.M. By searching processively RecA protein pairs DNA molecules that share a limited stretch of homology. Cell 34 (1983) 647-654
13. Gupta R.C., Folta-Stogniew E., O'Malley S., Takahashi M., and Radding C.M. Rapid exchange of A:T base pairs is essential for recognition of DNA homology by human Rad51 recombination protein. Mol. Cell 4 (1999) 705-714
14. Haber J.E., Leung W.Y., Borts R.H., and Lichten M. The frequency of meiotic recombination in yeast is independent of the number and position of homologous donor sequences: implications for chromosome pairing. Proc. Natl. Acad. Sci. USA 88 (1991) 1120-1124
15. Hansen J.C. Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu. Rev. Biophys. Biomol. Struct. 31 (2002) 361-392
16. Hsieh P., Camerini-Otero C.S., and Camerini-Otero R.D. The synapsis event in the homologous pairing of DNAs: RecA recognizes and pairs less than one helical repeat of DNA. Proc. Natl. Acad. Sci. USA 89 (1992) 6492-6496
17. Ikeda K., Steger D.J., Eberharter A., and Workman J.L. Activation domain-specific and general transcription stimulation by native histone acetyltransferase complexes. Mol. Cell. Biol. 19 (1999) 855-863
18. Inbar O., and Kupiec M. Homology search and choice of homologous partner during mitotic recombination. Mol. Cell. Biol. 19 (1999) 4134-4142
19. 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
20. Klapstein K., Chou T., and Bruinsma R. Physics of RecA-mediated homologous recognition. Biophys. J. 87 (2004) 1466-1477
21. Konforti B.B., and Davis R.W. 3′ homologous free ends are required for stable joint molecule formation by the RecA and single-stranded binding proteins of Escherichia coli. Proc. Natl. Acad. Sci. USA 84 (1987) 690-694
22. Logie C., and Peterson C.L. Purification and biochemical properties of yeast SWI/SNF complex. Methods Enzymol. 304 (1999) 726-741
23. Luger K., Rechsteiner T.J., and Richmond T.J. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119 (1999) 1-16
24. Menetski J.P., Bear D.G., and Kowalczykowski S.C. Stable DNA heteroduplex formation catalyzed by the Escherichia coli RecA protein in the absence of ATP hydrolysis. Proc. Natl. Acad. Sci. USA 87 (1990) 21-25
25. Paques F., and Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63 (1999) 349-404
26. Peterson C.L., and Cote J. Cellular machineries for chromosomal DNA repair. Genes Dev. 18 (2004) 602-616
27. Ramdas J., Mythili E., and Muniyappa K. Nucleosomes on linear duplex DNA allow homologous pairing but prevent strand exchange promoted by RecA protein. Proc. Natl. Acad. Sci. USA 88 (1991) 1344-1348
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. Richardson C., Moynahan M.E., and Jasin M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12 (1998) 3831-3842
30. Riddles P.W., and Lehman I.R. The formation of paranemic and plectonemic joints between DNA molecules by the recA and single-stranded DNA-binding proteins of Escherichia coli. J. Biol. Chem. 260 (1985) 165-169
31. Solinger J.A., Lutz G., Sugiyama T., Kowalczykowski S.C., and Heyer W.D. Rad54 protein stimulates heteroduplex DNA formation in the synaptic phase of DNA strand exchange via specific interactions with the presynaptic Rad51 nucleoprotein filament. J. Mol. Biol. 307 (2001) 1207-1221
32. 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
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. Sung P., Krejci L., Van Komen S., and Sehorn M.G. Rad51 recombinase and recombination mediators. J. Biol. Chem. 278 (2003) 42729-42732
35. van Attikum H., Fritsch O., and Gasser S.M. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J. 26 (2007) 4113-4125
36. Van Komen S., Petukhova G., Sigurdsson S., and Sung P. Functional cross-talk among Rad51, Rad54, and replication protein A in heteroduplex DNA joint formation. J. Biol. Chem. 277 (2002) 43578-43587
37. 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
38. Zaitseva E.M., Zaitsev E.N., and Kowalczykowski S.C. The DNA binding properties of Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 274 (1999) 2907-2915
39. Zhang Z., Fan H.Y., Goldman J.A., and Kingston R.E. Homology-driven chromatin remodeling by human RAD54. Nat. Struct. Mol. Biol. 14 (2007) 397-405