Insights into the mechanism of Rad51 recombinase from the structure and properties of a filament interface mutant

Nucleic Acids Research

Volumn 38, Issue 14, 2010, Pages 4889-4906

  Chen, Jianhong ^a   Villanueva, Nicolas ^a   Rould, Mark A ^a   Morrical, Scott W ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; RAD51 PROTEIN; RECA PROTEIN; DNA; HISTIDINE; NUCLEOTIDE; RAD51 PROTEIN, S CEREVISIAE; REPLICATION FACTOR A; SACCHAROMYCES CEREVISIAE PROTEIN; SINGLE STRANDED DNA;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA STRAND; ESCHERICHIA COLI; HYDROLYSIS; ISOMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; YEAST; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MUTATION;

ESCHERICHIA COLI; EUKARYOTA;

ADENOSINE TRIPHOSPHATE; DNA; DNA, SINGLE-STRANDED; HISTIDINE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEOTIDES; RAD51 RECOMBINASE; REPLICATION PROTEIN A; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 77955777906     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq209     Document Type: Article

References (42)

1. Bianco,P.R., Tracy,R.B. and Kowalczykowski,S.C. (1998) DNA strand exchange proteins: a biochemical and physical comparison. Front. Biosci., 3, D570-D603.
2. San Filippo,J., Sung,P. and Klein,H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem., 77, 229-257.
3. Chi,P., Van Komen,S., Sehorn,M.G., Sigurdsson,S. and Sung,P. (2006) Roles of ATP binding and ATP hydrolysis in human Rad51 recombinase function. DNA Repair, 5, 381-391.
4. Chen,Z., Yang,H. and Pavletich,N.P. (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature, 453, 489-484.
5. Sheridan,S.D., Yu,X., Roth,R., Heuser,J.E., Sehorn,M.G., Sung,P., Egelman,E.H. and Bishop,D.K. (2008) A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic Acids Res., 36, 4057-4066.
6. New,J.H., Sugiyama,T., Zaitseva,E. and Kowalczykowski,S.C. (1998) Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature, 391, 407-410.
7. Sung,P. (1997) Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem., 272, 28194-28197.
8. Beernink,H.T. and Morrical,S.W. (1998) The uvsY recombination protein of bacteriophage T4 forms hexamers in the presence and absence of single-stranded DNA. Biochemistry, 37, 5673-5681.
9. Fortin,G.S. and Symington,L.S. (2002) Mutations in yeast Rad51 that partially bypass the requirement for Rad55 and Rad57 in DNA repair by increasing the stability of Rad51-DNA complexes. EMBO J., 21, 3160-3170.
10. Kelley,J.A. and Knight,K.L. (1997) Allosteric regulation of RecA protein function is mediated by Gln194. J. Biol. Chem., 272, 25778-25782.
11. Conway,A.B., Lynch,T.W., Zhang,Y., Fortin,G.S., Fung,C.W., Symington,L.S. and Rice,P.A. (2004) Crystal structure of a Rad51 filament. Nat. Struct. Mol. Biol., 11, 791-796.
12. De Zutter,J.K. and Knight,K.L. (1999) The hRad51 and RecA proteins show significant differences in cooperative binding to single-stranded DNA. J. Mol. Biol., 293, 769-780.
13. Grigorescu,A.A., Vissers,J.H., Ristic,D., Pigli,Y.Z., Lynch,T.W., Wyman,C. and Rice,P.A. (2009) Inter-subunit interactions that coordinate Rad510s activities. Nucleic Acids Res., 37, 557-567.
14. Lefebvre,S.D. and Morrical,S.W. (1997) Interactions of the bacteriophage T4 gene 59 protein with single-stranded polynucleotides: binding parameters and ion effects. J. Mol. Biol., 272, 312-326.
15. Menetski,J.P. and Kowalczykowski,S.C. (1985) Interaction of recA protein with single-stranded DNA. Quantitative aspects of binding affinity modulation by nucleotide cofactors. J. Mol. Biol., 181, 281-295.
16. Henricksen,L.A., Umbricht,C.B. and Wold,M.S. (1994) Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem., 269, 11121-11132.
17. Zaitseva,E.M., Zaitsev,E.N. and Kowalczykowski,S.C. (1999) The DNA binding properties of Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem., 274, 2907-2915.
18. Sweezy,M.A. and Morrical,S.W. (1997) Single-stranded DNA binding properties of the uvsY recombination protein of bacteriophage T4. J. Mol. Biol., 266, 927-938.
19. Liu,J., Qian,N. and Morrical,S.W. (2006) Dynamics of bacteriophage T4 presynaptic filament assembly from extrinsic fluorescence measurements of Gp32-single-stranded DNA interactions. J. Biol. Chem., 281, 26308-26319.
20. Rice,K.P., Eggler,A.L., Sung,P. and Cox,M.M. (2001) DNA pairing and strand exchange by the Escherichia coli RecA and yeast Rad51 proteins without ATP hydrolysis: on the importance of not getting stuck. J. Biol. Chem., 276, 38570-38581.
21. Sugiyama,T. and Kowalczykowski,S.C. (2002) Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J. Biol. Chem., 277, 31663-31672.
22. Ando,R.A. and Morrical,S.W. (1998) Single-stranded DNA binding properties of the UvsX recombinase of bacteriophage T4: binding parameters and effects of nucleotides. J. Mol. Biol., 283, 785-796.
23. Birdsall,B., King,R.W., Wheeler,M.R., Lewis,C.A. Jr, Goode,S.R., Dunlap,R.B. and Roberts,G.C. (1983) Correction for light absorption in fluorescence studies of protein-ligand interactions. Anal. Biochem., 132, 353-361.
24. Otwinowski,Z. and Minor,W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
25. Kissinger,C.R., Gehlhaar,D.K. and Fogel,D.B. (1999) Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. D Biol. Crystallogr., 55, 484-491.
26. Emsley,P. and Cowtan,K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
27. Brunger,A.T., Adams,P.D., Clore,G.M., DeLano,W.L., Gros,P., Grosse-Kunstleve,R.W., Jiang,J.S., Kuszewski,J., Nilges,M. and Pannu,N.S. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
28. Leonard,N.J. (1984) Etheno-substituted nucleotides and coenzymes: fluorescence and biological activity. CRC Crit. Rev. Biochem., 15, 125-199.
29. Sung,P. and Robberson,D.L. (1995) DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell, 82, 453-461.
30. Hegner,M., Smith,S.B. and Bustamante,C. (1999) Polymerization and mechanical properties of single RecA-DNA filaments. Proc. Natl Acad. Sci. USA, 96, 10109-10114.
31. van Noort,J., Verbrugge,S., Goosen,N., Dekker,C. and Dame,R.T. (2004) Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc. Natl Acad. Sci. USA, 101, 6969-6974.
32. Kim,J.M., Maraboeuf,F., Kim,S.K., Shinohara,A. and Takahashi,M. (2001) Effect of ions and nucleotides on the interactions of yeast Rad51 protein with single-stranded oligonucleotides. J. Biochem., 129, 469-475.
33. Kiianitsa,K., Solinger,J.A. and Heyer,W.D. (2003) NADH-coupled microplate photometric assay for kinetic studies of ATP-hydrolyzing enzymes with low and high specific activities. Anal. Biochem., 321, 266-271.
34. Sung,P. (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science, 265, 1241-1243.
35. van Mameren,J., Modesti,M., Kanaar,R., Wyman,C., Peterman,E.J. and Wuite,G.J. (2009) Counting RAD51 proteins disassembling from nucleoprotein filaments under tension. Nature, 457, 745-748.
36. Kantake,N., Sugiyama,T., Kolodner,R.D. and Kowalczykowski,S.C. (2003) The recombination-deficient mutant RPA (rfa1-t11) is displaced slowly from single-stranded DNA by Rad51 protein. J. Biol. Chem., 278, 23410-23417.
37. McRobbie,A.M., Carter,L.G., Kerou,M., Liu,H., McMahon,S.A., Johnson,K.A., Oke,M., Naismith,J.H. and White,M.F. (2009) Structural and functional characterisation of a conserved archaeal RadA paralog with antirecombinase activity. J. Mol. Biol., 389, 661-673.
38. Brunger,A.T. (1997) Free R value: cross-validation in crystallography. Methods Enzymol., 277, 366.
39. Luzzati,V. (1952) Traitement statistique des erreurs dans la determination des structures cristallines. Acta Crystallogr., 5, 802-810.
40. Collaborative Computational Project, N. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr., 50, 760-763.
41. Laskowski,R.A., MacArthur,M.W., Moss,D.S. and Thornton,J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr., 26, 283-291.
42. Sugiyama,T., Zaitseva,E.M. and Kowaczykowski,S.C. (1997) A single-stranded DNA binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem., 272, 7940-7945.