Loop 2 in Saccharomyces cerevisiae Rad51 protein regulates filament formation and ATPase activity

Nucleic Acids Research

Volumn 37, Issue 1, 2009, Pages 158-171

  Zhang, Xiao Ping ^a   Galkin, Vitold E ^b   Yu, Xiong ^b   Egelman, Edward H ^b   Heyer, Wolf Dietrich ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALKYLATING AGENT; DOUBLE STRANDED DNA; MUTANT PROTEIN; RAD51 PROTEIN; SINGLE STRANDED DNA;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HYDROLYSIS; MICROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; WILD TYPE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; DNA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 58549116135     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn914     Document Type: Article

References (70)

1. Heyer,W.D. (2007) In Aguilera,A. and Rothstein,R. (eds), Molecular Genetics of Recombination., Springer-Verlag, Berlin-Heidelberg, pp. 95-133.
2. Krogh,B.O. and Symington,L.S. (2004) Recombination proteins in yeast. Annu. Rev. Genet., 38, 233-271.
3. Paques,F. and Haber,J.E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 63, 349-404.
4. Bianco,P.R., Tracy,R.B. and Kowalczykowski,S.C. (1998) DNA strand exchange proteins: A biochemical and physical comparison. Front. Biosci., 3, 570-603.
5. Kowalczykowski,S.C. (1991) Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange. Annu. Rev. Biophys. Biophys. Chem., 20, 539-575.
6. Gupta,R.C., Folta-Stogniew,E., O'Malley,S., Takahashi,M. and Radding,C.M. (1999) Rapid exchange of A: T base pairs is essential for recognition of DNA homology by human Rad51 recombination protein. Mol. Cell, 4, 705-714.
7. Folta-Stogniew,E., O'Malley,S., Gupta,R., Anderson,K.S. and Radding,C.M. (2004) Exchange of DNA base pairs that coincides with recognition of homology promoted by E. coli RecA protein. Mol. Cell. 15 965-975.
8. Howard-Flanders, P., West,S.C. and Stasiak,A. (1984) Role of RecA protein spiral filaments in genetic recombination. Nature, 309 215-219.
9. Mazin,A.V. and Kowalczykowski,S.C. (1996) The specificity of the secondary DNA binding site of RecA protein defines its role in DNA strand exchange. Proc. Natl Acad. Sci. USA, 93, 10673-10678.
10. Mazin,A.V. and Kowalczykowski,S.C. (1998) The function of the secondary DNA-binding site of RecA protein during DNA strand exchange. EMBO J. 17, 1161-1168.
11. Story,R.M., Weber,I.T. and Steitz,T.A. (1992) The structure of the E. coli recA protein monomer and polymer. Nature, 355, 318-325.
12. Egelman,E.H. and Stasiak,A. (1986) Structure of helical RecA-DNA complexes. Complexes formed in the presence of ATP-gamma-S or ATP. J. Mol. Biol., 191, 677-697.
13. Yu,X. and Egelman,E.H. (1993) The LexA repressor binds within the deep helical groove of the activated RecA filament. J. Mol. Biol., 231, 29-40.
14. Chen,Z., Yang,H. and Pavletich,N.P. (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature, 453 489-484.
15. 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. Nature Struct. Mol. Biol., 11, 791-796.
16. Ogawa,T., Yu,X., Shinohara,A. and Egelman,E.H. (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science, 259, 1896-1899.
17. Aihara,H., Ito,Y., Kurumizaka,H., Yokoyama,S. and Shibata,T. (1999) The N-terminal domain of the human Rad51 protein binds DNA: Structure and a DNA binding surface as revealed by NMR. J. Mol. Biol., 290, 495-504.
18. Yu,X., Jacobs,S.A., West,S.C., Ogawa,T. and Egelman,E.H. (2001) Domain structure and dynamics in the helical filaments formed by RecA and Rad51 on DNA. Proc. Natl Acad. Sci. USA, 98, 8419-8425.
19. 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.
20. Krejci,L., Damborsky,J., Thomsen,B., Duno,M. and Bendixen,C. (2001) Molecular dissection of interactions between Rad51 and members of the recombination-repair group. Mol. Cell Biol., 21, 966-976.
21. Liu,L., Maguire,K.K. and Kmiec,E.B. (2004) Genetic re-engineering of Saccharomyces cerevisiae RAD51 leads to a significant increase in the frequency of gene repair in vivo. Nucleic Acids Res., 32, 2093-2101.
22. Prasad,T.K., Yeykal,C.C. and Greene,E.C. (2006) Visualizing the assembly of human Rad51 filaments on double-stranded DNA. J. Mol. Biol., 363, 713-728.
23. Zhang,X.P., Lee,K.I., Solinger,J.A., Kiianitsa,K. and Heyer,W.D. (2005) Gly-103 in the N-terminal domain of Saccharomyces cerevisiae Rad51 protein is critical for DNA binding. J. Biol. Chem., 280, 26303-26311.
24. Sung,P. (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science, 265, 1241-1243.
25. Solinger,J.A., Lutz,G., Sugiyama,T., Kowalczykowski,S.C. and Heyer,W.-D. (2001) 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 1207-1221.
26. 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.
27. Kiianitsa,K., Solinger,J.A. and Heyer,W.D. (2002) Rad54 protein exerts diverse modes of ATPase activity on duplex DNA partially and fully covered with Rad51 protein. J. Biol. Chem., 277, 46205-46215.
28. Egelman,E.H. (2000) A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy, 85 225-234.
29. Thompson,J.D., Gibson,T.J., Plewniak,F., Jeanmougin,F. and Higgins,D.G. (1997) The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882.
30. Hall,T.A. (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser., 41, 95-98.
31. Marti-Renom,M.A., Stuart,A.C., Fiser,A., Sanchez,R., Melo,F. and Sali,A. (2000) Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct., 29, 291-325.
32. Sali,A. and Blundell,T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol., 234, 779-815.
33. 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. Cryst., 26, 283-291.
34. Vriend,G. (1990) WHAT IF: A molecular modeling and drug design program. J. Mol. Graph., 8, 52-56.
35. Sippl,M.J. (1993) Recognition of errors in three-dimensional structures of proteins. Proteins, 17, 355-362.
36. Bowie,J.U., Luthy,R. and Eisenberg,D. (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science, 253, 164-170.
37. Luthy,R., Bowie,J.U. and Eisenberg,D. (1992) Assessment of protein models with three-dimensional profiles. Nature, 356, 83-85.
38. Roca,A.I. and Cox,M.M. (1997) RecA protein: Structure, function and role in recombinational DNA repair. Prog. Nucleic Acid Res. Mol. Biol., 56, 129-223.
39. Solinger,J.A., Kiianitsa,K. and Heyer,W.-D. (2002) Rad54, a Swi2/ Snf2-like recombinational repair protein, disassembles Rad51:dSDNA filaments. Mol. Cell, 10, 1175-1188.
40. Petukhova,G., Stratton,S. and Sung,P. (1998) Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature, 393, 91-94.
41. Pugh,B.F. and Cox,M.M. (1988) High salt activation of recA protein ATPase in the absence of DNA. J. Biol. Chem., 263, 76-83.
42. DiCapua,E., Ruigrok,R.W. and Timmins,P.A. (1990) Activation of recA protein: The salt-induced structural transition. J. Struct. Biol., 104, 91-96.
43. Morimatsu,K. and Horii,T. (1995) DNA-binding surface of RecA protein photochemical cross-linking of the first DNA binding site on RecA filament. Eur. J. Biochem., 234, 695-705.
44. Malkov,V.A. and Camerini-Otero,R.D. (1995) Photocross-links between single-stranded DNA and Escherichia coli RecA protein map to loops L1 (amino acid residues 157-164) and L2 (amino acid residues 195-209). J. Biol. Chem., 270, 30230-30233.
45. Rehrauer,W.M. ane, Kowalczykowski,S.C. (1996) The DNA binding site(s) of the Escherichia coli RecA protein. J. Biol. Chem., 271 11996-12002.
46. Wang,Y. and Adzuma,K. (1996) Differential proximity probing of two DNA binding sites in the Escherichia coli recA protein using photo-cross-linking methods. Biochemistry, 35, 3563-3571.
47. Gardner,R.V., Voloshin,O.N. and Camerini-Otero,R.D. (1995) The identification of the single-stranded DNA-binding domain of the Escherichia coli RecA protein. Eur. J. Biochem., 233, 419-425.
48. Voloshin,O.N., Wang,L.J. and Camerini-Otero,R.D. (1996) Homologous DNA pairing promoted by a 20-amino acid peptide derived from RecA. Science, 272, 868-872.
49. Maraboeuf,F., Voloshin,O., Camerini-Otero,R.D. and Takahashi,M. (1995) The central aromatic residue in loop L2 of RecA interacts with DNA. Quenching of the fluorescence of a tryptophan reporter inserted in L2 upon binding to DNA. J. Biol. Chem., 270, 30927-30932.
50. Mirshad,J.K. and Kowalczykowski,S.C. (2003) Biochemical characterization of a mutant RecA protein altered in DNA-binding loop 1. Biochemistry 42, 5945-5954.
51. Wang,W.B. and Tessman,E.S. (1986) Location of functional regions of the Escherichia coli RecA protein by DNA sequence analysis of RecA protease-constitutive mutants. J. Bacteriol., 168, 901-910.
52. Menetski,J.P. and Kowalczykowski,S.C. (1990) Biochemical properties of the Escherichia coli recA430 protein. Analysis of a mutation that affects the interaction of the ATP-recA protein complex with single-stranded DNA. J. Mol. Biol., 211, 845-855.
53. Kawashima,H., Horii,T., Ogawa,T. and Ogawa,H. (1984) Functional domains of Escherichia coli recA protein deduced from the mutational sites in the gene. Mol. Gen. Genet., 193, 288-292.
54. Cazaux,C., Blanchet,J.S., Dupuis,D., Villani,G., Defais,M. and Johnson,N.P. (1998) Investigation of the secondary DNA-binding site of the bacterial recombinase RecA. J. Biol. Chem., 273, 28799-28804.
55. Matsuo,Y., Sakane,I., Takizawa,Y., Takahashi,M. and Kurumizaka,H. (2006) Roles of the human Rad51 L1 and L2 loops in DNA binding. FEBS J., 273, 3148-3159.
56. Kurumizaka,H., Aihara,H., Kagawa,W., Shibata,T. and Yokoyama,S. (1999) Human Rad51 amino acid residues required for Rad52 binding. J. Mol. Biol., 291, 537-548.
57. 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.
58. Bannister,L.A, Pezza,R.J., Donaldson,J.R., de Rooij,D.G., Schimenti,K.J., Camerini-Otero,R.D. and Schimenti,J.C. (2007) A dominant, recombination-defective allele of Dmcl causing male-specific sterility. PLoS Biol., 5, 1016-1025.
59. Sigurdsson,S., Trujillo,K., Song,B.W., Stratton,S. and Sung,P. (2001) Basis for avid homologous DNA strand exchange by human Rad51 and RPA. J. Biol. Chem., 276, 8798-8806.
60. 2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proc. Natl Acad. Sci. USA, 101, 9988-9993.
61. 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.
62. Wu,Y., Qian,X., He,Y., Moya,I.A. and Luo,Y. (2005) Crystal structure of an ATPase-active form of Rad51 homolog from Methanococcus voltae. Insights into potassium dependence. J. Biol. Chem., 280, 722-728.
63. Datta,S., Ganesh,N., Chandra,N.R., Muniyappa,K. and Vijayan,M. (2003) Structural studies on MtRecA-nucleotide complexes: Insights into DNA and nucleotide binding and the structural signature of NTP recognition. Proteins, 50, 474-485.
64. Aihara,H., Ito,Y., Kurumizaka,H., Terada,T., Yokoyama,S. and Shibata,T. (1997) An interaction between a specified surface of the C-terminal domain of RecA protein and double-stranded DNA for homologous pairing. J. Mol. Biol., 274, 213-221.
65. Story,R.M. and Steitz,T.A. (1992) Structure of the recA protein-ADP complex. Nature, 355, 374-376.
66. Voloshin,O.N., Wang,L.J. and Camerini-Otero,R.D. (2000) The homologous pairing domain of RecA also mediates the allosteric regulation of DNA binding and ATP hydrolysis: A remarkable concentration of functional residues. J. Mol. Biol., 303, 709-720.
67. Kelley,J.A. and Knight,K.L. (1997) Allosteric regulation of RecA protein function is mediated by Gln194. J. Biol. Chem., 272, 25778-25782.
68. Heyer,W.D., Li,X., Rolfsmeier,M. and Zhang,X.P. (2006) Rad54: The Swiss Army knife of homologous recombination? Nucleic Acids Res., 34 4115-4125.
69. Tan,T.L.R., Kanaar,R. and Wyman,C. (2003) Rad54, a Jack of all trades in homologous recombination. DNA Repair, 2, 787-794.
70. Kiianitsa,K., Solinger,J.A. and Heyer,W.D. (2006) Terminal association of Rad54 protein with the Rad51-dsDNA filament. Proc. Natl Acad. Sci. USA, 103, 9767-9772.