Full-length archaeal Rad51 structure and mutants: Mechanisms for RAD51 assembly and control by BRCA2

EMBO Journal

Volumn 22, Issue 17, 2003, Pages 4566-4576

  Shin, David S ^a,b   Pellegrini, Luca ^e   Daniels, Douglas S ^a,b   Yelent, Biana ^f   Craig, Lisa ^a,b   Bates, Debbie ^e   Yu, David S ^e   Shivji, Mahmud K ^e   Hitomi, Chiharu ^a,b   Arvai, Andrew S ^a,b   Volkmann, Niels ^c   Tsuruta, Hiro ^d   Blundell, Tom L ^e   Venkitaraman, Ashok R ^e   Tainer, John A ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c BURNHAM INSTITUTE   (United States)

^d SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BRCA2; DNA repair; Homologous recombination; RAD51; X ray crystal structure

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BRCA2 PROTEIN; CHAPERONE; DNA; MUTANT PROTEIN; NUCLEIC ACID BINDING PROTEIN; RAD51 PROTEIN; RAD52 PROTEIN; RAD54 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARCHAEBACTERIUM; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; GAMMA IRRADIATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN POLYMERIZATION; PYROCOCCUS FURIOSUS; X RAY ANALYSIS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; BINDING SITES; BRCA2 PROTEIN; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DNA; DNA-BINDING PROTEINS; HUMANS; MICROSCOPY, ELECTRON; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PYROCOCCUS FURIOSUS; RAD51 RECOMBINASE; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; PYROCOCCUS; PYROCOCCUS FURIOSUS;

EID: 0042738069     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg429     Document Type: Article

References (42)

1. 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.
2. 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.
3. Ariyoshi, M., Nishino, T., Iwasaki, H., Shinagawa, H. and Morikawa, K. (2000) Crystal structure of the Holliday junction DNA in complex with a single RuvA tetramer. Proc. Natl Acad. Sci. USA, 97, 8257-8262.
4. Benson, F.E., Stasiak, A. and West, S.C. (1994) Purification and characterization of the human Rad51 protein, an analogue of E.coli RecA. EMBO J., 13, 5764-5771.
5. Datta, S., Prabu, M.M., Vaze, M.B., Ganesh, N., Chandra, N.R., Muniyappa, K. and Vijayan, M. (2000) Crystal structures of Mycobacterium tuberculosis RecA and its complex with ADP-A1F(4): implications for decreased ATPase activity and molecular aggregation. Nucleic Acids Res., 28, 4964-4973.
6. Davies, A.A., Masson, J.Y., McIlwraith, M.J., Stasiak, A.Z., Stasiak, A., Venkitaraman, A.R. and West, S.C. (2001) Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol. Cell, 7, 273-282.
7. 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.
8. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol., 233, 123-138.
9. Holmes, V.F., Scandellari, F., Benjamin, K.R. and Cozzarelli, N.R. (2002) Structure of reaction intermediates formed during Saccharomyces cerevisiae Rad51-catalyzed strand transfer. J. Biol. Chem., 277, 38945-38953.
10. Kagawa, W., Kurumizaka, H., Ishitani, R., Fukai, S., Nureki, O., Shibata, T. and Yokoyama, S. (2002) Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol. Cell, 10, 359-371.
11. Khanna, K.K. and Jackson, S.P. (2001) DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet., 27, 247-254.
12. Komori, K., Miyata, T., DiRuggiero, J., Holley-Shanks, R., Hayashi, I., Cann, I.K., Mayanagi, K., Shinagawa, H. and Ishino, Y. (2000) Both RadA and RadB are involved in homologous recombination in Pyrococcus furiosus. J. Biol. Chem., 275, 33782-33790.
13. 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.
14. Lim, D.S. and Hasty, P. (1996) A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell Biol, 16, 7133-7143.
15. Ludtke, S.J., Baldwin, P.R. and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol., 128, 82-97.
16. Mazin, A.V., Alexeev, A.A. and Kowalczykowski, S.C. (2003) A novel function of RAD54 protein: Stabilization of the RAD51 nucleoprotein filament. J. Biol. Chem., 278, 14029-14036.
17. Nishinaka, T., Ito, Y., Yokoyama, S. and Shibata, T. (1997) An extended DNA structure through deoxyribose-base stacking induced by RecA protein. Proc. Natl Acad. Sci. USA, 94, 6623-6628.
18. Pellegrini, L., Yu, D.S., Lo, T., Anand, S., Lee, M., Blundell, T.L. and Venkitaraman, A.R. (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature, 420, 287-293.
19. Sawaya, M.R., Prasad, R., Wilson, S.H., Kraut, J. and Pelletier, H. (1997) Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry, 36, 11205-11215.
20. Singleton, M.R., Sawaya, M.R., Ellenberger, T. and Wigley, D.B. (2000) Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell, 101, 589-600.
21. Singleton, M.R., Wentzell, L.M., Liu, Y., West, S.C. and Wigley, D.B. (2002) Structure of the single-strand annealing domain of human RAD52 protein. Proc. Natl Acad. Sci. USA, 99, 13492-13497.
22. 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.
23. Sonoda, E., Sasaki, M.S., Buerstedde, J.M., Bezzubova, O., Shinohara, A., Ogawa, H., Takata, M., Yamaguchi-Iwai, Y. and Takeda, S. (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J., 17, 598-608.
24. Story, R.M. and Steitz, T.A. (1992) Structure of the recA protein-ADP complex. Nature, 355, 374-376.
25. 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.
26. Sugawara, N., Wang, X. and Haber, J.E. (2003) In vivo roles of Rad52, Rad54 and Rad55 proteins in Rad51-mediated recombination. Mol. Cell, in press.
27. 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.
28. Sugiyama, T., Zaitseva, E.M. and Kowalczykowski, 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.
29. 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.
30. 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.
31. Symington, L.S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev., 66, 630-670.
32. Thayer, M.M., Ahern, H., Xing, D., Cunningham, R.P. and Tainer, J.A. (1995) Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J., 14, 4108-4120.
33. Tombline, G. and Fishel, R. (2002) Biochemical characterization of the human RAD51 protein. I. ATP hydrolysis. J. Biol. Chem., 277, 14417-14425.
34. van Gent, D.C., Hoeijmakers, J.H. and Kanaar, R. (2001) Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet., 2, 196-206.
35. Van Komen, S., Petukhova, G., Sigurdsson, S. and Sung, P. (2002) Functional cross-talk among Rad51, Rad54 and replication protein A in heteroduplex DNA joint formation. J. Biol. Chem., 277, 43578-43587.
36. VanLoock, M.S., Yu, X., Yang, S., Lai, A.L., Low, C., Campbell, M.J. and Egelman, E.H. (2003) ATP-mediated conformational changes in the RecA filament. Structure, 11, 187-196.
37. Volkmann, N. and Hanein, D. (1999) Quantitative fitting of atomic models into observed densities derived by electron microscopy. J. Struct. Biol., 125, 176-184.
38. Yang, H. et al. (2002) BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science, 297, 1837-1848.
39. Yang, S., VanLoock, M.S., Yu, X. and Egelman, E.H. (2001a) Comparison of bacteriophage T4 UvsX and human Rad51 filaments suggests that RecA-like polymers may have evolved independently. J. Mol. Biol., 312, 999-1009.
40. Yang, S., Yu, X., Seitz, E.M., Kowalczykowski, S.C. and Egelman, E.H. (2001b) Archaeal RadA protein binds DNA as both helical filaments and octameric rings. J. Mol. Biol., 314, 1077-1085.
41. Yu, V.P., Koehler, M., Steinlein, C., Schmid, M., Hanakahi, L.A., van Gool, A.J., West, S.C. and Venkitaraman, A.R. (2000) Gross chromosomal rearrangements and genetic exchange between nonhomologous chromosomes following BRCA2 inactivation. Genes Dev., 14, 1400-1406.
42. 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, 8419-8424.