Conformational changes modulate the activity of human RAD51 protein

Journal of Molecular Biology

Volumn 337, Issue 4, 2004, Pages 817-827

  Liu, Yilun ^a   Stasiak, Alicja Z ^b   Masson, Jean Yves ^a,c   McIlwraith, Michael J ^a   Stasiak, Andrzej ^b   West, Stephen C ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c LAVAL UNIVERSITY   (Canada)

Author keywords

DSB, double strand break; DsDNA, double stranded DNA; HR, homologous recombination; RecA; Recombination; Repair; ssDNA, single stranded DNA; Strand exchange

Indexed keywords

DOUBLE STRANDED DNA; NAKED DNA; RAD51 PROTEIN; RECA PROTEIN; SINGLE STRANDED DNA;

AMINO ACID SEQUENCE; ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; IONIC STRENGTH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

EID: 1642264199     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.02.022     Document Type: Article

References (48)

1. van Gent D.C., Hoeijmakers J.H., Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nature Rev. Genet. 2:2001;196-206.
2. West S.C. Molecular views of recombination proteins and their control. Nature Rev. Mol. Cell Biol. 4:2003;1-11.
3. Benson F.E., Stasiak A., West S.C. Purification and characterisation of the human RAD51 protein, an analogue of E. coli RecA. EMBO J. 13:1994;5764-5771.
4. Baumann P., Benson F.E., West S.C. Human RAD51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell. 87:1996;757-766.
5. Tsuzuki T., Fujii Y., Sakuma K., Tominaga Y., Nakao K., Sekiguchi M., et al. Targeted disruption of the RAD51 gene leads to lethality in embryonic mice. Proc. Natl Acad. Sci. USA. 93:1996;6236-6240.
6. Sonoda E., Sasaki M.S., Buerstedde J.M., Bezzubova O., Shinohara A., Ogawa H., et al. RAD51 deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17:1998;598-608.
7. West S.C. Enzymes and molecular mechanisms of homologous recombination. Annu. Rev. Biochem. 61:1992;603-640.
8. Kowalczykowski S.C., Eggleston A.K. Homologous pairing and DNA strand-exchange proteins. Annu. Rev. Biochem. 63:1994;991-1043.
9. Roca A.I., Cox M.M. RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucl. Acid Res. Mol. Biol. 56:1997;129-222.
10. Baumann P., West S.C. The human RAD51 protein: polarity of strand transfer and stimulation by hRP-A. EMBO J. 16:1997;5198-5206.
11. Benson F.E., Baumann P., West S.C. Synergistic actions of RAD51 and RAD52 in genetic recombination and DNA repair. Nature. 391:1998;401-404.
12. McIlwraith M.J., Van Dyck E., Masson J.-Y., Stasiak A.Z., Stasiak A., West S.C. Reconstitution of the strand invasion step of double-strand break repair using human RAD51, RAD52 and RPA proteins. J. Mol. Biol. 304:2000;151-164.
13. Sigurdsson S., Van Komen S., Bussen W., Schild D., Albala J.S., Sung P. Mediator function of the human RAD51B-RAD51C complex in RAD51/RPA-catalyzed DNA strand-exchange. Genes Dev. 15:2001;3308-3318.
14. Sigurdsson S., Van Komen S., Petukhovan G., Sung P. Homologous DNA pairing by human recombination factors RAD51 and RAD54. J. Biol. Chem. 277:2002;42790-42794.
15. Sigurdsson S., Trujillo K., Song B.W., Stratton S., Sung P. Basis for avid homologous DNA strand-exchange by human RAD51 and RPA. J. Biol. Chem. 276:2001;8798-8806.
16. Cox M.M., Lehman I.R. Enzymes of genetic recombination. Annu. Rev. Biochem. 56:1987;229-262.
17. Sung P. Catalysis of ATP-dependent homologous DNA pairing and strand-exchange by yeast RAD51 protein. Science. 265:1994;1241-1243.
18. Flory J., Tsang S.S., Muniyappa K., Bianchi M., Gonda D., Kahn R., et al. Intermediates in homologous pairing promoted by RecA protein and correlations of recombination in vitro and in vivo. Cold Spring Harbor Symp. Quant. Biol. 49:1984;513-523.
19. Tsang S.S., Chow S.A., Radding C.M. Networks of DNA and RecA protein are intermediates in homologous pairing. Biochemistry. 24:1985;3226-3232.
20. Chow S.A., Radding C.M. Ionic inhibition of formation of RecA nucleoprotein networks blocks homologous pairing. Proc. Natl Acad. Sci. USA. 82:1985;5646-5650.
21. Yu X., Jacobs S.A., West S.C., Ogawa T., Egelman E.H. Domain structure and dynamics in the helical filaments formed by RecA and RAD51 on DNA. Proc. Natl Acad. Sci. USA. 98:2001;8419-8424.
22. Stasiak A., DiCapua E., Koller T. Elongation of duplex DNA by RecA protein. J. Mol. Biol. 151:1981;557-564.
23. Stasiak A., DiCapua E. The helicity of DNA in complexes with RecA protein. Nature. 299:1982;185-186.
24. DiCapua E., Engel A., Stasiak A., Koller T. Characterization of complexes between RecA protein and duplex DNA by electron microscopy. J. Mol. Biol. 157:1982;87-103.
25. Yu X., Egelman E.H. Structural data suggest that the active and inactive forms of the RecA filament are not simply interconvertible. J. Mol. Biol. 227:1992;334-346.
26. Rice K.P., Eggler A.L., Sung P., Cox M.M. 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. 276:2001;38570-38581.
27. Soltis D.A., Lehman I.R. RecA protein-promoted DNA strand-exchange. Effect of ionic strength. J. Biol. Chem. 259:1984;12020-12024.
28. Kowalczykowski S.C. Biochemistry of genetic recombination: energetics and mechanism of DNA strand-exchange. Annu. Rev. Biophys. Biophys. Chem. 20:1991;539-575.
29. Howard-Flanders P., West S.C., Cassuto E., Han T.R., Egelman E. Structure of RecA spiral filaments and their role in homologous pairing and strand-exchange in genetic recombination. Kelly T., McMacken R. Mechanisms of DNA replication and recombination. UCLA Symposium on Molecular and Cellular Biology, New Series. Mechanisms of DNA replication and recombination. UCLA Symposium on Molecular and Cellular Biology, New Series. vol. 47:1987;609-617 Liss, New York.
30. Sung P., 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.
31. Zaitseva E.M., Zaitsev E.N., Kowalczykowski S.C. The DNA binding properties of Saccharomyces cerevisiae RAD51 protein. J. Biol. Chem. 274:1999;2907-2915.
32. Baumann P., West S.C. Heteroduplex formation by human RAD51 protein: effects of DNA end-structure, hRP-A and hRAD52. J. Mol. Biol. 291:1999;363-374.
33. Flory J., Radding C.M. Visualization of RecA protein and its association with DNA: a priming effect of single-strand-binding protein. Cell. 28:1982;747-756.
34. Dombroski D.F., Scraba D.G., Bradley R.D., Morgan A.R. Studies of the interaction of RecA protein with DNA. Nucl. Acids Res. 11:1983;7487-7516.
35. Heuser J., Griffith J. Visualization of RecA protein and its complexes with DNA by quick-freeze/deep etch electron microscopy. J. Mol. Biol. 210:1989;473-484.
36. Stasiak A., Stasiak A.Z., Koller T. Visualization of RecA-DNA complexes involved in consecutive stages of an in vitro strand-exchange reaction. Cold Spring Harbor Symp. Quant. Biol. 49:1984;561-570.
37. Howard-Flanders P., West S.C., Stasiak A.J. Role of RecA spiral filaments in genetic recombination. Nature. 309:1984;215-220.
38. Register J.C., Christiansen G., Griffith J. Electron microscopic visualization of the RecA-mediated pairing and branch migration phases of DNA strand-exchange. J. Biol. Chem. 262:1987;12812-12820.
39. Yu X., Egelman E.H. Direct visualization of dynamics and cooperative conformational changes within RecA filaments that appear to be associated with the hydrolysis of adenosine 5′-O-(3-thiotriphosphate). J. Mol. Biol. 225:1992;193-216.
40. Ogawa T., Yu X., Shinohara A., Egelman E.H. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science. 259:1993;1896-1899.
41. Chen G., Yuan S.S.Y., Liu W., Xu Y., Trujillo K., Song B., et al. Radiation-induced assembly of RAD51 and RAD52 recombination complex requires ATP and c-Abl. J. Biol. Chem. 274:1999;12748-12752.
42. Slupianek A., Schmutte C., Tombline G., Nieborowska-Skorska M., Hoser G., Nowicki M.O., et al. BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol. Cell. 8:2001;795-806.
43. Eggleston A.K., Mitchell A.H., West S.C. In vitro reconstitution of the late steps of genetic recombination in E. coli. Cell. 89:1997;607-617.
44. Baumann P., Benson F.E., Hajibagheri N., West S.C. Purification of human RAD51 protein by selective spermidine precipitation. Mutat. Res. DNA Repair. 384:1997;65-72.
45. Brill S.J., Stillman B. Yeast replication factor-A functions in the unwinding of the SV40 origin of DNA replication. Nature. 342:1989;92-95.
46. Henricksen L.A., Umbricht C.B., Wold M.S. Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem. 269:1994;11121-11132.
47. Kiltie A.E., Ryan A.J. SYBR Green I staining of pulsed field agarose gels is a sensitive and inexpensive way of quantitating DNA double-strand breaks in mammalian cells. Nucl. Acids Res. 25:1997;2945-2946.
48. Sogo J., Stasiak A., De Bernadin W., Losa R., Koller T. Negative staining of proteins and filaments. Sommerville J., Scheer U. Electron Microscopy in Molecular Biology. 1987;61-79 IRL Press, Oxford.