A recombinase paralog from the hyperthermophilic crenarchaeon Sulfolobus solfataricus enhances SsoRadA ssDNA binding and strand displacement

Gene

Volumn 515, Issue 1, 2013, Pages 128-139

  Graham, William J ^a   Haseltine, Cynthia A ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Archaea; ATPase; DNA binding; Recombination; Strand invasion

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PROTEIN; RECOMBINASE; SINGLE STRANDED DNA; SSORAL3 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHEMICAL ANALYSIS; CONCENTRATION (PARAMETERS); DNA BINDING; ENZYME ACTIVITY; FILAMENTOUS ALGA; HYPERTHERMOPHILIC ARCHAEON; NONHUMAN; PARALOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SULFOLOBUS SOLFATARICUS;

ADENOSINE TRIPHOSPHATASES; DNA, SINGLE-STRANDED; ENZYME ACTIVATION; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; PROTEIN BINDING; REC A RECOMBINASES; SULFOLOBUS SOLFATARICUS;

CRENARCHAEOTA; EUKARYOTA; SULFOLOBUS SOLFATARICUS;

EID: 84872266551     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2012.11.010     Document Type: Article

References (52)

1. Arenson T.A., Tsodikov O.V., Cox M.M. Quantitative analysis of the kinetics of end-dependent disassembly of RecA filaments from ssDNA. J. Mol. Biol. 1999, 288:391-401.
2. Braybrooke J.P., Spink K.G., Thacker J., Hickson I.D. The RAD51 family member, RAD51L3, is a DNA-stimulated ATPase that forms a complex with XRCC2. J. Biol. Chem. 2000, 275:29100-29106.
3. Bugreev D.V., Mazin A.V. Ca2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9988-9993.
4. Carreira A., Kowalczykowski S.C. Two classes of BRC repeats in BRCA2 promote RAD51 nucleoprotein filament function by distinct mechanisms. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10448-10453.
5. Forget A.L., Kowalczykowski S.C. Single-molecule imaging brings Rad51 nucleoprotein filaments into focus. Trends Cell Biol. 2010, 20:269-276.
6. Gasior S.L., Wong A.K., Kora Y., Shinohara A., Bishop D.K. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev. 1998, 12:2208-2221.
7. Hada M., Georgakilas A.G. Formation of clustered DNA damage after high-LET irradiation: a review. J. Radiat. Res. 2008, 49:203-210.
8. Haldenby S., White M.F., Allers T. RecA family proteins in archaea: RadA and its cousins. Biochem. Soc. Trans. 2009, 37:102-107.
9. Haseltine C.A., Kowalczykowski S.C. An archaeal Rad54 protein remodels DNA and stimulates DNA strand exchange by RadA. Nucleic Acids Res. 2009, 2757-2770.
10. Hays S.L., Firmenich A.A., Berg P. Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:6925-6929.
11. Johnson R.D., Symington L.S. Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol. Cell. Biol. 1995, 15:4843-4850.
12. Kurumizaka H., et al. Homologous-pairing activity of the human DNA-repair proteins Xrcc3 and Rad51C. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5538-5543.
13. Kurumizaka H., et al. Homologous pairing and ring and filament structure formation activities of the human Xrcc2*Rad51D complex. J. Biol. Chem. 2002, 277:14315-14320.
14. Lee M.H., et al. Self-polymerization of archaeal RadA protein into long and fine helical filaments. Biochem. Biophys. Res. Commun. 2004, 323:845-851.
15. Li X., et al. Rad51 and Rad54 ATPase activities are both required to modulate Rad51-dsDNA filament dynamics. Nucleic Acids Res. 2007, 35:4124-4140.
16. Lisby M., Barlow J.H., Burgess R.C., Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 2004, 118:699-713.
17. Liu J., Bond J.P., Morrical S.W. Mechanism of presynaptic filament stabilization by the bacteriophage T4 UvsY recombination mediator protein. Biochemistry 2006, 45:5493-5502.
18. Liu J., Ehmsen K.T., Heyer W.D., Morrical S.W. Presynaptic filament dynamics in homologous recombination and DNA repair. Crit. Rev. Biochem. Mol. Biol. 2011, 46:240-270.
19. Liu J., Renault L., Veaute X., Fabre F., Stahlberg H., Heyer W.D. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 2011, 479:245-248.
20. Masson J.Y., Stasiak A.Z., Stasiak A., Benson F.E., West S.C. Complex formation by the human RAD51C and XRCC3 recombination repair proteins. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8440-8446.
21. Masson J.Y., et al. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev. 2001, 15:3296-3307.
22. 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. 2000, 304:151-164.
23. McRobbie A.M., et al. Structural and functional characterisation of a conserved archaeal RadA paralog with antirecombinase activity. J. Mol. Biol. 2009, 389:661-673.
24. Miller K.A., Yoshikawa D.M., McConnell I.R., Clark R., Schild D., Albala J.S. RAD51C interacts with RAD51B and is central to a larger protein complex in vivo exclusive of RAD51. J. Biol. Chem. 2002, 277:8406-8411.
25. Mine J., Disseau L., Takahashi M., Cappello G., Dutreix M., Viovy J.L. Real-time measurements of the nucleation, growth and dissociation of single Rad51-DNA nucleoprotein filaments. Nucleic Acids Res. 2007, 35:7171-7187.
26. Morimatsu K., Kowalczykowski S.C. RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol. Cell 2003, 11:1337-1347.
27. New J.H., Sugiyama T., Zaitseva E., Kowalczykowski S.C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 1998, 391:407-410.
28. Pâques F., Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 1999, 63:349-404.
29. Price L.B., Shand R.F. Halocin S8: a 36-amino-acid microhalocin from the haloarchaeal strain S8a. J. Bacteriol. 2000, 182:4951-4958.
30. Robertson R.B., et al. Visualizing the disassembly of S. cerevisiae Rad51 nucleoprotein filaments. J. Mol. Biol. 2009, 388:703-720.
31. Rolfsmeier M.L., Haseltine C.A. The single-stranded DNA binding protein of Sulfolobus solfataricus acts in the presynaptic step of homologous recombination. J. Mol. Biol. 2010, 397:31-45.
32. Rolfsmeier M.L., Laughery M.F., Haseltine C.A. Repair of DNA double-strand breaks following UV damage in three Sulfolobus solfataricus strains. J. Bacteriol. 2010, 192:4954-4962.
33. Rolfsmeier M.L., Laughery M.F., Haseltine C.A. Repair of DNA double-strand breaks induced by ionizing radiation damage correlates with upregulation of homologous recombination genes in Sulfolobus solfataricus. J. Mol. Biol. 2011, 414:485-498.
34. Schild D., Lio Y.C., Collins D.W., Tsomondo T., Chen D.J. Evidence for simultaneous protein interactions between human Rad51 paralogs. J. Biol. Chem. 2000, 275:16443-16449.
35. Seitz E.M., Brockman J.P., Sandler S.J., Clark A.J., Kowalczykowski S.C. RadA protein is an archaeal RecA protein homolog that catalyzes DNA strand exchange. Genes Dev. 1998, 12:1248-1253.
36. Seybert A., Scott D.J., Scaife S., Singleton M.R., Wigley D.B. Biochemical characterisation of the clamp/clamp loader proteins from the euryarchaeon Archaeoglobus fulgidus. Nucleic Acids Res. 2002, 30:4329-4338.
37. Shibata T., DasGupta C., Cunningham R.P., Radding C.M. Purified Escherichia coli recA protein catalyzes homologous pairing of superhelical DNA and single-stranded fragments. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:1638-1642.
38. Shibata T., Ohtani T., Iwabuchi M., Ando T. D-loop cycle. A circular reaction sequence which comprises formation and dissociation of D-loops and inactivation and reactivation of superhelical closed circular DNA promoted by recA protein of Escherichia coli. J. Biol. Chem. 1982, 257:13981-13986.
39. Shibata T., et al. Homologous genetic recombination as an intrinsic dynamic property of a DNA structure induced by RecA/Rad51-family proteins: a possible advantage of DNA over RNA as genomic material. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8425-8432.
40. Shikazono N., Noguchi M., Fujii K., Urushibara A., Yokoya A. The yield, processing, and biological consequences of clustered DNA damage induced by ionizing radiation. J. Radiat. Res. 2009, 50:27-36.
41. 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. 2001, 15:3308-3318.
42. Sugiyama T., Kowalczykowski S.C. 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. 2002, 277:31663-31672.
43. Sung P. Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev. 1997, 11:1111-1121.
44. Sung P., Trujillo K.M., Van Komen S. Recombination factors of Saccharomyces cerevisiae. Mutat. Res. 2000, 451:257-275.
45. Sweezy M.A., Morrical S.W. Single-stranded DNA binding properties of the uvsY recombination protein of bacteriophage T4. J. Mol. Biol. 1997, 266:927-938.
46. Takata M., et al. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 2001, 21:2858-2866.
47. Wang L., et al. Sulfolobus tokodaii RadA paralog, stRadC2, is involved in DNA recombination via interaction with RadA and Hjc. Sci. China Life Sci. 2012, 55:261-267.
48. Ward J.F. Biochemistry of DNA lesions. Radiat. Res. Suppl. 1985, 8:S103-S111.
49. Wiese C., Collins D.W., Albala J.S., Thompson L.H., Kronenberg A., Schild D. Interactions involving the Rad51 paralogs Rad51C and XRCC3 in human cells. Nucleic Acids Res. 2002, 30:1001-1008.
50. Wu Y., Kantake N., Sugiyama T., Kowalczykowski S.C. Rad51 protein controls Rad52-mediated DNA annealing. J. Biol. Chem. 2008, 283:14883-14892.
51. Yang S., Yu X., Seitz E.M., Kowalczykowski S.C., Egelman E.H. Archaeal RadA protein binds DNA as both helical filaments and octameric rings. J. Mol. Biol. 2001, 314:1077-1085.
52. Yassa D.S., Chou K.M., Morrical S.W. Characterization of an amino-terminal fragment of the bacteriophage T4 uvsY recombination protein. Biochimie 1997, 79:275-285.