Disparate requirements for the Walker A and B ATPase motifs of human RAD51D in homologous recombination

Nucleic Acids Research

Volumn 34, Issue 9, 2006, Pages 2833-2843

  Wiese, Claudia ^b   Hinz, John M ^a   Tebbs, Robert S ^a   Nham, Peter B ^a   Urbin, Salustra S ^a   Collins, David W ^b   Thompson, Larry H ^a   Schild, David ^b  

^a LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; MUTANT PROTEIN; NUCLEIC ACID BINDING PROTEIN; RAD51 PROTEIN; RAD51C PROTEIN; RAD51D PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; WALKER A ADENOSINE TRIPHOSPHATASE; WALKER B ADENOSINE TRIPHOSPHATASE; XRCC2 PROTEIN; DNA BINDING PROTEIN; RAD51L3 PROTEIN, HUMAN;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; BINDING SITE; CELL SURVIVAL; CHO CELL; CONTROLLED STUDY; DNA CROSS LINKING; GENETIC COMPLEMENTATION; GENETIC TRANSFECTION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; PARALOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PURIFICATION; SEQUENCE HOMOLOGY; TWO HYBRID SYSTEM; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CRICETULUS; DNA DAMAGE; DNA REPAIR; GENETIC RECOMBINATION; GENETICS; HAMSTER; METABOLISM; MOLECULAR GENETICS; MUTATION;

CRICETINAE; VERTEBRATA;

ADENOSINE TRIPHOSPHATASES; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; GENETIC COMPLEMENTATION TEST; HUMANS; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; MUTATION; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 33744795195     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl366     Document Type: Article

References (55)

1. Helleday,T. (2003) Pathways for mitotic homologous recombination in mammalian cells. Mutat. Res., 532, 103-115.
2. Hinz,J.M., Tebbs,R.S., Wilson,P.F., Nham,P.B., Salazar,E.P., Nagasawa,H., Urbin,S.S., Bedford,J.S. and Thompson,L.H. (2006) Repression of mutagenesis by Rad51D-mediated homologous recombination. Nucleic Acids Res., 34, 1358-1368.
3. Rothkamm,K., Kruger,I., Thompson,L.H. and Lobrich,M. (2003) Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol., 23, 5706-5715.
4. Sigurdsson,S., Van Komen,S., Bussen,W., Schild,D., Albala,J.S. and Sung,P. (2001) Mediator function of the human Rad51B-Rad51C complex in Rad51/RPA-catalyzed DNA strand exchange. Genes Dev., 15, 3308-3318.
5. Forget,A.L., Bennett,B.T. and Knight,K.L. (2004) Xrcc3 is recruited to DNA double strand breaks early and independent of Rad51. J. Cell Biochem., 93, 429-436.
6. Hatanaka,A., Yamazoe,M., Sale,J.E., Takata,M., Yamamoto,K., Kitao,H., Sonoda,E., Kikuchi,K., Yonetani,Y. and Takeda,S. (2005) Similar effects of Brca2 truncation and Rad51 paralog deficiency on immunoglobulin V gene diversification in DT40 cells support an early role for Rad51 paralogs in homologous recombination. Mol. Cell. Biol., 25, 1124-1134.
7. Rodrigue,A., Lafrance,M., Gauthier,M.C., McDonald,D., Hendzel,M., West,S.C., Jasin,M. and Masson,J.Y. (2006) Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J., 25, 222-231.
8. Liu,Y., Masson,J.Y., Shah,R., O'Regan,P. and West,S.C. (2004) RAD51C is required for Holliday junction processing in mammalian cells. Science, 303, 243-246.
9. Braybrooke,J.P., Li,J.L., Wu,L., Caple,F., Benson,F.E. and Hickson,I.D. (2003) Functional interaction between the Bloom's syndrome helicase and the RAD51 paralog, RAD51L3 (RAD51D). J. Biol. Chem., 278, 48357-48366.
10. Brenneman,M.A., Wagener,B.M., Miller,C.A., Allen,C. and Nickoloff,J.A. (2002) XRCC3 controls the fidelity of homologous recombination: Roles for XRCC3 in late stages of recombination. Mol. Cell, 10, 387-395.
11. Yonetani,Y., Hochegger,H., Sonoda,E., Shinya,S., Yoshikawa,H., Takeda,S. and Yamazoe,M. (2005) Differential and collaborative actions of Rad51 paralog proteins in cellular response to DNA damage. Nucleic Acids Res., 33, 4544-4552.
12. Thacker,J. (1999) A surfeit of RAD51-like genes? Trends Genet., 15, 166-168.
13. Thompson,L.H. and Schild,D. (1999) The contribution of homologous recombination in preserving genome integrity in mammalian cells. Biochimie., 81, 87-105.
14. Takata,M., Sasaki,M.S., Tachiiri,S., Fukushima,T., Sonoda,E., Schild,D., Thompson,L.H. and Takeda,S. (2001) Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol., 21, 2858-2866.
15. Thacker,J. (2005) The RAD51 gene family, genetic instability and cancer. Cancer Lett., 219, 125-135.
16. Thompson,L.H. and Schild,D. (2001) Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutat Res., 477, 131-153.
17. Braybrooke,J.P., Spink,K.G., Thacker,J. and Hickson,I.D. (2000) The RAD51 family member, RAD51L3, is a DNA-stimulated ATPase that forms a complex with XRCC2. J. Biol. Chem., 275, 29100-29106.
18. Kurumizaka,H., Ikawa,S., Nakada,M., Eda,K., Kagawa,W., Takata,M., Takeda,S., Yokoyama,S. and Shibata,T. (2001) Homologous-pairing activity of the human DNA-repair proteins Xrcc3.Rad51C. Proc. Natl Acad Sci USA, 98, 5538-5543.
19. Kurumizaka,H., Ikawa,S., Nakada,M., Enomoto,R., Kagawa,W., Kinebuchi,T., Yamazoe,M., Yokoyama,S. and Shibata,T. (2002) Homologous pairing and ring and filament structure formation activities of the human Xrcc2*Rad51D complex. J. Biol. Chem., 277, 14315-14320.
20. Liu,N., Schild,D., Thelen,M.P. and Thompson,L.H. (2002) Involvement of Rad51C in two distinct protein complexes of Rad51 paralogs in human cells. Nucleic Acids Res., 30, 1009-1015.
21. Miller,K.A., Yoshikawa,D.M., McConnell,I.R., Clark,R., Schild,D. and Albala,J.S. (2002) RAD51C interacts with RAD51B and is central to a larger protein complex in vivo exclusive of RAD51. J. Biol. Chem., 277, 8406-8411.
22. Wiese,C., Collins,D.W., Albala,J.S., Thompson,L.H., Kronenberg,A. and Schild,D. (2002) Interactions involving the Rad51 paralogs Rad51C and XRCC3 in human cells. Nucleic Acids Res., 30, 1001-1008.
23. Masson,J.Y., Stasiak,A.Z., Stasiak,A., Benson,F.E. and West,S.C. (2001) Complex formation by the human RAD51C and XRCC3 recombination repair proteins. Proc. Natl Acad Sci USA, 98, 8440-8446.
24. Masson,J.Y., Tarsounas,M.C., Stasiak,A.Z., Stasiak,A., Shah,R., McIlwraith,M.J., Benson,F.E. and West,S.C. (2001) Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev., 15, 3296-3307.
25. Lio,Y.C., Mazin,A.V., Kowalczykowski,S.C. and Chen,D.J. (2003) Complex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro. J. Biol. Chem., 278, 2469-2478.
26. Shim,K.S., Schmutte,C., Tombline,G., Heinen,C.D. and Fishel,R. (2004) hXRCC2 enhances ADP/ATP processing and strand exchange by hRAD51. J. Biol. Chem., 279, 30385-30394.
27. Yokoyama,H., Sarai,N., Kagawa,W., Enomoto,R., Shibata,T., Kurumizaka,H. and Yokoyama,S. (2004) Preferential binding to branched DNA strands and strand-annealing activity of the human Rad51B, Rad51C, Rad51D and Xrcc2 protein complex. Nucleic Acids Res., 32, 2556-2565.
28. Walker,J.E., Saraste,M., Runswick,M.J. and Gay,N.J. (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J., 1, 945-951.
29. 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.
30. Bell,C.E. (2005) Structure and mechanism of Escherichia coli RecA ATPase. Mol. Microbiol., 58, 358-366.
31. Morrison,C., Shinohara,A., Sonoda,E., Yamaguchi-Iwai,Y., Takata,M., Weichselbaum,R.R. and Takeda,S. (1999) The essential functions of human Rad51 are independent of ATP hydrolysis. Mol. Cell. Biol., 19, 6891-6897.
32. 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 (Amst), 5, 381-391.
33. Stark,J.M., Hu,P., Pierce,A.J., Moynahan,M.E., Ellis,N. and Jasin,M. (2002) ATP hydrolysis by mammalian RAD51 has a key role during homology-directed DNA repair. J. Biol. Chem., 277, 20185-20194.
34. French,C.A., Tambini,C.E. and Thacker,J. (2003) Identification of functional domains in the RAD51L2 (RAD51C) protein and its requirement for gene conversion. J. Biol. Chem., 278, 45445-45450.
35. Yamada,N.A., Hinz,J.M., Kopf,V.L., Segalle,K.D. and Thompson,L.H. (2004) XRCC3 ATPase activity is required for normal XRCC3-Rad51C complex dynamics and homologous recombination. J. Biol. Chem., 279, 23250-23254.
36. O'Regan,P., Wilson,C., Townsend,S. and Thacker,J. (2001) XRCC2 is a nuclear RAD51-like protein required for damage-dependent RAD51 focus formation without the need for ATP binding. J. Biol. Chem., 276, 22148-22153.
37. Rafii,S., Lindblom,A., Reed,M., Meuth,M. and Cox,A. (2003) A naturally occurring mutation in an ATP-binding domain of the recombination repair gene XRCC3 ablates its function without causing cancer susceptibility. Hum. Mol. Genet., 12, 915-923.
38. Lindh,A.R., Rafii,S., Schultz,N., Cox,A. and Helleday,T. (2006) Mitotic defects in XRCC3 variants T241M and D213N and their relation to cancer susceptibility. Hum. Mol. Genet., 15, 1217-1224.
39. Gruver,A.M., Miller,K.A., Rajesh,C., Smiraldo,P.G., Kaliyaperumal,S., Balder,R., Stiles,K.M., Albala,J.S. and Pittman,D.L.The ATPase motif in RAD51D is required for resistance to DNA interstrand crosslinking agents and interaction with RAD51C. Mutagenesis, 20, 433-440.
40. Schild,D., Lio,Y.C., Collins,D.W., Tsomondo,T. and Chen,D.J. (2000) Evidence for simultaneous protein interactions between human Rad51 paralogs. J. Biol. Chem., 275, 16443-16449.
41. Fields,S. (1993) The two-hybrid system to detect protein-protein interactions. Methods, 5, 116-124.
42. Vernet,T., Dignard,D. and Thomas,D.Y. (1987) A family of yeast expression vectors containing the phage f1 intergenic region. Gene, 52, 225-233.
43. Bartel,P.L. and Fields,S. (1995) Analyzing protein-protein interactions using two-hybrid system. Meth. Enzymol., 254, 241-263.
44. Hoffman,G.A., Garrison,T.R. and Dohlman,H.G. (2002) Analysis of RGS proteins in Saccharomyces cerevisiae. Meth. Enzymol., 344, 617-631.
45. van den Hoff,M.J., Moorman,A.F. and Lamers,W.H. (1992) Electroporation in 'intracellular' buffer increases cell survival. Nucleic Acids Res., 20, 2902.
46. Khasanov,F.K., Salakhova,A.F., Chepurnaja,O.V., Korolev,V.G. and Bashkirov,V.I. (2004) Identification and characterization of the rlp1+, the novel Rad51 paralog in the fission yeast Schizosaccharomyces pombe. DNA Repair (Amst), 3, 1363-1374.
47. 2-phase cells. J. Biol. Chem., 279, 42313-42320.
48. Xu,Z.Y., Loignon,M., Han,F.Y., Panasci,L. and Aloyz,R. (2005) Xrcc3 induces cisplatin resistance by stimulation of Rad51-related recombinational repair, S-phase checkpoint activation, and reduced apoptosis. J. Pharmacol Exp. Ther., 314, 495-505.
49. Shin,D.S., Chahwan,C., Huffman,J.L. and Tainer,J.A. (2004) Structure and function of the double-strand break repair machinery. DNA Repair (Amst), 3, 863-873.
50. Wu,Y., He,Y., Moya,I.A., Qian,X. and Luo,Y. (2004) Crystal structure of archaeal recombinase RADA: A snapshot of its extended conformation. Mol. Cell, 15, 423-435.
51. 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.
52. Qian,X., Wu,Y., He,Y. and Luo,Y. (2005) Crystal structure of Methanococcus voltae RadA in complex with ADP: Hydrolysis-induced conformational change. Biochemistry, 44, 13753-13761.
53. Shin,D.S., Pellegrini,L., Daniels,D.S., Yelent,B., Craig,L., Bates,D., Yu,D.S., Shivji,M.K., Hitomi,C., Arvai,A.S. et al. (2003) Full-length archaeal Rad51 structure and mutants: Mechanisms for RAD51 assembly and control by BRCA2. EMBO J., 22, 4566-4576.
54. 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.
55. 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 (Camb), 11, 187-196.