The HsRAD51B-HsRAD51C stabilizes the HsRAD51 nucleoprotein filament

DNA Repair

Volumn 12, Issue 9, 2013, Pages 723-732

  Amunugama, Ravindra ^a   Groden, Joanna ^a   Fishel, Richard ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

ATPase, Bloom's syndrome; BLM; Homologous recombination; RAD51 paralogs

Indexed keywords

BLOOM SYNDROME HELICASE; DOUBLE STRANDED DNA; HSRAD51 PROTEIN; HSRAD51B PROTEIN; HSRAD51C PROTEIN; RAD51 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; NONHUMAN; NUCLEOPROTEIN FILAMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

ATPASE, BLOOM'S SYNDROME; BLM; HOMOLOGOUS RECOMBINATION; RAD51 PARALOGS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DNA, SINGLE-STRANDED; DNA, SUPERHELICAL; DNA-BINDING PROTEINS; HOMOLOGOUS RECOMBINATION; HUMANS; MODELS, MOLECULAR; NUCLEOPROTEINS; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RAD51 RECOMBINASE; RECQ HELICASES; REPLICATION PROTEIN A; SF9 CELLS; SPODOPTERA; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84880950728     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.05.005     Document Type: Article

References (88)

1. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell. 2010, 40:179-204.
2. Krogh B.O., Symington L.S. Recombination proteins in yeast. Annu. Rev. Genet. 2004, 38:233-271.
3. Symington L.S. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 2002, 66:630-670.
4. San Filippo J., Sung P., Klein H. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 2008, 77:229-257.
5. Tarsounas M., Davies D., West S.C. BRCA2-dependent and independent formation of RAD51 nuclear foci. Oncogene 2003, 22:1115-1123.
6. Shim K.S., Schmutte C., Yoder K., Fishel R. Defining the salt effect on human RAD51 activities. DNA Repair (Amst) 2006, 5:718-730.
7. Liu Y., Stasiak A.Z., Masson J.Y., McIlwraith M.J., Stasiak A., West S.C. Conformational changes modulate the activity of human RAD51 protein. J. Mol. Biol. 2004, 337:817-827.
8. Heyer W.D., Ehmsen K.T., Liu J. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 2010, 44:113-139.
9. Lin Z., Kong H., Nei M., Ma H. Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. P. Natl. Acad. Sci. U.S.A. 2006, 103:10328-10333.
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. P. Natl. Acad. Sci. 1995, 92:6925-6929.
11. Johnson R., Symington L. Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol. Cell. Biol. 1995, 15:4843-4850.
12. Fortin G.S., Symington L.S. 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. 2002, 21:3160-3170.
13. 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.
14. 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.
15. Thompson L.H., Schild D. The contribution of homologous recombination in preserving genome integrity in mammalian cells. Biochimie 1999, 81:87-105.
16. Pittman D.L., Weinberg L.R., Schimenti J.C. Characterization, identification, and genetic mapping ofRad51d, a new mouse and humanRAD51/RecA-related gene. Genomics 1998, 49:103-111.
17. Dosanjh M.K., Collins D.W., Schild D., Fan W., Lennon G.G., Albala J.S., Shen Z. Isolation and characterization of RAD51C, a new human member of the RAD51 family of related genes. Nucleic Acids Res. 1998, 26:1179-1184.
18. Cartwright R., Dunn A.M., Simpson P.J., Tambini C.E., Thacker J. Isolation of novel human and mouse genes of the recA/RAD51 recombination-repair gene family. Nucleic Acids Res. 1998, 26:1653-1659.
19. Rice M.C., Smith S.T., Bullrich F., Havre P., Kmiec E.B. Isolation of human and mouse genes based on homology to REC2, a recombinational repair gene from the fungus Ustilago maydis. P. Natl. Acad. Sci. 1997, 94:7417-7422.
20. Albala J.S., Thelen M.P., Prange C., Fan W., Christensen M., Thompson L.H., Lennon G.G. Identification of a novel humanRAD51Homolog, RAD51B. Genomics 1997, 46:476-479.
21. Shim K.S., Schmutte C., Tombline G., Heinen C.D., Fishel R. hXRCC2 enhances ADP/ATP processing and strand exchange by hRAD51. J. Biol. Chem. 2004, 279:30385-30394.
22. Lio Y.C., Mazin A.V., Kowalczykowski S.C., Chen D.J. Complex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro. J. Biol. Chem. 2003, 278:2469-2478.
23. 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.
24. 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.
25. 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.
26. Liu N., Lamerdin J.E., Tebbs R.S., Schild D., Tucker J.D., Shen M.R., Brookman K.W., Siciliano M.J., Walter C.A., Fan W., Narayana L.S., Zhou Z.Q., Adamson A.W., Sorensen K.J., Chen D.J., Jones N.J., Thompson L.H. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol. Cell 1998, 1:783-793.
27. Tebbs R.S., Zhao Y., Tucker J.D., Scheerer J.B., Siciliano M.J., Hwang M., Liu N., Legerski R.J., Thompson L.H. Correction of chromosomal instability and sensitivity to diverse mutagens by a cloned cDNA of the XRCC3 DNA repair gene. P. Natl. Acad. Sci. 1995, 92:6354-6358.
28. Griffin C.S., Simpson P.J., Wilson C.R., Thacker J. Mammalian recombination-repair genes XRCC2 and XRCC3 promote correct chromosome segregation. Nat. Cell. Biol. 2000, 2:757-761.
29. Cui X., Brenneman M., Meyne J., Oshimura M., Goodwin E.H., Chen D.J. The XRCC2 and XRCC3 repair genes are required for chromosome stability in mammalian cells. Mutat. Res. 1999, 434:75-88.
30. Deans B., Griffin C.S., Maconochie M., Thacker J. Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice. EMBO J. 2000, 19:6675-6685.
31. Pittman D.L., Schimenti J.C. Midgestation lethality in mice deficient for the RecA-related gene Rad51d/Rad51l3,. Genesis 2000, 26:167-173.
32. Shu Z., Smith S., Wang L., Rice M.C., Kmiec E.B. Disruption of muREC2/RAD51L1 in mice results in early embryonic lethality which can be partially rescued in a p53-/- background. Mol. Cell. Biol. 1999, 19:8686-8693.
33. Sonoda E., Sasaki M.S., Buerstedde J.M., Bezzubova O., Shinohara A., Ogawa H., Takata M., Yamaguchi-Iwai Y., Takeda S. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 1998, 17:598-608.
34. Tsuzuki T., Fujii Y., Sakumi K., Tominaga Y., Nakao K., Sekiguchi M., Matsushiro A., Yoshimura Y., Morita T. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. P. Natl. Acad. Sci. U.S.A. 1996, 93:6236-6240.
35. Schoenmakers E.F.P.M., Huysmans C., Van de Ven Allelic W.J.M. Knockout of novel splice variants of human recombination repair gene RAD51B in t(12;14) uterine leiomyomas. Cancer Res. 1999, 59:19-23.
36. Ingraham S.E., Lynch R.A., Kathiresan S., Buckler A.J., Menon A.G. hREC2, a RAD51-like gene, is disrupted by t(12;14)(q15;q24.1) in a uterine leiomyoma. Cancer Genet. Cytogen. 1999, 115:56-61.
37. Meindl A., Hellebrand H., Wiek C., Erven V., Wappenschmidt B., Niederacher D., Freund M., Lichtner P., Hartmann L., Schaal H., Ramser J., Honisch E., Kubisch C., Wichmann H.E., Kast K., Deiszler H., Engel C., Muller-Myhsok B., Neveling K., Kiechle M., Mathew C.G., Schindler D., Schmutzler R.K., Hanenberg H. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat. Genet. 2010, 42:410-414.
38. Vaz F., Hanenberg H., Schuster B., Barker K., Wiek C., Erven V., Neveling K., Endt D., Kesterton I., Autore F., Fraternali F., Freund M., Hartmann L., Grimwade D., Roberts R.G., Schaal H., Mohammed S., Rahman N., Schindler D., Mathew C.G. Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat. Genet. 2010, 42:406-409.
39. Levy-Lahad E. Fanconi anemia and breast cancer susceptibility meet again. Nat. Genet. 2010, 42:368-369.
40. Kee Y., D'Andrea A.D. Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev. 2010, 24:1680-1694.
41. 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. P. Natl. Acad. Sci. U.S.A. 2001, 98:8440-8446.
42. Masson J.Y., Tarsounas M.C., Stasiak A.Z., Stasiak A., Shah R., McIlwraith M.J., Benson F.E., West S.C. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev. 2001, 15:3296-3307.
43. Compton S.A., Özgür S., Griffith J.D. Ring-shaped Rad51 paralog protein complexes bind holliday junctions and replication forks as visualized by electron microscopy. J. Biol. Chem. 2010, 285:13349-13356.
44. Chen Z., Yang H., Pavletich N.P. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 2008, 453. 489-484.
45. Qian X., He Y., Wu Y., Luo Y. Asp302 determines potassium dependence of a RadA recombinase from Methanococcus voltae. J. Mol. Biol. 2006, 360:537-547.
46. Wu Y., He Y., Moya I.A., Qian X., Luo Y. Crystal structure of archaeal recombinase RADA: a snapshot of its extended conformation. Mol. Cell 2004, 15:423-435.
47. Wu Y., Qian X., He Y., Moya I.A., Luo Y. Crystal structure of an ATPase-active form of Rad51 homolog from Methanococcus voltae. Insights into potassium dependence. J. Biol. Chem. 2005, 280:722-728.
48. Amunugama R., He Y., Willcox S., Forties R.A., Shim K.S., Bundschuh R., Luo Y., Griffith J., Fishel R. RAD51 protein ATP cap regulates nucleoprotein filament stability. J. Biol. Chem. 2012, 287:8724-8736.
49. Roy A., Kucukural A., Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protocols 2010, 5:725-738.
50. Wu Y., Qian X., He Y., Moya I.A., Luo Y. Crystal structure of an ATPase-active form of Rad51 homolog from Methanococcus voltae. Insights into potassium dependence. J. Biol. Chem. 2005, 280:722-728.
51. DeLano W.L. The PyMOL Molecular Graphics System 2002, DeLano Scientific LLC, Palo Alto, CA.
52. Amunugama R., Fishel R. Subunit interface residues F129 and H294 of human RAD51 are essential for recombinase function. PLoS ONE 2011, 6:e23071.
53. Bhattacharyya S., Keirsey J., Russell B., Kavecansky J., Lillard-Wetherell K., Tahmaseb K., Turchi J.J., Groden J. Telomerase-associated protein 1, HSP90, and topoisomerase IIα associate directly with the BLM helicase in immortalized cells using ALT and modulate its helicase activity using telomeric DNA substrates. J. Biol. Chem. 2009, 284:14966-14977.
54. Van Komen S., Petukhova G., Sigurdsson S., Sung P. Functional cross-talk among Rad51, Rad54, and replication protein A in heteroduplex DNA joint formation. J. Biol. Chem. 2002, 277:43578-43587.
55. Tombline G., Fishel R. Biochemical characterization of the human RAD51 protein. I. ATP hydrolysis. J. Biol. Chem. 2002, 277:14417-14425.
56. Benson F.E., Stasiak A., West S.C. Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J. 1994, 13:5764-5771.
57. Kowalczykowski S.C. Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange. Annu. Rev. Biophys. Biophys. Chem. 1991, 20:539-575.
58. Bugreev D.V., Mazin A.V. Ca2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. P. Natl. Acad. Sci. U.S.A. 2004, 101:9988-9993.
59. Bugreev D.V., Yu X., Egelman E.H., Mazin A.V. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 2007, 21:3085-3094.
60. Veaute X., Jeusset J., Soustelle C., Kowalczykowski S.C., Le Cam E., Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 2003, 423:309-312.
61. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., Ellenberger T., Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 2003, 423:305-309.
62. Sugiyama T., Zaitseva E.M., Kowalczykowski S.C. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 1997, 272:7940-7945.
63. Jensen R.B., Carreira A., Kowalczykowski S.C. Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 2010, 467:678-683.
64. Yang H., Li Q., Fan J., Holloman W.K., Pavletich N.P. The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature 2005, 433:653-657.
65. Shinohara A., Ogawa T. Stimulation by Rad52 of yeast Rad51- mediated recombination. Nature 1998, 391:404-407.
66. 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.
67. Kanaar R., Hoeijmakers J.H.J. Genetic recombination: from competition to collaboration. Nature 1998, 391:335-338.
68. Conant G.C., Wolfe K.H. Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 2008, 9:938-950.
69. Takata M., Sasaki M.S., Tachiiri S., Fukushima T., Sonoda E., Schild D., Thompson L.H., Takeda S. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 2001, 21:2858-2866.
70. Takata M., Sasaki M.S., Sonoda E., Fukushima T., Morrison C., Albala J.S., Swagemakers S.M.A., Kanaar R., Thompson L.H., Takeda S. The Rad51 paralog Rad51B promotes homologous recombinational repair. Mol. Cell. Biol. 2000, 20:6476-6482.
71. Story R., Bishop D., Kleckner N., Steitz T. Structural relationship of bacterial RecA proteins to recombination proteins from bacteriophage T4 and yeast. Science 1993, 259:1892-1896.
72. Ogawa T., Yu X., Shinohara A., Egelman E. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 1993, 259:1896-1899.
73. 2+ homeostasis. Cell Calcium 2011, 49:314-321.
74. Haaf T., Golub E.I., Reddy G., Radding C.M., Ward D.C. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. P. Nat. Acad. Sci. 1995, 92:2298-2302.
75. Scully R., Chen J., Ochs R.L., Keegan K., Hoekstra M., Feunteun J., Livingston D.M. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 1997, 90:425-435.
76. Gildemeister O.S., Sage J.M., Knight K.L. Cellular redistribution of Rad51 in response to DNA damage. J. Biol. Chem. 2009, 284:31945-31952.
77. Carreira A., Kowalczykowski S.C. Two classes of BRC repeats in BRCA2 promote RAD51 nucleoprotein filament function by distinct mechanisms. P. Natl. Acad. Sci. 2011, 108:10448-10453.
78. Carreira A., Hilario J., Amitani I., Baskin R.J., Shivji M.K., Venkitaraman A.R., Kowalczykowski S.C. The BRC repeats of BRCA2 modulate the DNA-binding selectivity of RAD51. Cell 2009, 136:1032-1043.
79. Goggins M., Schutte M., Lu J., Moskaluk C.A., Weinstein C.L., Petersen G.M., Yeo C.J., Jackson C.E., Lynch H.T., Hruban R.H., Kern S.E. Germline BRCA2 gene mutations in patients with apparently sporadic pancreatic carcinomas. Cancer Res. 1996, 56:5360-5364.
80. Wu L., Hickson I.D. DNA helicases required for homologous recombination and repair of damaged replication forks. Annu. Rev. Genet. 2006, 40:279-306.
81. Ira G., Malkova A., Liberi G., Foiani M., Haber Srs2 J.E. Sgs1'ÄìTop3 suppress crossovers during double-strand break repair in yeast. Cell 2003, 115:401-411.
82. Mankouri H.W., Craig T.J., Morgan A. SGS1 is a multicopy suppressor of srs2: functional overlap between DNA helicases. Nucleic Acids Res. 2002, 30:1103-1113.
83. Hu Y., Raynard S., Sehorn M.G., Lu X., Bussen W., Zheng L., Stark J.M., Barnes E.L., Chi P., Janscak P., Jasin M., Vogel H., Sung P., Luo G. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev. 2007, 21:3073-3084.
84. Bernstein K.A., Reid R.J.D., Sunjevaric I., Demuth K., Burgess R.C., Rothstein R. The Shu complex, which contains Rad51 paralogues, promotes DNA repair through inhibition of the Srs2 anti-recombinase. Mol. Biol Cell 2011, 22:1599-1607.
85. Braybrooke J.P., Li J.-L., Wu L., Caple F., Benson F.E., Hickson I.D. Functional Interaction between the bloom's syndrome helicase and the RAD51 paralog, RAD51L3 (RAD51D). J. Biol. Chem. 2003, 278:48357-48366.
86. Eggler A.L., Inman R.B., Cox M.M. The Rad51-dependent pairing of long DNA substrates is stabilized by replication protein A. J. Biol. Chem. 2002, 277:39280-39288.
87. Chun J., Buechelmaier E.S., Powell S.N. Rad51 paralog complexes BCDX2 and CX3 act at different stages in the BRCA1-BRCA2-dependent homologous recombination pathway. Mol. Cell Biol. 2013, 33:387-395.
88. Jensen R.B., Ozes A., Kim T., Estep A., Kowalczykowski S.C. BRCA2 is epistatic to the RAD51 paralogs in response to DNA damage. DNA Repair (Amst) 2013, 12:306-311.