Human replication protein A-Rad52-single-stranded DNA complex: Stoichiometry and evidence for strand transfer regulation by phosphorylation

Biochemistry

Volumn 48, Issue 28, 2009, Pages 6633-6643

  Deng, Xiaoyi ^a,b   Prakash, Aishwarya ^a   Dhar, Kajari ^a   Baia, Gilson S ^a   Kolar, Carol ^a   Oakley, Greg G ^c   Borgstahl, Gloria E O ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMILUMINESCENCE DETECTION; DNA DAMAGING AGENTS; DNA METABOLISM; DOUBLE-STRANDED DNA BREAKS; INDIVIDUAL PROTEINS; MULTI-ANGLE LIGHT SCATTERINGS; PROTEIN SPECIES; REPLICATION PROTEIN A; SINGLE-STRANDED DNA; SINGLE-STRANDED DNA-BINDING PROTEINS; SODIUM DODECYL SULFATE-POLYACRYLAMIDE GEL ELECTROPHORESIS;

CHROMATOGRAPHIC ANALYSIS; DIFFUSERS (OPTICAL); DNA; DYES; ELECTROPHORESIS; GELATION; GENES; HYDROGELS; MOLECULAR MASS; PHOSPHORYLATION; PROTEINS; REPAIR; SIZE EXCLUSION CHROMATOGRAPHY; SODIUM; SODIUM SULFATE; STOICHIOMETRY;

NUCLEIC ACIDS;

RAD52 PROTEIN; REPLICATION FACTOR A; SINGLE STRANDED DNA;

ARTICLE; BIOTINYLATION; CHEMOLUMINESCENCE; COMPLEX FORMATION; CROSS LINKING; DNA DAMAGE; DNA METABOLISM; DNA PROTEIN COMPLEX; DNA REPAIR; DNA TRANSFER; GEL PERMEATION CHROMATOGRAPHY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; LIGHT SCATTERING; MOLECULAR WEIGHT; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; STOICHIOMETRY;

CHROMATOGRAPHY, GEL; DNA REPAIR; DNA, SINGLE-STRANDED; HUMANS; LIGHT; MODELS, BIOLOGICAL; PHOSPHORYLATION; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; REPLICATION PROTEIN A; SCATTERING, RADIATION;

EUKARYOTA;

EID: 67650489517     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900564k     Document Type: Article

References (78)

1. Shinohara, A., and Ogawa, T. (1995) Homologous recombination and the roles of double-strand breaks. Trends Biochem. Sci. 20, 387-391.
2. Krogh, B. O., and Symington, L. S. (2004) Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271.
3. Sung, P., Trujillo, K. M., and Van Komen, S. (2000) Recombination factors of Saccharomyces cerevisiae. Mutat. Res. 451, 257-275.
4. 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.
5. Shinohara, A., and Ogawa, T. (1998) Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391, 404-407. (Pubitemid 28093517)
6. New, J. H., Sugiyama, T., Zaitseva, E., and Kowalczykowski, S. C. (1998) Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391, 407-410. (Pubitemid 28093518)
7. Sugiyama, T., New, J. H., and Kowalczykowski, S. C. (1998) DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc. Natl. Acad. Sci. U.S.A. 95, 6049-6054.
8. Benson, F. E., Baumann, P., and West, S. C. (1998) Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature 391, 401-404. (Pubitemid 28093516)
9. Baumann, P., and West, S. C. (1999) Heteroduplex formation by human Rad51 protein: Effects of DNA end-structure, hRP-A and hRad52. J. Mol. Biol. 291, 363-374.
10. McIlwraith, M. J., Van Dyck, E., Masson, J. Y., Stasiak, A. Z., Stasiak, A., and West, S. C. (2000) Reconstitution of the strand invasion step of double-strand break repair using human Rad51 Rad52 and RPA proteins. J. Mol. Biol. 304, 151-164.
11. Sung, P., Krejci, L., Van Komen, S., and Sehorn, M. G. (2003) Rad51 recombinase and recombination mediators. J. Biol. Chem. 278, 42729-42732.
12. Beernink, H. T., and Morrical, S. W. (1999) RMPs: Recombination/ replication mediator proteins. Trends Biochem. Sci. 24, 385-389.
13. McIlwraith, M. J., and West, S. C. (2008) DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. Mol. Cell 29, 510-516. (Pubitemid 351282535)
14. Kowalczykowski, S. C. (2005) Cancer: Catalyst of a catalyst. Nature 433, 591-592.
15. Iftode, C., Daniely, Y., and Borowiec, J. A. (1999) Replication Protein A(RPA): The Eukaryotic SSB. Crit. Rev. Biochem. Mol. Biol. 34, 141-180.
16. Wold, M. S. (1997) RPA: A Heterotrimeric, Single-Stranded DNA-Binding Protein Required for Eukaryotic DNA Metabolism. Annu. Rev. Biochem. 66, 61-91.
17. Loo, Y.-M., and Melendy, T. (2000) The majority of human replication protein A remains complexed throughout the cell cycle. Nucleic Acids Res. 28, 3354-3360. (Pubitemid 30662301)
18. Dimitrova, D. S., and Gilbert, D. M. (2000) Stability and Nuclear Distribution of Mammalian Replication Protein A Heterotrimeric Complex. Exp. Cell Res. 254, 321-327.
19. Fairman, M. P., and Stillman, B. (1988) Cellular Factors Required for Multiple Stages of SV40 DNA Replication in Vitro. EMBO J. 7, 1211-1218.
20. Kim, C., Paulus, B. F., and Wold, M. S. (1994) Interactions of Human Replication Protein A with Oligonucleotides. Biochemistry 33, 14197-14206. (Pubitemid 24382365)
21. Fanning, E., Klimovich, V., and Nager, A. R. (2006) A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 34, 4126-4137. (Pubitemid 44542191)
22. Gomes, X. V., Henricksen, L. A., and Wold, M. S. (1996) Proteolytic Mapping of Human Replication Protein A: Evidence for Multiple Structural Domains and a Conformational Change upon Interaction with Single-stranded DNA. Biochemistry 35, 5587-5594.
23. Blackwell, L., Borowiec, J., and Mastrangelo, I. (1996) Single-Stranded DNA Binding Alters Human Replication Protein A Structure and Facilitates Interaction with DNA-Dependent Protein Kinase. Mol. Cell. Biol. 16, 4798-4807.
24. Wu, X., Yang, Z., Liu, Y., and Zou, Y. (2005) Preferential localization of hyperphosphorylated replication protein A to double-strand break repair and checkpoint complexes upon DNA damage. Biochem. J. 391, 473-480. (Pubitemid 41634773)
25. Zhou, B. B., and Elledge, S. J. (2000) The DNA damage response: Putting checkpoints in perspective. Nature 408, 433-439.
26. Niu, H., Erdjument-Bromage, H., Pan, Z., Lee, S., Tempst, P., and Hurwitz, J. (1997) Mapping of amino acid residues in the p34 subunit of human single-stranded DNA-binding protein phosphorylated by DNA-dependent protein kinase and cdc2 kinase in vitro. J. Biol. Chem. 272, 12634-12641.
27. Zernik-Kobak, M., Vasunia, K., Connelly, M., Anderson, C. W., and Dixon, K. (1997) Sites of UV-induced Phosphorylation of the p34 Subunit of Replication Protein A from HeLa Cells. J. Biol. Chem. 272, 23896-23904.
28. Binz, S. K., Sheehan, A. M., and Wold, M. S. (2004) Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair 3, 1015-1024. (Pubitemid 39004091)
29. Treuner, K., Okuyama, A., Knippers, R., and Fackelmayer, F. O. (1999) Hyperphosphorylation of replication protein A middle subunit (RPA32) in apoptosis. Nucleic Acids Res. 27, 1499-1504. (Pubitemid 29206292)
30. Liu, V. F., and Weaver, D. T. (1993) The ionizing radiation-induced Replication Protein A phosphorylation response differs between ataxia telangiectasia and normal human cells. Mol. Cell. Biol. 13, 7222-7231.
31. Fang, F., and Newport, J. W. (1993) Distinct Roles of cdk2 and cdc2 in RP-A Phosphorylation During the Cell Cycle. J. Cell Sci. 106, 983-994. (Pubitemid 23346810)
32. Din, S.-U., Brill, S. J., Fairman, M. P., and Stillman, B. (1990) Cell cycle regulated phosphorylation of DNA replication factor A from human and yeast cells. Genes Dev. 4, 968-977. (Pubitemid 20188972)
33. Carty, M. P., Zernik-Kobak, M., McGrath, S., and Dixon, K. (1994) UV light-induced DNA synthesis arrest in HeLa cells is associated with changes in phosphorylation of human single-stranded DNA-binding protein. EMBO J. 13, 2114-2123. (Pubitemid 24139724)
34. Treuner, K., Findeisen, M., Strausfeld, U., and Knippers, R. (1999) Phosphorylation of Replication Protein A Middle Subunit (RPA32) Leads to a Disassembly of the RPA Heterotrimer. J. Biol. Chem. 274, 15556-15561.
35. Block, W. D., Yu, Y., and Lees-Miller, S. P. (2004) Phosphatidyl inositol 3-kinase-like serine/threonine protein kinases (PIKKs) are required for DNA damage-induced phosphorylation of the 32 kDa subunit of replication protein A at threonine 21. Nucleic Acids Res. 32, 997-1005. (Pubitemid 38854700)
36. Anantha, R. W., Vassin, V. M., and Borowiec, J. A. (2007) Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J. Biol. Chem. 282, 35910-35923.
37. Nuss, J. E., Patrick, S. M., Oakley, G. G., Alter, G. M., Robison, J. G., Dixon, K., and Turchi, J. J. (2005) DNA damage induced hyperphosphorylation of replication protein A. 1. Identification of novel sites of phosphorylation in response to DNA damage. Biochemistry 44, 8428-8437.
38. Oakley, G. G., Patrick, S. M., Yao, J., Carty, M. P., Turchi, J. J., and Dixon, K. (2003) RPA phosphorylation in mitosis alters DNA binding and protein-protein interactions. Biochemistry 42, 3255-3264. (Pubitemid 36348634)
39. Patrick, S. M., Oakley, G. G., Dixon, K., and Turchi, J. J. (2005) DNA damage induced hyperphosphorylation of replication protein A. 2. Characterization of DNA binding activity, protein interactions, and activity in DNA replication and repair. Biochemistry 44, 8438-8448.
40. Sleeth, K. M., Sorensen, C. S., Issaeva, N., Dziegielewski, J., Bartek, J., and Helleday, T. (2007) RPA mediates recombination repair during replication stress and is displaced from DNA by checkpoint signalling in human cells. J. Mol. Biol. 373, 38-47.
41. Sugiyama, T., Kantake, N., Wu, Y., and Kowalczykowski, S. C. (2006) Rad52-mediated DNA annealing after Rad51-mediated DNA strand exchange promotes second ssDNA capture. EMBO J. 25, 5539-5548. (Pubitemid 44847194)
42. Gudmundsdottir, K., and Ashworth, A. (2006) The roles of BRCA1 and BRCA2 and associated proteins in the maintenance of genomic stability. Oncogene 25, 5864-5874. (Pubitemid 44453442)
43. Paques, F., and Haber, J. E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63, 349-404.
44. Larminat, F., Germanier, M., Papouli, E., and Defais, M. (2002) Deficiency in BRCA2 leads to increase in non-conservative homologous recombination. Oncogene 21, 5188-5192. (Pubitemid 34907746)
45. Tutt, A., Bertwistle, D., Valentine, J., Gabriel, A., Swift, S., Ross, G., Griffin, C., Thacker, J., and Ashworth, A. (2001) Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J. 20, 4704-4716. (Pubitemid 32848624)
46. Navadgi, V. M., Dutta, A., and Rao, B. J. (2003) Human Rad52 facilitates a three-stranded pairing that follows no strand exchange: A novel pairing function of the protein. Biochemistry 42, 15237-15251. (Pubitemid 38031723)
47. Ristic, D., Modesti, M., Kanaar, R., and Wyman, C. (2003) Rad52 and Ku bind to different DNA structures produced early in double-strand break repair. Nucleic Acids Res. 31, 5229-5237. (Pubitemid 37441890)
48. Kagawa, W., Kagawa, A., Saito, K., Ikawa, S., Shibata, T., Kurumizaka, H., and Yokoyama, S. (2008) Identification of a second DNA binding site in the human Rad52 protein. J. Biol. Chem. 283, 24264-24273.
49. Van Dyck, E., Stasiak, A. Z., Stasiak, A., and West, S. C. (1999) Binding of double-strand breaks in DNA by human Rad52 protein. Nature 398, 728-731. (Pubitemid 29197653)
50. Parsons, C. A., Baumann, P., Van Dyck, E., and West, S. C. (2000) Precise binding of single-stranded DNA termini by human RAD52 protein. EMBO J. 19, 4175-4181. (Pubitemid 30608555)
51. Wu, Y., Siino, J. S., Sugiyama, T., and Kowalczykowski, S. C. (2006) The DNA binding preference of RAD52 and RAD59 proteins: Implications for RAD52 and RAD59 protein function in homologous recombination. J. Biol. Chem. 281, 40001-40009.
52. Lloyd, J. A., Forget, A. L., and Knight, K. L. (2002) Correlation of biochemical properties with the oligomeric state of human rad52 protein. J. Biol. Chem. 277, 46172-46178.
53. Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S., and Ogawa, T. (1998) Rad52 forms ring structures and cooperates with RPA in single-strand DNA annealing. Genes Cells 3, 145-156. (Pubitemid 28374987)
54. Van Dyck, E., Hajibagheri, N. M. A., Stasiak, A., and West, S. C. (1998) Visualisation of Human Rad52 Protein and its Complexes with hRad51 and DNA. J. Mol. Biol. 284, 1027-1038.
55. Kagawa, W., Kurumizaka, H., Ikawa, S., Yokoyama, S., and Shibata, T. (2001) Homologous Pairing Promoted by the Human Rad52 Protein. J. Biol. Chem. 276, 35201-35208.
56. Stasiak, A. Z., Larquet, E., Stasiak, A., Muller, S., Engel, A., Dyck, E. V., West, S. C., and Egelman, E. H. (2000) The human Rad52 protein exists as a heptameric ring. Curr. Biol. 10, 337-340.
57. Ranatunga, W., Jackson, D., Lloyd, J. A., Forget, A. L., Knight, K. L., and Borgstahl, G. E. O. (2001) Human Rad52 Exhibits Two Modes of Self-association. J. Biol. Chem. 276, 15876-15880.
58. 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. (Pubitemid 35007350)
59. 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. U.S.A. 99, 13492-13497.
60. Plate, I., Albertsen, L., Lisby, M., Hallwyl, S. C., Feng, Q., Seong, C., Rothstein, R., Sung, P., and Mortensen, U. H. (2008) Rad52 multimerization is important for its nuclear localization in Saccharomyces cerevisiae. DNA Repair 7, 57-66. (Pubitemid 350184404)
61. Park, M. S., Ludwig, D. L., Stigger, E., and Lee, S. H. (1996) Physical interaction between Human RAD52 and RPA is Required for Homologous Recombination in Mammalian Cells. J. Biol. Chem. 271, 18996-19000.
62. Jackson, D., Dhar, K., Wahl, J. K., Wold, M. S., and Borgstahl, G. E. (2002) Analysis of the human replication protein A:Rad52 complex: Evidence for crosstalk between RPA32, RPA70, Rad52 and DNA. J. Mol. Biol. 321, 133-148.
63. Mer, G., Bochkarev, A., Gupta, R., Bochkareva, E., Frappier, L., Ingles, C. J., Edwards, A. M., and Chazin, W. J. (2000) Structural Basis for the Recognition of DNA Repair Proteins UNG2, XPA and Rad52 by Replication Factor RPA. Cell 103, 449-456.
64. Hays, S. L., Firmenich, A. A., Massey, P., Banerjee, R., and Berg, P. (1998) Studies of the Interaction between Rad52 Protein and the Yeast Single-Stranded DNA Binding Protein RPA. Mol. Cell. Biol. 18, 4400-4406.
65. Seong, C., Sehorn, M. G., Plate, I., Shi, I., Song, B., Chi, P., Mortensen, U., Sung, P., and Krejci, L. (2008) Molecular anatomy of the recombination mediator function of Saccharomyces cerevisiae Rad52. J. Biol. Chem. 283, 12166-12174.
66. Plate, I., Hallwyl, S. C., Shi, I., Krejci, L., Muller, C., Albertsen, L., Sung, P., and Mortensen, U. H. (2008) Interaction with RPA is necessary for Rad52 repair center formation and for its mediator activity. J. Biol. Chem. 283, 29077-29085.
67. Tarazona, M. P., and Saiz, E. (2003) Combination of SEC/MALS experimental procedures and theoretical analysis for studying the solution properties of macromolecules. J. Biochem. Biophys. Methods 56, 95-116.
68. Mogridge, J. (2004) Using light scattering to determine the stoichiometry of protein complexes. Methods Mol. Biol. 261, 113-118.
69. Henricksen, L. A., Umbricht, C. B., and Wold, M. S. (1994) Recombinant Replication Protein A: Expression, Complex Formation and Function Characterization. J. Biol. Chem. 269, 11121-11132.
70. Navadgi, V. M., Shukla, A., and Rao, B. J. (2005) Effect of DNA sequence and nucleotide cofactors on hRad51 binding to ssDNA: Role of hRad52 in recruitment. Biochem. Biophys. Res. Commun. 334, 696-701.
71. D'Souza, J. S., Dharmadhikari, J. A., Dharmadhikari, A. K., Navadgi, V., Mathur, D., and Rao, B. J. (2006) Human Rad52 binding reders ssDNA unfolded: Image and contour length analysis by atomic force microscopy. Curr. Sci. 91, 1641-1648.
72. Wold, M. S., and Kelly, T. (1988) Purification and Characterization of Replication protein A, a Cellular Protein Required for in vitro Replication of Simian Virus 40 DNA. Proc. Natl. Acad. Sci. U.S.A. 85, 2523-2527.
73. Kenny, M. K., Schlegel, U., Furneaux, H., and Hurwitz, J. (1990) The Role of Human Single-stranded DNA Binding Protein and Its Individual Subunits in Simian Virus 40 DNA Replication. J. Biol. Chem. 265, 7693-7700.
74. Seroussi, E., and Lavi, S. (1993) Replication protein A is the major single-stranded DNA binding protein detected in mammalian cell extracts by gel retardation assays and UV cross-linking of long and short single-stranded DNA molecules. J. Biol. Chem. 268, 7147-7154.
75. Kim, C., and Wold, M. S. (1995) Recombinant Human Replication Protein A Binds to Polynucleotides with Low Cooperativity. Biochemistry 34, 2058-2064.
76. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003) Global analysis of protein expression in yeast. Nature 425, 737-741. (Pubitemid 37314318)
77. 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.
78. Navadgi, V. M., Shukla, A., Vempati, R. K., and Rao, B. J. (2006) DNA mediated disassembly of hRad51 and hRad52 proteins and recruitment of hRad51 to ssDNA by hRad52. FEBS J. 273, 199-207.