The putative nuclear localization signal of the human RAD52 protein is a potential sumoylation site

Journal of Biochemistry

Volumn 147, Issue 6, 2010, Pages 833-842

  Saito, Kengo ^a,b   Kagawa, Wataru ^a,b   Suzuki, Takehiro ^c   Suzuki, Hidekazu ^d   Yokoyama, Shigeyuki ^b   Saitoh, Hisato ^e   Tashiro, Satoshi ^d   Dohmae, Naoshi ^c   Kurumizaka, Hitoshi ^a,b  

^a WASEDA UNIVERSITY   (Japan)

^b RIKEN YOKOHAMA INSTITUTE   (Japan)

^c RIKEN   (Japan)

^d HIROSHIMA UNIVERSITY   (Japan)

^e KUMAMOTO UNIVERSITY   (Japan)

Author keywords

enzymes; homologous recombination; post translational modification; RAD52; self association; sumoylation

Indexed keywords

RAD52 PROTEIN; SUMO PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; DNA BINDING; ESCHERICHIA COLI; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STRUCTURE ANALYSIS; SUMOYLATION;

ESCHERICHIA COLI;

EID: 77953696034     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvq020     Document Type: Article

References (53)

1. O'Driscoll, M., and Jeggo, P.A. (2006) The role of double-strand break repair - insights from human genetics. Nat. Rev. Genet. 7, 45-54
2. Symington, L.S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair (table of contents). Microbiol. Mol. Biol. Rev. 66, 630-670
3. San Filippo, J., Sung, P., and Klein, H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257
4. Song, B., and Sung, P. (2000) Functional interactions among yeast Rad51 recombinase, Rad52 mediator, and replication protein A in DNA strand exchange. J. Biol. Chem. 275, 15895-15904
5. 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
6. 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
7. 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
8. 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
9. Shinohara, A., and Ogawa, T. (1998) Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391, 404-407
10. Ivanov, E.L., Sugawara, N., Fishman-Lobell, J., and Haber, J.E. (1996) Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics 142, 693-704
11. Mortensen, U.H., Bendixen, C., Sunjevaric, I., and Rothstein, R. (1996) DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl Acad. Sci. USA 93, 10729-10734
12. Reddy, G., Golub, E.I., and Radding, C.M. (1997) Human Rad52 protein promotes single-strand DNA annealing followed by branch migration. Mutat. Res. 377, 53-59
13. 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
14. Bi, B., Rybalchenko, N., Golub, E.I., and Radding, C.M. (2004) Human and yeast Rad52 proteins promote DNA strand exchange. Proc. Natl Acad. Sci. USA 101, 9568-9572
15. Kumar, J.K., and Gupta, R.C. (2004) Strand exchange activity of human recombination protein Rad52. Proc. Natl Acad. Sci. USA 101, 9562-9567
16. 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
17. Bugreev, D.V., Hanaoka, F., and Mazin, A.V. (2007) Rad54 dissociates homologous recombination intermediates by branch migration. Nat. Struct. Mol. Biol. 14, 746-753
18. 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
19. Mazloum, N., and Holloman, W.K. (2009) Second-end capture in DNA double-strand break repair promoted by Brh2 protein of Ustilago maydis. Mol. Cell. 33, 160-170
20. Rijkers, T., Van Den Ouweland, J., Morolli, B., Rolink, A.G., Baarends, W.M., Van Sloun, P.P., Lohman, P.H., and Pastink, A. (1998) Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18, 6423-6429
21. Yamaguchi-Iwai, Y., Sonoda, E., Buerstedde, J.M., Bezzubova, O., Morrison, C., Takata, M., Shinohara, A., and Takeda, S. (1998) Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52. Mol. Cell. Biol. 18, 6430-6435
22. Johnson, E.S. (2004) Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382
23. Kerscher, O., Felberbaum, R., and Hochstrasser, M. (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180
24. Seeler, J.S., and Dejean, A. (2003) Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell Biol. 4, 690-699
25. Heun, P. (2007) SUMOrganization of the nucleus. Curr. Opin. Cell. Biol. 19, 350-355
26. Seeler, J.S., Bischof, O., Nacerddine, K., and Dejean, A. (2007) SUMO, the three Rs and cancer. Curr. Top. Microbiol. Immunol. 313, 49-71
27. Ho, J.C., Warr, N.J., Shimizu, H., and Watts, F.Z. (2001) SUMO modification of Rad22, the Schizosaccharomyces pombe homologue of the recombination protein Rad52. Nucleic Acids Res. 29, 4179-4186
28. Sacher, M., Pfander, B., Hoege, C., and Jentsch, S. (2006) Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 8, 1284-1290
29. Torres-Rosell, J., Sunjevaric, I., De Piccoli, G., Sacher, M., Eckert-Boulet, N., Reid, R., Jentsch, S., Rothstein, R., Aragó n, L., and Lisby, M. (2007) The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9, 923-931
30. Uchimura, Y., Nakamura, M., Sugasawa, K., Nakao, M., and Saitoh, H. (2004) Overproduction of eukaryotic SUMO-1- and SUMO-2-conjugated proteins in Escherichia coli. Anal. Biochem. 331, 204-206
31. 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
32. Yunus, A.A., and Lima, C.D. (2005) Purification and activity assays for Ubc9, the ubiquitin-conjugating enzyme for the small ubiquitin-like modifier SUMO. Methods Enzymol. 398, 74-87
33. Bayer, P., Arndt, A., Metzger, S., Mahajan, R., Melchior, F., Jaenicke, R., and Becker, J. (1998) Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 280, 275-286
34. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
35. Sarai, N., Kagawa, W., Kinebuchi, T., Kagawa, A., Tanaka, K., Miyagawa, K., Ikawa, S., Shibata, T., Kurumizaka, H., and Yokoyama, S. (2006) Stimulation of Dmc1-mediated DNA strand exchange by the human Rad54B protein. Nucleic Acids Res. 34, 4429-4437
36. Baba, D., Maita, N., Jee, J.G., Uchimura, Y., Saitoh, H., Sugasawa, K., Hanaoka, F., Tochio, H., Hiroaki, H., and Shirakawa, M. (2005) Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435, 979-982
37. Ivanov, A.V., Peng, H., Yurchenko, V., Yap, K.L., Negorev, D.G., Schultz, D.C., Psulkowski, E., Fredericks, W.J., White, D.E., Maul, G.G., Sadofsky, M.J., Zhou, M.M., and Rauscher, F.J. (2007) PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell. 28, 823-837
38. Meulmeester, E., Kunze, M., Hsiao, H.H., Urlaub, H., and Melchior, F. (2008) Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol. Cell. 30, 610-619
39. Tateishi, Y., Ariyoshi, M., Igarashi, R., Hara, H., Mizuguchi, K., Seto, A., Nakai, A., Kokubo, T., Tochio, H., and Shirakawa, M. (2009) Molecular basis for SUMOylation-dependent regulation of DNA binding activity of heat shock factor 2. J. Biol. Chem. 284, 2435-2447
40. Ranatunga, W., Jackson, D., Lloyd, J.A., Forget, A.L., Knight, K.L., and Borgstahl, G.E. (2001) Human RAD52 exhibits two modes of self-association. J. Biol. Chem. 276, 15876-15880
41. 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
42. 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. USA 99, 13492-13497
43. 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
44. Shen, Z., Cloud, K.G., Chen, D.J., and Park, M.S. (1996) Specific interactions between the human RAD51 and RAD52 proteins. J. Biol. Chem. 271, 148-152
45. Stasiak, A.Z., Larquet, E., Stasiak, A., Müller, S., Engel, A., Van Dyck, E., West, S.C., and Egelman, E.H. (2000) The human Rad52 protein exists as a heptameric ring. Curr. Biol. 10, 337-340
46. Essers, J., Houtsmuller, A.B., van Veelen, L., Paulusma, C., Nigg, A.L., Pastink, A., Vermeulen, W., Hoeijmakers, J.H., and Kanaar, R. (2002) Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J. 21, 2030-2037
47. Ohuchi, T., Seki, M., and Enomoto, T. (2008) Nuclear localization of Rad52 is pre-requisite for its sumoylation. Biochem. Biophys. Res. Commun. 372, 126-130
48. Vethantham, V., Rao, N., and Manley, J.L. (2008) Sumoylation regulates multiple aspects of mammalian poly(A) polymerase function. Genes. Dev. 22, 499-511
49. 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
50. Kerscher, O. (2007) SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 8, 550-555
51. Li, W., Hesabi, B., Babbo, A., Pacione, C., Liu, J., Chen, D.J., Nickoloff, J.A., and Shen, Z. (2000) Regulation of double-strand break-induced mammalian homologous recombination by UBL1, a RAD51-interacting protein. Nucleic Acids Res. 28, 1145-1153
52. Saitoh, H., and Hinchey, J. (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275, 6252-6258
53. Bohren, K.M., Nadkarni, V., Song, J.H., Gabbay, K.H., and Owerbach, D. (2004) A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J. Biol. Chem. 279, 27233-27238