Activation of the SUMO modification system is required for the accumulation of RAD51 at sites of DNA damage

Journal of Cell Science

Volumn 126, Issue 22, 2013, Pages 5284-5292

  Shima, Hiroki ^a,b   Suzuki, Hidekazu ^a   Sun, Jiying ^a   Kono, Kazuteru ^a   Shi, Lin ^a   Kinomura, Aiko ^a   Horikoshi, Yasunori ^a   Ikura, Tsuyoshi ^c   Ikura, Masae ^c   Kanaar, Roland ^d   Igarashi, Kazuhiko ^b   Saitoh, Hisato ^e   Kurumizaka, Hitoshi ^f   Tashiro, Satoshi ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d ERASMUS MEDICAL CENTER   (Netherlands)

^e KUMAMOTO UNIVERSITY   (Japan)

^f WASEDA UNIVERSITY   (Japan)

Author keywords

RAD51; Recombinational DNA repair; SUMO

Indexed keywords

DNA; RAD51 PROTEIN; SUMO 1 PROTEIN; SUMO PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SUMOYLATION; UBIQUITINATION;

RAD51; RECOMBINATIONAL DNA REPAIR; SUMO;

CELL LINE; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; HUMANS; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN PROCESSING, POST-TRANSLATIONAL; RAD51 RECOMBINASE; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84888083025     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.133744     Document Type: Article

References (65)

1. Albiez, H., Cremer, M., Tiberi, C., Vecchio, L., Schermelleh, L., Dittrich, S., Küpper, K., Joffe, B., Thormeyer, T., von Hase, J. et al. (2006). Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks. Chromosome Res. 14, 707-733.
2. Anachkova, B., Djeliova, V. and Russev, G. (2005). Nuclear matrix support of DNA replication. J. Cell. Biochem. 96, 951-961.
3. Atwell, S., Disseau, L., Stasiak, A. Z., Stasiak, A., Renodon-Cornière, A., Takahashi, M., Viovy, J. L. and Cappello, G. (2012). Probing Rad51-DNA interactions by changing DNA twist. Nucleic Acids Res. 40, 11769-11776.
4. Bekker-Jensen, S., Lukas, C., Kitagawa, R., Melander, F., Kastan, M. B., Bartek, J. and Lukas, J. (2006). Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173, 195-206.
5. Bergink, S., Ammon, T., Kern, M., Schermelleh, L., Leonhardt, H. and Jentsch, S. (2013) Role of Cdc48/p97 as a SUMO-targeted segregase curbing Rad51-Rad52 interaction. Nature Cell Biol. 15 526-532.
6. Cheng, Z., Ke, Y., Ding, X., Wang, F., Wang, H., Ahmed, K., Liu, Z., Xu, Y., Aikhionbare, F., Yan, H. et al. (2008). Functional characterization of TIP60 sumoylation in UV-irradiated DNA damage response. Oncogene 27, 931-941.
7. Chiolo, I., Minoda, A., Colmenares, S. U., Polyzos, A., Costes, S. V. and Karpen, G. H. (2011). Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144, 732-744.
8. Courbet, S., Gay, S., Arnoult, N., Wronka, G., Anglana, M., Brison, O. and Debatisse, M. (2008). Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455, 557-560.
9. Cremer, T. and Cremer, M. (2010). Chromosome territories. Cold Spring Harb. Perspect. Biol. 2, a003889.
10. Cubeñas-Potts, C. and Matunis, M. J. (2013). SUMO: a multifaceted modifier of chromatin structure and function. Dev. Cell 24, 1-12.
11. Danielsen, J. R., Povlsen, L. K., Villumsen, B. H., Streicher, W., Nilsson, J., Wikström, M., Bekker-Jensen, S. and Mailand, N. (2012). DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding Zinc finger. J. Cell Biol. 197, 179-187.
12. Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S. and Ren, B. (2012). Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380.
13. Dou, H., Huang, C., Singh, M., Carpenter, P. B. and Yeh, E. T. (2010). Regulation of DNA repair through deSUMOylation and SUMOylation of replication protein A complex. Mol. Cell 39, 333-345.
14. Durant, S. T. and Nickoloff, J. A. (2005). Good timing in the cell cycle for precise DNA repair by BRCA1. Cell Cycle 4, 1216-1222.
15. Eladad, S., Ye, T. Z., Hu, P., Leversha, M., Beresten, S., Matunis, M. J. and Ellis, N. A. (2005). Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum. Mol. Genet. 14, 1351-1365.
16. Galanty, Y., Belotserkovskaya, R., Coates, J., Polo, S., Miller, K. M. and Jackson, S. P. (2009). Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939.
17. Galanty, Y., Belotserkovskaya, R., Coates, J. and Jackson, S. P. (2012). RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26, 1179-1195.
18. Haaf, T., Golub, E. I., Reddy, G., Radding, C. M. and Ward, D. C. (1995). Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. USA 92, 2298- 2302.
19. Hayashi, T., Seki, M., Maeda, D., Wang, W., Kawabe, Y., Seki, T., Saitoh, H., Fukagawa, T., Yagi, H. and Enomoto, T. (2002). Ubc9 is essential for viability of higher eukaryotic cells. Exp. Cell Res. 280, 212-221.
20. Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G. and Jentsch, S. (2002). RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135-141.
21. Holloman, W. K. (2011). Unraveling the mechanism of BRCA2 in homologous recombination. Nat. Struct. Mol. Biol. 18, 748-754.
22. Hosoya, N., Okajima, M., Kinomura, A., Fujii, Y., Hiyama, T., Sun, J., Tashiro, S. and Miyagawa, K. (2012). Synaptonemal complex protein SYCP3 impairs mitotic recombination by interfering with BRCA2. EMBO Rep. 13, 44-51.
23. Ikura, T., Tashiro, S., Kakino, A., Shima, H., Jacob, N., Amunugama, R., Yoder, K., Izumi, S., Kuraoka, I., Tanaka, K. et al. (2007). DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27, 7028-7040.
24. Jackson, S. P. and Durocher, D. (2013). Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49, 795-807.
25. Kalocsay, M., Hiller, N. J. and Jentsch, S. (2009). Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol. Cell 33, 335-343.
26. Kobayashi, J., Kato, A., Ota, Y., Ohba, R. and Komatsu, K. (2010). Bisbenzamidine derivative, pentamidine represses DNA damage response through inhibition of histone H2A acetylation. Mol. Cancer 9, 34.
27. Kovalenko, O. V., Plug, A. W., Haaf, T., Gonda, D. K., Ashley, T., Ward, D. C., Radding, C. M. and Golub, E. I. (1996). Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc. Natl. Acad. Sci. USA 93, 2958-2963.
28. 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.
29. Lin, D. Y., Huang, Y. S., Jeng, J. C., Kuo, H. Y., Chang, C. C., Chao, T. T., Ho, C. C., Chen, Y. C.,Lin, T. P., Fang, H. I. et al. (2006). Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 24, 341-354.
30. Liu, J., Doty, T., Gibson, B. and Heyer, W. D. (2010). Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA. Nat. Struct. Mol. Biol. 17, 1260-1262.
31. Luo, K., Zhang, H., Wang, L., Yuan, J. and Lou, Z. (2012). Sumoylation of MDC1 is important for proper DNA damage response. EMBO J. 31, 3008-3019.
32. Manthei, K. A. and Keck, J. L. (2013). The BLM dissolvasome in DNA replication and repair. Cell. Mol. Life Sci. [Epub ahead of print].
33. Markaki, Y, Smeets, D., Fiedler, S., Schmid, V. J., Schermelleh, L., Cremer, T. and Cremer, M. (2012). The potential of 3D-FISH and super-resolution structured illumination microscopy for studies of 3D nuclear architecture: 3D structured illumination microscopy of defined chromosomal structures visualized by 3D (immuno)-FISH opens new perspectives for studies of nuclear architecture. Bioessays 34, 412-426.
34. Mladenov, E. V., Kalev, P. S. and Anachkova, B. B. (2009). Nuclear matrix binding site in the Rad51 recombinase. J. Cell. Physiol. 219, 202-208.
35. Morris, J. R., Boutell, C., Keppler, M., Densham, R., Weekes, D., Alamshah, A., Butler, L., Galanty, Y., Pangon, L., Kiuchi, T. et al. (2009). The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890.
36. Nagai, S., Dubrana, K., Tsai-Pflugfelder, M., Davidson, M. B., Roberts, T. M., Brown, G. W., Varela, E., Hediger, F., Gasser, S. M. and Krogan, N. J. (2008). Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322, 597-602.
37. Nagai, S., Davoodi, N. and Gasser, S. M. (2011). Nuclear organization in genome stability: SUMO connections. Cell Res. 21, 474-485.
38. Nakatani, Y. and Ogryzko, V. (2003). Immunoaffinity purification of mammalian protein complexes. Methods Enzymol. 370, 430-444.
39. Nishida, T., Tanaka, H. and Yasuda, H. (2000). A novel mammalian Smt3-specific isopeptidase 1 (SMT3IP1) localized in the nucleolus at interphase. Eur. J. Biochem. 267, 6423-6427.
40. Ouyang, K. J., Woo, L. L., Zhu, J., Huo, D., Matunis, M. J. and Ellis, N. A. (2009). SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLoS Biol. 7, e1000252.
41. Pierce, A. J. and Jasin, M. (2005). Measuring recombination proficiency in mouse embryonic stem cells. Methods Mol. Biol. 291, 373-384.
42. Pinder, J. B., Attwood, K. M. and Dellaire, G. (2013). Reading, writing, and repair: the role of ubiquitin and the ubiquitin-like proteins in DNA damage signaling and repair. Front. Genet. 4, 45.
43. Polo, S. E. and Jackson, S. P. (2011). Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25, 409-433.
44. Praefcke, G. J., Hofmann, K. and Dohmen, R. J. (2012). SUMO playing tag with ubiquitin. Trends Biochem. Sci. 37, 23-31.
45. Psakhye, I. and Jentsch, S. (2012). Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807-820.
46. Richardson, C., Stark, J. M., Ommundsen, M. and Jasin, M. (2004). Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability. Oncogene 23, 546-553.
47. Riquelme, C., Barthel, K. K., Qin, X. F. and Liu, X. (2006). Ubc9 expression is essential for myotube formation in C2C12. Exp. Cell Res. 312, 2132-2141.
48. 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.
49. Saitoh, H., Pizzi, M. D. and Wang, J. (2002). Perturbation of SUMOlation enzyme Ubc9 by distinct domain within nucleoporin RanBP2/Nup358. J. Biol. Chem. 277, 4755-4763.
50. Sakamoto, S., Iijima, K., Mochizuki, D., Nakamura, K., Teshigawara, K., Kobayashi, J., Matsuura, S., Tauchi, H. and Komatsu, K. (2007). Homologous recombination repair is regulated by domains at the N- and C-terminus of NBS1 and is dissociated with ATM functions. Oncogene 26, 6002-6009.
51. Shen, Z., Pardington-Purtymun, P. E., Comeaux, J. C., Moyzis, R. K. and Chen, D. J. (1996a). Associations of UBE2I with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system. Genomics 37, 183-186.
52. Shen, Z., Pardington-Purtymun, P. E., Comeaux, J. C., Moyzis, R. K. and Chen, D. J. (1996b). UBL1, a human ubiquitin-like protein associating with human RAD51/ RAD52 proteins. Genomics 36, 271-279.
53. Shen, T. H., Lin, H. K., Scaglioni, P. P., Yung, T. M. and Pandolfi, P. P. (2006). The mechanisms of PML-nuclear body formation. Mol. Cell 24, 331-339.
54. Song, J., Durrin, L. K., Wilkinson, T. A., Krontiris, T. G. and Chen, Y. (2004). Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. USA 101, 14373-14378.
55. Stelter, P. and Ulrich, H. D. (2003). Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425, 188-191.
56. Tashiro, S., Kotomura, N., Shinohara, A., Tanaka, K., Ueda, K. and Kamada, N. (1996). S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene 12, 2165-2170.
57. Tashiro, S., Walter, J., Shinohara, A., Kamada, N. and Cremer, T. (2000). Rad51 accumulation at sites of DNA damage and in postreplicative chromatin. J. Cell Biol. 150, 283-292.
58. Thorslund, T., McIlwraith, M. J., Compton, S. A., Lekomtsev, S., Petronczki, M., Griffith, J. D. and West, S. C. (2010). The breast cancer tumor suppressor BRCA2 promotes the specific targeting of RAD51 to single-stranded DNA. Nat. Struct. Mol. Biol. 17, 1263-1265.
59. Ulrich, H. D. (2012). Ubiquitin and SUMO in DNA repair at a glance. J. Cell Sci. 125, 249-254.
60. Wyman, C. and Kanaar, R. (2006). DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40, 363-383.
61. Yan, J., Yang, X. P., Kim, Y. S., Joo, J. H. and Jetten, A. M. (2007). RAP80 interacts with the SUMO-conjugating enzyme UBC9 and is a novel target for sumoylation. Biochem. Biophys. Res. Commun. 362, 132-138.
62. Yin, Y., Seifert, A., Chua, J. S., Maure, J. F., Golebiowski, F. and Hay, R. T. (2012). SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 26, 1196-1208.
63. Yu, D. S., Sonoda, E., Takeda, S., Huang, C. L., Pellegrini, L., Blundell, T. L. and Venkitaraman, A. R. (2003). Dynamic control of Rad51 recombinase by selfassociation and interaction with BRCA2. Mol. Cell 12, 1029-1041.
64. Yurchenko, V., Xue, Z. and Sadofsky, M. J. (2006). SUMO modification of human XRCC4 regulates its localization and function in DNA double-strand break repair. Mol. Cell. Biol. 26, 1786-1794.
65. Zaidi, S. K., Young, D. W., Javed, A., Pratap, J., Montecino, M., van Wijnen, A., Lian, J. B., Stein, J. L. and Stein, G. S. (2007). Nuclear microenvironments in biological control and cancer. Nat. Rev. Cancer 7, 454-463.