Rap80 protein recruitment to DNA double-strand breaks requires binding to both small ubiquitin-like modifier (SUMO) and ubiquitin conjugates

Journal of Biological Chemistry

Volumn 287, Issue 30, 2012, Pages 25510-25519

  Hu, Xin ^a   Paul, Atanu ^a,b   Wangs, Bin ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DAMAGES; DOUBLE-STRAND BREAKS; MOLECULAR BASIS; REPAIR PROTEINS; SMALL UBIQUITIN-LIKE MODIFIERS; UBIQUITIN;

DNA; IONIZING RADIATION;

PROTEINS;

BINDING PROTEIN; BRCA1 PROTEIN; CELL DNA; LYSINE; PROTEIN RAP80; SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CELL FUNCTION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RADIOSENSITIVITY;

AMINO ACID MOTIFS; ANIMALS; BRCA1 PROTEIN; CARRIER PROTEINS; CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; HUMANS; MICE; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; TRANSCRIPTION FACTORS; UBIQUITINS;

EID: 84864076551     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.374116     Document Type: Article

References (31)

1. Haglund, K., and Dikic, I. (2005) Ubiquitylation and cell signaling. EMBO J. 24, 3353-3359 (Pubitemid 41486773)
2. Gareau, J. R., and Lima, C. D. (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation, and recognition. Nat. Rev. Mol. Cell Biol. 11, 861-871
3. Bergink, S., and Jentsch, S. (2009) Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458, 461-467
4. Bekker-Jensen, S., and Mailand, N. (2011) The ubiquitin- and SUMO-dependent signaling response toDNAdouble-strand breaks. FEBS Lett. 585, 2914-2919
5. Harper, J. W., and Elledge, S. J. (2007) The DNA damage response: ten years after. Mol. Cell 28, 739-745 (Pubitemid 350217064)
6. 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
7. Ciccia, A., and Elledge, S. J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204
8. Wang, B. (2012) BRCA1 tumor suppressor network: focusing on its tail. Cell Biosci. 2, 6
9. Wang, B., Matsuoka, S., Ballif, B. A., Zhang, D., Smogorzewska, A., Gygi, S. P., and Elledge, S. J. (2007) Abraxas and RAP80 form a BRCA1 protein complex required for theDNAdamage response. Science 316, 1194-1198 (Pubitemid 46877482)
10. Liu, Z., Wu, J., and Yu, X. (2007) CCDC98 targets BRCA1 to DNA damage sites. Nat. Struct. Mol. Biol. 14, 716-720 (Pubitemid 47220064)
11. Kim, H., Huang, J., and Chen, J. (2007) CCDC98 is a BRCA1-BRCT domain- binding protein involved in the DNA damage response. Nat. Struct. Mol. Biol. 14, 710-715 (Pubitemid 47220062)
12. Hu, X., Kim, J. A., Castillo, A., Huang, M., Liu, J., and Wang, B. (2011) NBA1/MERIT40 and BRE interaction is required for the integrity of two distinct deubiquitinating enzyme BRCC36-containing complexes. J. Biol. Chem. 286, 11734-11745
13. 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
14. Morris, J. R., Boutell, C., Keppler, M., Densham, R., Weekes, D., Alamshah, A., Butler, L., Galanty, Y., Pangon, L., Kiuchi, T., Ng, T., and Solomon, E. (2009) The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890
15. Hay, R. T. (2005) SUMO: a history of modification. Mol. Cell 18, 1-12
16. Tatham, M. H., Jaffray, E., Vaughan, O. A., Desterro, J. M., Botting, C. H., Naismith, J. H., and Hay, R. T. (2001) Polymeric chains of SUMO2 and SUMO3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276, 35368-35374
17. Matic, I., van Hagen, M., Schimmel, J., Macek, B., Ogg, S. C., Tatham, M. H., Hay, R. T., Lamond, A. I., Mann, M., and Vertegaal, A. C. (2008) In vivo identification of human small ubiquitin-like modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy. Mol. Cell. Proteomics 7, 132-144 (Pubitemid 351248239)
18. 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. U.S.A. 101, 14373-14378 (Pubitemid 39346756)
19. Hecker, C. M., Rabiller, M., Haglund, K., Bayer, P., and Dikic, I. (2006) Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 281, 16117-16127 (Pubitemid 43848507)
20. Wang, B., and Elledge, S. J. (2007) Ubc13/Rnf8 ubiquitin ligases control focus formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. U.S.A. 104, 20759-20763
21. Wang, B., Hurov, K., Hofmann, K., and Elledge, S. J. (2009) NBA1, a new player in the Brca1-A complex, is required for DNA damage resistance and checkpoint control. Genes Dev. 23, 729-739
22. Saitoh, H., and Hinchey, J. (2000) Functional heterogeneity of small ubiquitin- related protein modifiers SUMO1 versus SUMO2/3. J. Biol. Chem. 275, 6252-6258 (Pubitemid 30129915)
23. Chang, C. C., Naik, M. T., Huang, Y. S., Jeng, J. C., Liao, P. H., Kuo, H. Y., Ho, C. C., Hsieh, Y. L., Lin, C. H., Huang, N. J., Naik, N. M., Kung, C. C., Lin, S. Y., Chen, R. H., Chang, K. S., Huang, T. H., and Shih, H. M. (2011) Structural and functional roles of Daxx SIM phosphorylation in SUMO paralog-selective binding and apoptosis modulation. Mol. Cell 42, 62-74
24. Sobhian, B., Shao, G., Lilli, D. R., Culhane, A. C., Moreau, L. A., Xia, B., Livingston, D. M., and Greenberg, R. A. (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316, 1198-1202 (Pubitemid 46877483)
25. Kim, H., Chen, J., and Yu, X. (2007) Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316, 1202-1205 (Pubitemid 46877484)
26. Huang, J., Huen, M. S., Kim, H., Leung, C. C., Glover, J. N., Yu, X., and Chen, J. (2009) RAD18 transmits DNA damage signaling to elicit homologous recombination repair. Nat. Cell Biol. 11, 592-603
27. Tatham, M. H., Geoffroy, M. C., Shen, L., Plechanovova, A., Hattersley, N., Jaffray, E. G., Palvimo, J. J., and Hay, R. T. (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10, 538-546 (Pubitemid 351627373)
28. Golebiowski, F., Matic, I., Tatham, M. H., Cole, C., Yin, Y., Nakamura, A., Cox, J., Barton, G. J., Mann, M., and Hay, R. T. (2009) System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2, ra24
29. Nathan, D., Ingvarsdottir, K., Sterner, D. E., Bylebyl, G. R., Dokmanovic, M., Dorsey, J. A., Whelan, K. A., Krsmanovic, M., Lane, W. S., Meluh, P. B., Johnson, E. S., and Berger, S. L. (2006) Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev. 20, 966-976
30. Shiio, Y., and Eisenman, R. N. (2003) Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. U.S.A. 100, 13225-13230 (Pubitemid 37444723)
31. 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 (Pubitemid 47296303)