RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage

Science Signaling

Volumn 5, Issue 253, 2012, Pages

  Guzzo, Catherine M ^a   Berndsen, Christopher E ^b,d   Zhu, Jianmei ^a   Gupta, Vibhor ^c   Datta, Ajit ^b,e   Greenberg, Roger A ^c   Wolberger, Cynthia ^b   Matunis, Michael J ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d JAMES MADISON UNIVERSITY   (United States)

^e BOSE INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; BRCA1 PROTEIN; RAP80 PROTEIN; RNF4 PROTEIN; SMALL INTERFERING RNA; SUMO PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER SUSCEPTIBILITY; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN MOTIF; RNA INTERFERENCE; SUMOYLATION; UBIQUITINATION;

AMINO ACID MOTIFS; BRCA1 PROTEIN; CARRIER PROTEINS; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HUMANS; NUCLEAR PROTEINS; SUMO-1 PROTEIN; SUMOYLATION; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINS;

EID: 84870760201     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003485     Document Type: Article

References (40)

1. A. Ciccia, S. J. Elledge, The DNA damage response: Making it safe to play with knives. Mol. Cell 40, 179-204 (2010).
2. A. Bensimon, A. Schmidt, Y. Ziv, R. Elkon, S. Y. Wang, D. J. Chen, R. Aebersold, Y. Shiloh, ATM-dependent and -independent dynamics of the nuclear phosphoproteome after DNA damage. Sci. Signal. 3, rs3 (2010).
3. A. Rupnik, N. F. Lowndes, M. Grenon, MRN and the race to the break. Chromosoma 119, 115-135 (2010).
4. S. Bekker-Jensen, N. Mailand, The ubiquitin- and SUMO-dependent signaling response to DNA double-strand breaks. FEBS Lett. 585, 2914-2919 (2011).
5. S. Bergink, S. Jentsch, Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458, 461-467 (2009).
6. T. E. Messick, R. A. Greenberg, The ubiquitin landscape at DNA double-strand breaks. J. Cell Biol. 187, 319-326 (2009).
7. M. S. Luijsterburg, H. van Attikum, Close encounters of the RNF8th kind: When chromatin meets DNA repair. Curr. Opin. Cell Biol. 24, 439-447 (2012).
8. H. Kim, J. Chen, X. Yu, Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316, 1202-1205 (2007).
9. B. Sobhian, G. Shao, D. R. Lilli, A. C. Culhane, L. A. Moreau, B. Xia, D. M. Livingston, R. A. Greenberg, RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316, 1198-1202 (2007).
10. B.Wang, S. Matsuoka, B. A. Ballif, D. Zhang, A. Smogorzewska, S. P. Gygi, S. J. Elledge, Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316, 1194-1198 (2007).
11. Y. Galanty, R. Belotserkovskaya, J. Coates, S. Polo, K. M. Miller, S. P. Jackson, Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939 (2009).
12. J. R. Morris, C. Boutell, M. Keppler, R. Densham, D. Weekes, A. Alamshah, L. Butler, Y. Galanty, L. Pangon, T. Kiuchi, T. Ng, E. Solomon, The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890 (2009).
13. J. R. Danielsen, L. K. Povlsen, B. H. Villumsen, W. Streicher, J. Nilsson, M. Wikström, S. Bekker-Jensen, N. Mailand, DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding Zinc finger. J. Cell Biol. 197, 179-187 (2012).
14. R. C. Burgess, S. Rahman, M. Lisby, R. Rothstein, X. Zhao, The Slx5-Slx8 complex affects sumoylation of DNA repair proteins and negatively regulates recombination. Mol. Cell. Biol. 27, 6153-6162 (2007).
15. A. Kosoy, T. M. Calonge, E. A. Outwin, M. J. O'Connell, Fission yeast Rnf4 homologs are required for DNA repair. J. Biol. Chem. 282, 20388-20394 (2007).
16. J. Prudden, S. Pebernard, G. Raffa, D. A. Slavin, J. J. Perry, J. A. Tainer, C. H. McGowan, M. N. Boddy, SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 26, 4089-4101 (2007).
17. M. C. Geoffroy, R. T. Hay, An additional role for SUMO in ubiquitin-mediated proteolysis. Nat. Rev. Mol. Cell Biol. 10, 564-568 (2009).
18. M.Abed, K. C. Barry, D. Kenyagin, B.Koltun, T.M. Phippen, J. J. Delrow, S. M.Parkhurst, A. Orian, Degringolade, a SUMO-targeted ubiquitin ligase, inhibits Hairy/Groucho-mediated repression. EMBO J. 30, 1289-1301 (2011).
19. K. A. Fryrear, X. Guo, O. Kerscher, O. J. Semmes, The Sumo-targeted ubiquitin ligase RNF4 regulates the localization and function of the HTLV-1 oncoprotein Tax. Blood 119, 1173-1181 (2012).
20. B. Wang, K. Hurov, K. Hofmann, S. J. Elledge, NBA1, a new player in the Brca1 A complex, is required for DNA damage resistance and checkpoint control. Genes Dev. 23, 729-739 (2009).
21. J. Zhu, S. Zhu, C. M. Guzzo, N. A. Ellis, K. S. Sung, C. Y. Choi, M. J. Matunis, Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralogselective SUMO modification. J. Biol. Chem. 283, 29405-29415 (2008).
22. J. J. Sims, R. E. Cohen, Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of Rap80. Mol. Cell 33, 775-783 (2009).
23. Y.Galanty, R.Belotserkovskaya, J.Coates,S.P. Jackson,RNF4, aSUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev. 26, 1179-1195 (2012).
24. K. Luo, H. Zhang, L. Wang, J. Yuan, Z. Lou, Sumoylation of MDC1 is important for proper DNA damage response. EMBO J. 31, 3008-3019 (2012).
25. Y. Yin, A. Seifert, J. S. Chua, J. F. Maure, F. Golebiowski, R. T. Hay, SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev. 26, 1196-1208 (2012).
26. C. M. Pickart, D. Fushman, Polyubiquitin chains: Polymeric protein signals. Curr. Opin. Chem. Biol. 8, 610-616 (2004).
27. J. Schimmel, K. M. Larsen, I. Matic, M. van Hagen, J. Cox, M. Mann, J. S. Andersen, A. C. Vertegaal, The ubiquitin-proteasome system is a key component of the SUMO-2/3 cycle. Mol. Cell. Proteomics 7, 2107-2122 (2008).
28. M. H. Tatham, I. Matic, M. Mann, R. T. Hay, Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci. Signal. 4, rs4 (2011).
29. P. Schuck, On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 320, 104-124 (2003).
30. A. A. Armstrong, F. Mohideen, C. D. Lima, Recognition of SUMO-modified PCNA requires tandem receptor motifs in Srs2. Nature 483, 59-63 (2012).
31. S. Panier, Y. Ichijima, A. Fradet-Turcotte, C. C. Leung, L. Kaustov, C. H. Arrowsmith, D. Durocher, Tandem protein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. Mol. Cell 47, 383-395 (2012).
32. G. S. Stewart, S. Panier, K. Townsend, A. K. Al-Hakim, N. K. Kolas, E. S. Miller, S. Nakada, J. Ylanko, S. Olivarius, M. Mendez, C. Oldreive, J. Wildenhain, A. Tagliaferro, L. Pelletier, N. Taubenheim, A. Durandy, P. J. Byrd, T. Stankovic, A. M. Taylor, D. Durocher, The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420-434 (2009).
33. A. Y. Alontaga, E. Bobkova, Y. Chen, Biochemical analysis of protein SUMOylation. Curr. Protoc. Mol. Biol. Chapter 10, Unit10.29 (2012).
34. R. Bruderer, M. H. Tatham, A. Plechanovova, I. Matic, A. K. Garg, R. T. Hay, Purification and identification of endogenous polySUMO conjugates. EMBO Rep. 12, 142-148 (2011).
35. A. M. Moilanen, H. Poukka, U. Karvonen, M. Häkli, O. A. Jänne, J. J. Palvimo, Identification of a novel RING finger protein as a coregulator in steroid receptor-mediated gene transcription. Mol. Cell. Biol. 18, 5128-5139 (1998).
36. X. V. Hu, T.M. Rodrigues, H. Tao, R. K. Baker, L. Miraglia, A. P. Orth, G. E. Lyons, P. G. Schultz, X. Wu, Identification of RING finger protein 4 (RNF4) as a modulator of DNA demethylation through a functional genomics screen. Proc. Natl. Acad. Sci. U.S.A. 107, 15087-15092 (2010).
37. X. D. Zhang, J. Goeres, H. Zhang, T. J. Yen, A. C. Porter, M. J. Matunis, SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol. Cell 29, 729-741 (2008).
38. C. M. Pickart, S. Raasi, Controlled synthesis of polyubiquitin chains. Methods Enzymol. 399, 21-36 (2005).
39. T. M. Laue, B. D. Shah, T. M. Ridgeway, S. L. Pelletier, in Analytical Ultracentrifugation in Biochemistry and Polymer Science, S. E. Harding, A. J. Rowe, J. C. Horton, Eds. (The Royal Society of Chemistry, Cambridge, 1992), pp. 90-125.
40. P. Schuck, Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619 (2000).