UV-sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair

Nature Genetics

Volumn 44, Issue 5, 2012, Pages 598-602

  Schwertman, Petra ^a   Lagarou, Anna ^b   Dekkers, Dick H W ^a   Raams, Anja ^a   Van Der Hoek, Adriana C ^a   Laffeber, Charlie ^a   Hoeijmakers, Jan H J ^a   Demmers, Jeroen A A ^a   Fousteri, Maria ^b   Vermeulen, Wim ^a   Marteijn, Jurgen A ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ERCC6 PROTEIN; ESTERASE; RNA POLYMERASE II; SCAFFOLD PROTEIN; UBIQUITINATED PROTEIN; ULTRAVIOLET STIMULATED SCAFFOLD PROTEIN A; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; EXCISION REPAIR; GENE EXPRESSION; GENE SILENCING; PHOTOSENSITIVITY DISORDER; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEOMICS; REGULATORY MECHANISM; TRANSCRIPTION COUPLED NUCLEOTIDE EXCISION REPAIR; UBIQUITINATION; ULTRAVIOLET IRRADIATION; ULTRAVIOLET SENSITIVE SYNDROME;

CARRIER PROTEINS; CELLS, CULTURED; CHROMATIN; COCKAYNE SYNDROME; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA REPAIR ENZYMES; HUMANS; IMMUNOPRECIPITATION; MUTATION; PROTEOMICS; RNA POLYMERASE II; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; UBIQUITIN; UBIQUITIN THIOLESTERASE; ULTRAVIOLET RAYS;

EID: 84860330462     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.2230     Document Type: Article

References (46)

1. Hanawalt, P.C. & Spivak, G. Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell Biol. 9, 958-970 (2008).
2. Bergink, S., Jaspers, N.G. & Vermeulen, W. Regulation of UV-induced DNA damage response by ubiquitylation. DNA Repair (Amst.) 6, 1231-1242 (2007). (Pubitemid 47238678)
3. Itoh, T., Ono, T. & Yamaizumi, M. A new UV-sensitive syndrome not belonging to any complementation groups of xeroderma pigmentosum or Cockayne syndrome: siblings showing biochemical characteristics of Cockayne syndrome without typical clinical manifestations. Mutat. Res. 314, 233-248 (1994). (Pubitemid 24128667)
4. Hoeijmakers, J.H. DNA damage, aging, and cancer. N. Engl. J. Med. 361, 1475-1485 (2009).
5. Hendriks, G. et al. Transcription-dependent cytosine deamination is a novel mechanism in ultraviolet light-induced mutagenesis. Curr. Biol. 20, 170-175 (2010).
6. Sugasawa, K. et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121, 387-400 (2005). (Pubitemid 40692299)
7. Rapić-Otrin, V., McLenigan, M.P., Bisi, D.C., Gonzalez, M. & Levine, A.S. Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res. 30, 2588-2598 (2002). (Pubitemid 34619012)
8. Bregman, D.B. et al. UV-induced ubiquitination of RNA polymerase II: a novel modification deficient in Cockayne syndrome cells. Proc. Natl. Acad. Sci. USA 93, 11586-11590 (1996). (Pubitemid 26347165)
9. Groisman, R. et al. CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome. Genes Dev. 20, 1429-1434 (2006). (Pubitemid 43830649)
10. Anindya, R., Aygun, O. & Svejstrup, J.Q. Damage-induced ubiquitylation of human RNA polymerase II by the ubiquitin ligase Nedd4, but not Cockayne syndrome proteins or BRCA1. Mol. Cell 28, 386-397 (2007). (Pubitemid 350047546)
11. Fujimuro, M., Sawada, H. & Yokosawa, H. Production and characterization of monoclonal antibodies specific to multi-ubiquitin chains of polyubiquitinated proteins. FEBS Lett. 349, 173-180 (1994). (Pubitemid 24263257)
12. Nagase, T., Kikuno, R., Ishikawa, K., Hirosawa, M. & Ohara, O. Prediction of the coding sequences of unidentified human genes. XVII. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res. 7, 143-150 (2000).
13. Mizuno, E., Kawahata, K., Kato, M., Kitamura, N. & Komada, M. STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif. Mol. Biol. Cell 14, 3675-3689 (2003). (Pubitemid 37151618)
14. Bateman, A., Coggill, P. & Finn, R.D. DUFs: families in search of function. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 1148-1152 (2010).
15. Jaspers, N.G. et al. Anti-tumour compounds illudin S and Irofulven induce DNA lesions ignored by global repair and exclusively processed by transcription-and replication-coupled repair pathways. DNA Repair (Amst.) 1, 1027-1038 (2002). (Pubitemid 35335828)
16. Nakazawa, Y., Yamashita, S., Lehmann, A.R. & Ogi, T. A semi-automated non-radioactive system for measuring recovery of RNA synthesis and unscheduled DNA synthesis using ethynyluracil derivatives. DNA Repair (Amst.) 9, 506-516 (2010).
17. Spivak, G. UV-sensitive syndrome. Mutat. Res. 577, 162-169 (2005). (Pubitemid 41225496)
18. Horibata, K. et al. Complete absence of Cockayne syndrome group B gene product gives rise to UV-sensitive syndrome but not Cockayne syndrome. Proc. Natl. Acad. Sci. USA 101, 15410-15415 (2004). (Pubitemid 39441555)
19. Nardo, T. et al. A UV-sensitive syndrome patient with a specific CSA mutation reveals separable roles for CSA in response to UV and oxidative DNA damage. Proc. Natl. Acad. Sci. USA 106, 6209-6214 (2009).
20. Zhang, X. et al. Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair. Nat. Genet. published online (1 April 2012); doi:10.1038ng.2228.
21. Nakazawa, Y. et al. Mutations in UVSSA cause UV-sensitive syndrome and impair RNA polymerase IIo processing in transcription-coupled nucleotide-excision repair. Nat. Genet. published online (1 April 2012); doi:10.1038ng.2229.
22. Dinant, C. et al. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J. Cell Sci. 120, 2731-2740 (2007). (Pubitemid 47323879)
23. Volker, M. et al. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8, 213-224 (2001). (Pubitemid 32772919)
24. Kimura, H., Sugaya, K. & Cook, P.R. The transcription cycle of RNA polymerase II in living cells. J. Cell Biol. 159, 777-782 (2002). (Pubitemid 36008360)
25. van den Boom, V. et al. DNA damage stabilizes interaction of CSB with the transcription elongation machinery. J. Cell Biol. 166, 27-36 (2004). (Pubitemid 38931914)
26. Fousteri, M., Vermeulen, W., van Zeeland, A.A. & Mullenders, L.H. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell 23, 471-482 (2006). (Pubitemid 44226450)
27. Cdh-1-mediated proteolysis of Claspin. J. Cell Biol. 184, 13-19 (2009).
28. Khoronenkova, S.V., Dianova, I.I., Parsons, J.L. & Dianov, G.L. USP7/HAUSP stimulates repair of oxidative DNA lesions. Nucleic Acids Res. 39, 2604-2609 (2011).
29. Li, M. et al. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416, 648-653 (2002). (Pubitemid 34406767)
30. Meulmeester, E. et al. Loss of HAUSP-mediated deubiquitination contributes to DNA damage-induced destabilization of Hdmx and Hdm2. Mol. Cell 18, 565-576 (2005). (Pubitemid 40726233)
31. Wei, L. et al. BRCA1 contributes to transcription-coupled repair of DNA damage through polyubiquitination and degradation of Cockayne syndrome B protein. Cancer Sci. 102, 1840-1847 (2011).
32. Nicholson, B. & Suresh Kumar, K.G. The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem. Biophys. 60, 61-68 (2011).
33. Spivak, G. & Hanawalt, P.C. Host cell reactivation of plasmids containing oxidative DNA lesions is defective in Cockayne syndrome but normal in UV-sensitive syndrome fibroblasts. DNA Repair (Amst.) 5, 13-22 (2006). (Pubitemid 41832507)
34. D'Errico, M. et al. The role of CSA in the response to oxidative DNA damage in human cells. Oncogene 26, 4336-4343 (2007). (Pubitemid 47014469)
35. Gorgels, T.G. et al. Retinal degeneration and ionizing radiation hypersensitivity in a mouse model for Cockayne syndrome. Mol. Cell. Biol. 27, 1433-1441 (2007). (Pubitemid 46239824)
36. Newman, J.C., Bailey, A.D., Fan, H.Y., Pavelitz, T. & Weiner, A.M. An abundant evolutionarily conserved CSB-PiggyBac fusion protein expressed in Cockayne syndrome. PLoS Genet. 4, e1000031 (2008).
37. Campeau, E. et al. A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS ONE 4, e6529 (2009).
38. Epping, M.T. et al. TSPYL5 suppresses p53 levels and function by physical interaction with USP7. Nat. Cell Biol. 13, 102-108 (2011).
39. Sugaya, K., Vigneron, M. & Cook, P.R. Mammalian cell lines expressing functional RNA polymerase II tagged with the green fluorescent protein. J. Cell Sci. 113, 2679-2683 (2000). (Pubitemid 30649569)
40. Wilm, M. et al. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379, 466-469 (1996).
41. Cox, J. et al. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4, 698-705 (2009).
42. Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805 (2011).
43. Keller, A., Nesvizhskii, A.I., Kolker, E. & Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392 (2002). (Pubitemid 35215372)
44. Nesvizhskii, A.I., Keller, A., Kolker, E. & Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658 (2003). (Pubitemid 37082259)
45. Houtsmuller, A.B. & Vermeulen, W. Macromolecular dynamics in living cell nuclei revealed by fluorescence redistribution after photobleaching. Histochem. Cell Biol. 115, 13-21 (2001). (Pubitemid 32202049)
46. Marteijn, J.A. et al. Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response. J. Cell Biol. 186, 835-847 (2009).