SUMOylation of xeroderma pigmentosum group C protein regulates DNA damage recognition during nucleotide excision repair

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Akita, Masaki ^a   Tak, Yon Soo ^a   Shimura, Tsutomu ^a   Matsumoto, Syota ^a   Okuda Shimizu, Yuki ^b   Shimizu, Yuichiro ^b   Nishi, Ryotaro ^a,b   Saitoh, Hisato ^c   Iwai, Shigenori ^d   Mori, Toshio ^e   Ikura, Tsuyoshi ^f   Sakai, Wataru ^a   Hanaoka, Fumio ^b,g   Sugasawa, Kaoru ^a,b  

^a KOBE UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e NARA MEDICAL UNIVERSITY   (Japan)

^f KYOTO UNIVERSITY   (Japan)

^g GAKUSHUIN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DDB2 PROTEIN, HUMAN; DNA BINDING PROTEIN; PROTEIN BINDING; SUMO 1 PROTEIN; UBIQUITIN CONJUGATING ENZYME; XPC PROTEIN, HUMAN;

CELL LINE; DNA DAMAGE; DNA REPAIR; GENETICS; HUMAN; METABOLISM; MUTATION; RADIATION RESPONSE; SUMOYLATION; UBIQUITINATION; ULTRAVIOLET RADIATION;

CELL LINE; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; MUTATION; PROTEIN BINDING; SUMO-1 PROTEIN; SUMOYLATION; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION; ULTRAVIOLET RAYS;

EID: 84930655376     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep10984     Document Type: Article

References (48)

1. Riedl, T., Hanaoka, F. & Egly, J. M. The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J. 22, 5293-5303 (2003).
2. Sugasawa, K. et al. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell 2, 223-232 (1998).
3. Volker, M. et al. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8, 213-224 (2001).
4. Min, J. H. & Pavletich, N. P. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 449, 570-575 (2007).
5. Sugasawa, K. et al. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 15, 507-521 (2001).
6. Sugasawa, K., Shimizu, Y., Iwai, S. & Hanaoka, F. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst.) 1, 95-107 (2002).
7. Araújo, S. J. et al. Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK. Genes Dev. 14, 349-359 (2000).
8. Marteijn, J. A., Lans, H., Vermeulen, W. & Hoeijmakers, J. H. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat. Rev. Mol. Cell Biol. 15, 465-481 (2014).
9. Schärer, O. D. Nucleotide excision repair in eukaryotes. Cold Spring Harb. Perspect. Biol. 5, a012609 (2013).
10. Fujiwara, Y. et al. Characterization of DNA recognition by the human UV-damaged DNA-binding protein. J. Biol. Chem. 274, 20027-20033 (1999).
11. Wittschieben, B. O., Iwai, S. & Wood, R. D. DDB1-DDB2 (xeroderma pigmentosum group E) protein complex recognizes a cyclobutane pyrimidine dimer, mismatches, apurinic/apyrimidinic sites, and compound lesions in DNA. J. Biol. Chem. 280, 39982-39989 (2005).
12. Fitch, M. E., Nakajima, S., Yasui, A. & Ford, J. M. In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product. J. Biol. Chem. 278, 46906-46910 (2003).
13. Moser, J. et al. The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair (Amst.) 4, 571-582 (2005).
14. Wang, Q. E., Zhu, Q., Wani, G., Chen, J. & Wani, A. A. UV radiation-induced XPC translocation within chromatin is mediated by damaged-DNA binding protein, DDB2. Carcinogenesis 25, 1033-1043 (2004).
15. Hwang, B. J., Toering, S., Francke, U. & Chu, G. p48 Activates a UV-damaged-DNA binding factor and is defective in xeroderma pigmentosum group E cells that lack binding activity. Mol. Cell. Biol. 18, 4391-4399 (1998).
16. Tang, J. Y., Hwang, B. J., Ford, J. M., Hanawalt, P. C. & Chu, G. Xeroderma pigmentosum p48 gene enhances global genomic repair and suppresses UV-induced mutagenesis. Mol. Cell 5, 737-744 (2000).
17. Scrima, A. et al. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135, 1213-1223 (2008).
18. Groisman, R. et al. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113, 357-367 (2003).
19. Kapetanaki, M. G. et al. The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl. Acad. Sci. U.S.A. 103, 2588-2593 (2006).
20. Sugasawa, K. et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121, 387-400 (2005).
21. Wang, H. et al. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 22, 383-394 (2006).
22. Sugasawa, K. UV-induced ubiquitylation of XPC complex, the UV-DDB-ubiquitin ligase complex, and DNA repair. J. Mol. Histol. 37, 189-202 (2006).
23. Matsumoto, S. et al. Functional regulation of the DNA damage-recognition factor DDB2 by ubiquitination and interaction with xeroderma pigmentosum group C protein. Nucleic Acids Res 43, 1700-1713 (2015).
24. Cubeñas-Potts, C. & Matunis, M. J. SUMO: a multifaceted modifier of chromatin structure and function. Dev. Cell 24, 1-12 (2013).
25. Jackson, S. P. & Durocher, D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49, 795-807 (2013).
26. Rodriguez, M. S., Dargemont, C. & Hay, R. T. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654-12659 (2001).
27. Wang, Q. E. et al. Ubiquitylation-independent degradation of Xeroderma pigmentosum group C protein is required for efficient nucleotide excision repair. Nucleic Acids Res. 35, 5338-5350 (2007).
28. Nishi, R. et al. UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells. DNA Repair (Amst.) 8, 767-776 (2009).
29. Hwang, B. J., Ford, J. M., Hanawalt, P. C. & Chu, G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl. Acad. Sci. U.S.A. 96, 424-428 (1999).
30. Poulsen, S. L. et al. RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J. Cell Biol. 201, 797-807 (2013).
31. Wang, Q. E. et al. DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation. Nucleic Acids Res. 33, 4023-4034 (2005).
32. Bunick, C. G., Miller, M. R., Fuller, B. E., Fanning, E. & Chazin, W. J. Biochemical and structural domain analysis of xeroderma pigmentosum complementation group C protein. Biochemistry 45, 14965-14979 (2006).
33. Hendriks, I. A. et al. Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol 21, 927-936 (2014).
34. Saitoh, H. & Hinchey, J. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. Journal of Biological Chemistry 275, 6252-6258 (2000).
35. Sugasawa, K., Akagi, J., Nishi, R., Iwai, S. & Hanaoka, F. Two-step recognition of DNA damage for mammalian nucleotide excision repair: Directional binding of the XPC complex and DNA strand scanning. Mol. Cell 36, 642-653 (2009).
36. Fischer, E. S. et al. The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 147, 1024-1039 (2011).
37. Psakhye, I. & Jentsch, S. Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807-820 (2012).
38. Klein, U. R. & Nigg, E. A. SUMO-dependent regulation of centrin-2. J. Cell. Sci. 122, 3312-3321 (2009).
39. Tsuge, M. et al. SUMOylation of damaged DNA-binding protein DDB2. Biochem. Biophys. Res. Commun. 438, 26-31 (2013).
40. Bergink, S. et al. Role of Cdc48/p97 as a SUMO-targeted segregase curbing Rad51-Rad52 interaction. Nat. Cell Biol. 15, 526-532 (2013).
41. Nie, M. et al. Dual recruitment of Cdc48 (p97)-Ufd1-Npl4 ubiquitin-selective segregase by small ubiquitin-like modifier protein (SUMO) and ubiquitin in SUMO-targeted ubiquitin ligase-mediated genome stability functions. J. Biol. Chem. 287, 29610-29619 (2012).
42. Puumalainen, M. R. et al. Chromatin retention of DNA damage sensors DDB2 and XPC through loss of p97 segregase causes genotoxicity. Nat. Commun. 5, 3695 (2014).
43. Nishi, R. et al. Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol. Cell. Biol. 25, 5664-5674 (2005).
44. Nishi, R., Sakai, W., Tone, D., Hanaoka, F. & Sugasawa, K. Structure-function analysis of the EF-hand protein centrin-2 for its intracellular localization and nucleotide excision repair. Nucleic Acids Res. 41, 6917-6929 (2013).
45. Niwa, H., Yamamura, K. & Miyazaki, J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199 (1991).
46. Mori, T. et al. Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4) photoproduct from the same mouse immunized with ultraviolet-irradiated DNA. Photochem. Photobiol. 54, 225-232 (1991).
47. Yasuda, G. et al. In vivo destabilization and functional defects of the xeroderma pigmentosum C protein caused by a pathogenic missense mutation. Mol. Cell. Biol. 27, 6606-6614 (2007).
48. Sugasawa, K. et al. HHR23B, a human Rad23 homolog, stimulates XPC protein in nucleotide excision repair in vitro. Mol. Cell. Biol. 16, 4852-4861 (1996).