Ubiquitin at work: The ubiquitous regulation of the damage recognition step of NER

Experimental Cell Research

Volumn 329, Issue 1, 2014, Pages 101-109

  van Cuijk, Loes ^a   Vermeulen, Wim ^a   Marteijn, Jurgen A ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Damage recognition; K48 ubiquitin chains; K63 ubiquitin chains; Nucleotide excision repair (NER); Post translational modification (PTM); Ubiquitin

Indexed keywords

CSA PROTEIN; CSB PROTEIN; DDB1 PROTEIN; DDB2 PROTEIN; PROTEASOME; PROTEIN; RNA POLYMERASE II; UBIQUITIN; UNCLASSIFIED DRUG; UVSSA PROTEIN; XERODERMA PIGMENTOSUM GROUP C PROTEIN;

DNA BINDING; DNA DAMAGE; EXCISION REPAIR; GENOME; HUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEOMICS; REVIEW; SUMOYLATION; UBIQUITINATION; ANIMAL; DNA REPAIR; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN PROCESSING;

ANIMALS; DNA DAMAGE; DNA REPAIR; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSCRIPTION, GENETIC; UBIQUITIN; UBIQUITINATION;

EID: 84919420749     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.07.018     Document Type: Review

References (65)

1. Scharer O.D. Nucleotide excision repair in eukaryotes. Cold Spring Harb. Perspect. Biol. 2013, 5(10):a012609.
2. Lehmann A.R. DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 2003, 85(11):1101-1111.
3. Spivak G. UV-sensitive syndrome. Mutat. Res. 2005, 577(1-2):162-169.
4. Sugasawa K., et al. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell 1998, 2(2):223-232.
5. Hoogstraten D., et al. Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J. Cell Sci. 2008, 121(Pt 17):2850-2859.
6. Sugasawa K., et al. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 2001, 15(5):507-521.
7. Wakasugi M., et al. DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J. Biol. Chem. 2002, 277(3):1637-1640.
8. Scrima A., et al. Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 2008, 135(7):1213-1223.
9. Compe E., Egly J.M. TFIIH: when transcription met DNA repair. Nat. Rev. Mol. Cell Biol. 2012, 13(6):343-354.
10. Sugasawa K., et al. Two-step recognition of DNA damage for mammalian nucleotide excision repair: directional binding of the XPC complex and DNA strand scanning. Mol. Cell 2009, 36(4):642-653.
11. Mathieu N., et al. DNA quality control by a lesion sensor pocket of the xeroderma pigmentosum group D helicase subunit of TFIIH. Curr. Biol. 2013, 23(3):204-212.
12. Camenisch U., et al. Recognition of helical kinks by xeroderma pigmentosum group A protein triggers DNA excision repair. Nat. Struct. Mol. Biol. 2006, 13(3):278-284.
13. de Laat W.L., et al. DNA-binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev. 1998, 12(16):2598-2609.
14. Staresincic L., et al. Coordination of dual incision and repair synthesis in human nucleotide excision repair. EMBO J. 2009, 28(8):1111-1120.
15. Ogi T., et al. Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol. Cell 2010, 37(5):714-727.
16. Moser J., et al. Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III alpha in a cell-cycle-specific manner. Mol. Cell 2007, 27(2):311-323.
17. Vermeulen W., Fousteri M. Mammalian transcription-coupled excision repair. Cold Spring Harb. Perspect. Biol. 2013, 5(8):a012625.
18. Schwertman P., et al. UV-sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair. Nat. Genet. 2012, 44(5):598-602.
19. Zhang X., et al. Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair. Nat. Genet. 2012, 44(5):593-597.
20. Fousteri M., et al. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell 2006, 23(4):471-482.
21. Bergink S., Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 2009, 458(7237):461-467.
22. Jackson S.P., Durocher D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 2013, 49(5):795-807.
23. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
24. Kulathu Y., Komander D. Atypical ubiquitylation-the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol. 2012, 13(8):508-523.
25. Husnjak K., Dikic I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 2012, 81:291-322.
26. Jacq X., et al. Deubiquitylating enzymes and DNA damage response pathways. Cell. Biochem. Biophys. 2013, 67(1):25-43.
27. Povlsen L.K., et al. Systems-wide analysis of ubiquitylation dynamics reveals a key role for PAF15 ubiquitylation in DNA-damage bypass. Nat. Cell Biol. 2012, 14(10):1089-1098.
28. Kang T.H., Reardon J.T., Sancar A. Regulation of nucleotide excision repair activity by transcriptional and post-transcriptional control of the XPA protein. Nucleic Acids Res. 2011, 39(8):3176-3187.
29. 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. 2009, 186(6):835-847.
30. Hannah J., Zhou P. Regulation of DNA damage response pathways by the cullin-RING ubiquitin ligases. DNA Repair 2009, 8(4):536-543.
31. 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 2003, 113(3):357-367.
32. Sugasawa K., et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 2005, 121(3):387-400.
33. Matsuda N., et al. DDB2, the xeroderma pigmentosum group E gene product, is directly ubiquitylated by Cullin 4A-based ubiquitin ligase complex. DNA Repair 2005, 4(5):537-545.
34. 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. USA 2006, 103(8):2588-2593.
35. Lan L., et al. Monoubiquitinated histone H2A destabilizes photolesion-containing nucleosomes with concomitant release of UV-damaged DNA-binding protein E3 ligase. J. Biol. Chem. 2012, 287(15):12036-12049.
36. Wang H., et al. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 2006, 22(3):383-394.
37. Rapic-Otrin V., et al. Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res. 2002, 30(11):2588-2598.
38. Fischer E.S., et al. The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 2011, 147(5):1024-1039.
39. Puumalainen M.R., et al. Chromatin retention of DNA damage sensors DDB2 and XPC through loss of p97 segregase causes genotoxicity. Nat. Commun. 2014, 5:3695.
40. El-Mahdy M.A., et al. Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC. J. Biol. Chem. 2006, 281(19):13404-13411.
41. Liu L., et al. CUL4A abrogation augments DNA damage response and protection against skin carcinogenesis. Mol. Cell 2009, 34(4):451-460.
42. Chen X., et al. A kinase-independent function of c-Abl in promoting proteolytic destruction of damaged DNA binding proteins. Mol. Cell 2006, 22(4):489-499.
43. Alekseev S., et al. Cellular concentrations of DDB2 regulate dynamic binding of DDB1 at UV-induced DNA damage. Mol. Cell Biol. 2008, 28(24):7402-7413.
44. Zhang L., et al. The deubiquitinating protein USP24 interacts with DDB2 and regulates DDB2 stability. Cell Cycle 2012, 11(23):4378-4384.
45. Pines A., et al. PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J. Cell Biol. 2012, 199(2):235-249.
46. Ng J.M., et al. A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev. 2003, 17(13):1630-1645.
47. Xie Z., et al. Roles of Rad23 protein in yeast nucleotide excision repair. Nucleic Acids Res. 2004, 32(20):5981-5990.
48. Bergink S., et al. Recognition of DNA damage by XPC coincides with disruption of the XPC-RAD23 complex. J. Cell Biol. 2012, 196(6):681-688.
49. Poulsen S.L., et al. RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J. Cell Biol. 2013, 201(6):797-807.
50. Lubin A., et al. A human XPC protein interactome-a resource. Int. J. Mol. Sci. 2014, 15(1):141-158.
51. Wang Q.E., et al. DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation. Nucleic Acids Res. 2005, 33(13):4023-4034.
52. 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. 2006, 20(11):1429-1434.
53. Wei L., et al. BRCA1 contributes to transcription-coupled repair of DNA damage through polyubiquitination and degradation of Cockayne syndrome B protein. Cancer Sci. 2011, 102(10):1840-1847.
54. Anindya R., et al. A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair. Mol. Cell 2010, 38(5):637-648.
55. 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. 2012, 44(5):586-592.
56. Nicholson B., Kumar K.G. Suresh The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem. Biophys. 2011, 60(1-2):61-68.
57. Wilson M.D., Harreman M., Svejstrup J.Q. Ubiquitylation and degradation of elongating RNA polymerase II: the last resort. Biochim. Biophys. Acta 2013, 1829(1):151-157.
58. 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 1996, 93(21):11586-11590.
59. Chiba N., Parvin J.D. The BRCA1 and BARD1 association with the RNA polymerase II holoenzyme. Cancer Res. 2002, 62(15):4222-4228.
60. 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 2007, 28(3):386-397.
61. Starita L.M., et al. BRCA1/BARD1 ubiquitinate phosphorylated RNA polymerase II. J. Biol. Chem. 2005, 280(26):24498-24505.
62. Wu W., et al. BRCA1 ubiquitinates RPB8 in response to DNA damage. Cancer Res. 2007, 67(3):951-958.
63. Harreman M., et al. Distinct ubiquitin ligases act sequentially for RNA polymerase II polyubiquitylation. Proc. Natl. Acad. Sci. USA 2009, 106(49):20705-20710.
64. Verma R., et al. Cdc48/p97 mediates UV-dependent turnover of RNA Pol II. Mol. Cell 2011, 41(1):82-92.
65. Vertegaal A.C. Uncovering ubiquitin and ubiquitin-like signaling networks. Chem. Rev. 2011, 111(12):7923-7940.