UV-induced ubiquitylation of XPC complex, the UV-DDB-ubiquitin ligase complex, and DNA repair

Journal of Molecular Histology

Volumn 37, Issue 5-7, 2006, Pages 189-202

  Sugasawa, Kaoru ^a,b  

^a Japan Science and Technology Agency   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

DNA damage recognition; Nucleotide excision repair; Ubiquitin ligase; UV DDB; Xeroderma pigmentosum; XPC complex

Indexed keywords

CULLIN; DNA; DNA BINDING PROTEIN; GENE PRODUCT; PROTEIN; PROTEIN XPC; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

CANCER SUSCEPTIBILITY; CARCINOGENESIS; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; FUNCTIONAL GENOMICS; GENETIC DISORDER; GENOME; HUMAN; MOLECULAR MECHANICS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SKIN CANCER; UBIQUITINATION; ULTRAVIOLET RADIATION; XERODERMA PIGMENTOSUM;

DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; GENOME; HUMANS; MODELS, GENETIC; MOLECULAR STRUCTURE; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITIN-PROTEIN LIGASES; ULTRAVIOLET RAYS;

XERODERMA PIGMENTOSUM;

EID: 33751345828     PISSN: 15672379     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10735-006-9044-7     Document Type: Review

References (128)

1. Aboussekhra A, Biggerstaff M, Shivji MKK, Vilpo JA, Moncollin V, Podust VN, Protic M, Hübscher U, Egly J-M, Wood RD (1995) Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80:859-868
2. Andrejeva J, Poole E, Young DF, Goodbourn S, Randall RE (2002) The p127 subunit (DDB1) of the UV-DNA damage repair binding protein is essential for the targeted degradation of STAT1 by the V protein of the paramyxovirus simian virus 5. J Virol 76:11,379-11,386
3. Araki M, Masutani C, Takemura M, Uchida A, Sugasawa K, Kondoh J, Ohkuma Y, Hanaoka F (2001) Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J Biol Chem 276:18,665-18,672
4. Araújo SJ, Nigg EA, Wood RD (2001) Strong functional interactions of TFIIH with XPC and XPG in human DNA nucleotide excision repair, without a preassembled repairosome. Mol Cell Biol 21:2281-2291
5. Araújo SJ, Tirode F, Coin F, Pospiech H, Syväoja JE, Stucki M, Hübscher U, Egly J-M, Wood RD (2000) 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
6. Arias EE, Walter JC (2006) PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat Cell Biol 8:84-90
7. Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge SJ (1996) SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86:263-274
8. Batty D, Rapic'-Otrin V, Levine AS, Wood RD (2000) Stable binding of human XPC complex to irradiated DNA confers strong discrimination fordamagedsites. J Mol Biol 300:275-290
9. Bertolaet BL, Clarke DJ, Wolff M, Watson MH, Henze M, Divita G, Reed SI (2001) UBA domains of DNA damage-inducible proteins interact with ubiquitin. Nat Struct Biol 8:417-422
10. Bootsma D, Kraemer KH, Cleaver JE, Hoeijmakers JHJ (2001) Nucleotide excision repair syndromes: xeroderma pigmentosum, Cockayne syndrome, and trichothiodystrophy. In: Scriver CR, Beaudet al, Sly WS, Valle D (eds) The metabolic and molecular basis of inherited disease, vol 1. McGraw-Hill Book Co., New York, NY, pp 677-703
11. Chavanne F, Broughton BC, Pietra D, Nardo T, Browitt A, Lehmann AR, Stefanini M (2000) Mutations in the XPC gene in families with xeroderma pigmentosum and consequences at the cell, protein, and transcript levels. Cancer Res 60:1974-1982
12. Chen L, Madura K (2002) Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol Cell Biol 22:4902-4913
13. Chen L, Shinde U, Ortolan TG, Madura K (2001) Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly. EMBO Rep 2:933-938
14. Chen X, Zhang J, Lee J, Lin PS, Ford JM, Zheng N, Zhou P (2006) A kinase-independent function of c-Abl in promoting proteolytic descruction of damaged DNA binding proteins. Mol Cell 22:489-499
15. Chu G, Chang E (1988) Xeroderma pigmentosum group E cells lack a nuclear factor that binds to damaged DNA. Science 242:564-567
16. Cong F, Tang J, Hwang BJ, Vuong BQ, Chu G, Goff SP (2002) Interaction between UV-damaged DNA binding activity proteins and the c-Abl tyrosine kinase. J Biol Chem 277:34,870-34,878
17. Cope GA, Suh GS, Aravind L, Schwarz SE, Zipursky SL, Koonin EV, Deshaies RJ (2002) Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298:608-611
18. Datta A, Bagchi S, Nag A, Shiyanov P, Adami GR, Yoon T, Raychaudhuri P (2001) The p48 subunit of the damaged-DNA binding protein DDB associates with the CBP/p300 family of histone acetyltransferase. Mutat Res 486:89-97
19. Dualan R, Brody T, Keeney S, Nichols AF, Admon A, Linn S (1995) Chromosomal localization and cDNA cloning of the genes (DDB1 and DDB2) for the p127 and p48 subunits of a human damage-specific DNA binding protein. Genomics 29:62-69
20. El-Mahdy MA, Zhu Q, Wang Q, Wani G, Prætorius-Ibba M, Wani AA (2006) Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC. J Biol Chem 281:13,404-13,411
21. Evans E, Fellows J, Coffer A, Wood RD (1997a) Open complex formation around a lesion during nucleotide excision repair provides a structure for cleavage by human XPG protein. EMBO J 16:625-638
22. Evans E, Moggs JG, Hwang JR, Egly J-M, Wood RD (1997b) Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. EMBO J 16:6559-6573
23. Feldman RM, Correll CC, Kaplan KB, Deshaies RJ (1997) A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91:221-230
24. Fitch ME, Cross IV, Turner SJ, Adimoolam S, Lin CX, Williams KG, Ford JM (2003a) The DDB2 nucleotide excision repair gene product p48 enhances global genomic repair in p53 deficient human fibroblasts. DNA Repair (Amst) 2:819-826
25. Fitch ME, Nakajima S, Yasui A, Ford JM (2003b) In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product. J Biol Chem 278:46,906-46,910
26. Friedberg EC (2001) How nucleotide excision repair protects against cancer. Nat Rev Cancer 1:22-33
27. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2006) DNA repair and mutagenesis, 2nd edn. ASM Press, Washington, DC
28. Fujiwara Y, Masutani C, Mizukoshi T, Kondo J, Hanaoka F, Iwai S (1999) Characterization of DNA recognition by the human UV-damaged DNA-binding protein. J Biol Chem 274:20,027-20,033
29. Giglia-Mari G, Coin F, Ranish JA, Hoogstraten D, Theil A, Wijgers N, Jaspers NGJ, Raams A, Argentini M, van der Spek PJ, Botta E, Stefanini M, Egly J-M, Aebersold R, Hoeijmakers JHJ, Vermeulen W (2004) A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat Genet 36:714-719
30. Gillette TG, Huang W, Russell SJ, Reed SH, Johnston SA, Friedberg EC (2001) The 19S complex of the proteasome regulates nucleotide excision repair in yeast. Genes Dev 15:1528-1539
31. Gillette TG, Yu S, Zhou Z, Waters R, Johnston SA, Reed SH (2006) Distinct functions of the ubiquitin-proteasome pathway influence nucleotide excision repair. EMBO J published on line (doi: 10.1038/sj.emboj.7601120)
32. Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M, Drapkin R, Kisselev AF, Tanaka K, Nakatani Y (2003) 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
33. Guzder SN, Habraken Y, Sung P, Prakash L, Prakash S (1995) Reconstitution of yeast nucleotide excision repair with purified Rad proteins, replication protein A, and transcription factor TFIIH. J Biol Chem 270:12,973-12,976
34. Hayes S, Shiyanov P, Chen X, Raychaudhuri P (1998) DDB, a putative DNA repair protein, can function as a transcriptional partner of E2F1. Mol Cell Biol 18:240-249
35. Higa LAA, Mihaylov IS, Banks DP, Zheng J, Zhang H (2003) Radiation-mediated proteolysis of CDT1 by CUL4-ROC1 and CSN complexes constitutes a new checkpoint. Nat Cell Biol 5:1008-1015
36. Hiyama H, Yokoi M, Masutani C, Sugasawa K, Maekawa T, Tanaka K, Hoeijmakers JHJ, Hanaoka F (1999) Interaction of hHR23 with S5a. The ubiquitin-like domain of hHR23 mediates interaction with S5a subunit of 26 S proteasome. J Biol Chem 274:28,019-28,025
37. Hoeijmakers JHJ (2001) Genome maintenance mechanisms for preventing cancer. Nature 411:366-374
38. Hu J, McCall CM, Ohta T, Xiong Y (2004) Targeted ubiquitination of CDT1 by the DDB1-CUL4A-ROC1 ligase in response to DNA damage. Nat Cell Biol 6:1003-1009
39. Hwang BJ, Ford JM, Hanawalt PC, Chu G (1999) Expression of the p48 xeroderma pigmentosum gene is p53 dependent and is involved in global genome repair. Proc Natl Acad Sci USA 96:424-428
40. Hwang BJ, Liao JC, Chu G (1996) Isolation of a cDNA encoding a UV-damaged DNA binding factor defective in xeroderma pigmentosum group E cells. Mutat Res 362:105-117
41. Hwang BJ, Toering S, Francke U, Chu G (1998) 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
42. Itoh T, Cado D, Kamide R, Linn S (2004) DDB2 gene disruption leads to skin tumors and resistance to apoptosis after exposure to ultraviolet light but not a chemical carcinogen. Proc Natl Acad Sci USA 101:2052-2057
43. Itoh T, Linn S, Ono T, Yamaizumi M (2000) Reinvestigation of the classification of five cell strains of xeroderma pigmentosum group E with reclassification of three of them. J Invest Dermatol 114:1022-1029
44. Itoh T, O'Shea C, Linn S (2003) Impaired regulation of tumor suppressor p53 caused by mutations in the xeroderma pigmentosum DDB2 gene: mutual regulatory interactions between p48DDB2 and p53. Mol Cell Biol 23:7540-7553
45. Janicijevic A, Sugasawa K, Shimizu Y, Hanaoka F, Wijgers N, Djurica M, Hoeijmakers JHJ, Wyman C (2003) DNA bending by the human damage recognition complex XPC-HR23B. DNA Repair (Amst) 2:325-336
46. Jia S, Kobayashi R, Grewal SIS (2005) Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat Cell Biol 7:1007-1013
47. Kamiuchi S, Saijo M, Citterio E, de Jager M, Hoeijmakers JHJ, Tanaka K (2002) Translocation of Cockayne syndrome group A protein to the nuclear matrix: possible relevance to transcription-coupled DNA repair. Proc Natl Acad Sci USA 99:201-206
48. Kamura T, Koepp DM, Conrad MN, Skowyra D, Moreland RJ, Iliopoulos O, Lane WS, Kaelin WG Jr, Elledge SJ, Conaway RC, Harper JW, Conaway JW (1999) Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 284:657-661
49. Keeney S, Chang GJ, Linn S (1993) Characterization of a human DNA damage binding protein implicated in xeroderma pigmentosum E. J Biol Chem 268:21,293-21,300
50. Keeney S, Wein H, Linn S (1992) Biochemical heterogeneity in xeroderma pigmentosum complementation group E. Mutat Res 273:49-56
51. Khan SG, Levy HL, Legerski R, Quackenbush E, Reardon JT, Emmert S, Sancar A, Li L, Schneider TD, Cleaver JE, Kraemer KH (1998) Xeroderma pigmentosum group C splice mutation associated with autism and hypoglycinemia. J Invest Dermatol 111:791-796
52. Kim J-K, Patel D, Choi B-S (1995) Contrasting structural impacts induced by cis-syn cyclobutane dimer and (6-4) adduct in DNA duplex decamers: implication in mutagenesis and repair activity. Photochem Photobiol 62:44-50
53. Kusumoto R, Masutani C, Sugasawa K, Iwai S, Araki M, Uchida A, Mizukoshi T, Hanaoka F (2001) Diversity of the damage recognition step in the global genomic nucleotide excision repair in vitro. Mutat Res 485:219-227
54. Lambertson D, Chen L, Madura K (1999) Pleiotropic defects caused by loss of the proteasome-interacting factors Rad23 and Rpn10 of Saccharomyces cerevisiae. Genetics 153:69-79
55. Legerski R, Peterson C (1992) Expression cloning of a human DNA repair gene involved in xeroderma pigmentosum group C. Nature 359:70-73
56. Li L, Bales ES, Peterson CA, Legerski RJ (1993) Characterization of molecular defects in xeroderma pigmentosum group C. Nat Genet 5:413-417
57. Li T, Chen X, Garbutt KC, Zhou P, Zheng N (2006) Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124:105-117
58. Lin GY, Paterson RG, Richardson CD, Lamb RA (1998) The V protein of the paramyxovirus SV5 interacts with damage-specific DNA binding protein. Virology 249:189-200
59. CAND1, an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol Cell 10:1511-1518
60. Lyapina S, Cope G, Shevchenko A, Serino G, Tsuge T, Zhou C, Wolf DA, Wei N, Shevchenko A, Deshaies RJ (2001) Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292:1382-1385
61. Masutani C, Sugasawa K, Yanagisawa J, Sonoyama T, Ui M, Enomoto T, Takio K, Tanaka K, van der Spek PJ, Bootsma D, Hoeijmakers JHJ, Hanaoka F (1994) Purification and cloning of a nucleotide excision repair complex involving the xeroderma pigmentosum group C protein and a human homolog of yeast RAD23. EMBO J 13:1831-1843
62. Matsuda N, Azuma K, Saijo M, Iemura S, Hioki Y, Natsume T, Chiba T, Tanaka K, Tanaka K (2005) DDB2, the xeroderma pigmentosum group E gene product, is directly ubiquitylated by Cullin 4A-based ubiquitin ligase complex. DNA Repair (Amst) 4:537-545
63. Matsunaga T, Mu D, Park CH, Reardon JT, Sancar A (1995) Human DNA repair excision nuclease. Analysis of the roles of the subunits involved in dual incisions by using anti-XPG and anti-ERCC1 antibodies. J Biol Chem 270:20,862-20,869
64. McAteer K, Jing Y, Kao J, Taylor J-S, Kennedy MA (1998) Solution-state structure of a DNA dodecamer duplex containing a cis-syn thymine cyclobutane dimer, the major UV photoproduct of DNA. J Mol Biol 282:1013-1032
65. McCready S (1994) Repair of 6-4 photoproducts and cyclobutane pyrimidine dimers in rad mutants of Saccharomyces cerevisiae. Mutat Res 315:261-273
66. Mitchell DL, Nairn RS (1989) The biology of the (6-4) photoproduct. Photochem Photobiol 49:805-819
67. Moser J, Volker M, Kool H, Alekseev S, Vrieling H, Yasui A, van Zeeland AA, Mullenders LHF (2005) 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
68. Mu D, Park CH, Matsunaga T, Hsu DS, Reardon JT, Sancar A (1995) Reconstitution of human DNA repair excision nuclease in a highly defined system. J Biol Chem 270:2415-2418
69. Mu D, Wakasugi M, Hsu DS, Sancar A (1997) Characterization of reaction intermediates of human excision repair nuclease. J Biol Chem 272:28,971-28,979
70. Neuwald AF, Poleksic A (2000) PSI-BLAST searches using hidden markov models of structural repeats: prediction of an unusual sliding DNA clamp and of beta-propellers in UV-damaged DNA-binding protein. Nucleic Acids Res 28:3570-3580
71. Ng JMY, Vermeulen W, van der Horst GTJ, Bergink S, Sugasawa K, Vrieling H, Hoeijmakers JHJ (2003) A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev 17:1630-1645
72. Ng JMY, Vrieling H, Sugasawa K, Ooms MP, Grootegoed JA, Vreeburg JT, Visser P, Beems RB, Gorgels TG, Hanaoka F, Hoeijmakers JHJ, van der Horst GTJ (2002) Developmental defects and male sterility in mice lacking the ubiquitin-like DNA repair gene mHR23B. Mol Cell Biol 22:1233-1245
73. Nichols AF, Itoh T, Graham JA, Liu W, Yamaizumi M, Linn S (2000) Human damage-specific DNA-binding protein p48. Characterization of XPE mutations and regulation following UV irradiation. J Biol Chem 275:21,422-21,428
74. - phenotype. J Biol Chem 271:24,317-24,320
75. Nishi R, Okuda Y, Watanabe E, Mori T, Iwai S, Masutani C, Sugasawa K, Hanaoka F (2005) Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol Cell Biol 25:5664-5674
76. O'Donovan A, Davies AA, Moggs JG, West SC, Wood RD (1994) XPG endonuclease makes the 3′ incision in human DNA nucleotide excision repair. Nature 371:432-435
77. Obuse C, Yang H, Nozaki N, Goto S, Okazaki T, Yoda K (2004) Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNA binding protein 1 (DDB-1) is a component of the CEN-complex, while BMI-1 is transiently co-localized with the centromeric region in interphase. Genes Cells 9:105-120
78. Ohta T, Michel JJ, Schottelius AJ, Xiong Y (1999) ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol Cell 3:535-541
79. Okuda Y, Nishi R, Ng JMY, Vermeulen W, van der Horst GTJ, Mori T, Hoeijmakers JHJ, Hanaoka F, Sugasawa K (2004) Relative levels of the two mammalian Rad23 homologs determine composition and stability of the xeroderma pigmentosum group C protein complex. DNA Repair (Amst) 3:1285-1295
80. Otrin VR, McLenigan M, Takao M, Levine AS, Protic M (1997) Translocation of a UV-damaged DNA binding protein into a tight association with chromatin after treatment of mammalian cells with UV light. J Cell Sci 110:1159-1168
81. Payne A, Chu G (1994) Xeroderma pigmentosum group E binding factor recognizes a broad spectrum of DNA damage. Mutat Res 310:89-102
82. Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6:9-20
83. Raasi S, Pickart CM (2003) Rad23 ubiquitin-associated domains (UBA) inhibit 26 S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J Biol Chem 278:8951-8959
84. Rapic'-Otrin V, McLenigan MP, Bisi DC, Gonzalez M, Levine AS (2002) 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
85. Rapic'-Otrin V, Navazza V, Nardo T, Botta E, McLenigan M, Bisi DC, Levine AS, Stefanini M (2003) True XP group E patients have a defective UV-damaged DNA binding protein complex and mutations in DDB2 which reveal the functional domains of its p48 product. Hum Mol Genet 12:1507-1522
86. Reardon JT, Nichols AF, Keeney S, Smith CA, Taylor JS, Linn S, Sancar A (1993) Comparative analysis of binding of human damaged DNA-binding protein (XPE) and Escherichia coli damage recognition protein (UvrA) to the major ultraviolet photoproducts: T[c,s]T, T[t,s]T, T[6-4]T, and T[Dewar]T. J Biol Chem 268:21,301-21,308
87. Riedl T, Hanaoka F, Egly J-M (2003) The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J 22:5293-5303
88. Russell SJ, Reed SH, Huang W, Friedberg EC, Johnston SA (1999) The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. Mol Cell 3:687-695
89. Salisbury JL, Suino KM, Busby R, Springett M (2002) Centrin-2 is required for centriole duplication in mammalian cells. Curr Biol 12:1287-1292
90. Schauber C, Chen L, Tongaonkar P, Vega I, Lambertson D, Potts W, Madura K (1998) Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature 391:715-718
91. Seol JH, Feldman RM, Zachariae W, Shevchenko A, Correll CC, Lyapina S, Chi Y, Galova M, Claypool J, Sandmeyer S, Nasmyth K, Deshaies RJ, Shevchenko A, Deshaies RJ (1999) Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev 13:1614-1626
92. Shivji MKK, Eker APM, Wood RD (1994) DNA repair defect in xeroderma pigmentosum group C and complementing factor from HeLa cells. J Biol Chem 269:22,749-22,757
93. Shivji MKK, Podust VN, Hübscher U, Wood RD (1995) Nucleotide excision repair DNA synthesis by DNA polymerase e in the presence of PCNA, RFC, and RPA. Biochemistry 34:5011-5017
94. Shiyanov P, Hayes SA, Donepudi M, Nichols AF, Linn S, Slagle BL, Raychaudhuri P (1999a) The naturally occurring mutants of DDB are impaired in stimulating nuclear import of the p125 subunit and E2F1-activated transcription. Mol Cell Biol 19:4935-4943
95. Shiyanov P, Nag A, Raychaudhuri P (1999b) Cullin 4A associates with the UV-damaged DNA-binding protein DDB. J Biol Chem 274:35,309-35,312
96. Sijbers AM, de Laat WL, Ariza RR, Biggerstaff M, Wei Y-F, Moggs JG, Carter KC, Shell BK, Evans E, de Jong MC, Rademakers S, de Rooij J, Jaspers NGJ, Hoeijmakers JHJ, Wood RD (1996) Xeroderma pigmentosum group F caused by a defect of in structure-specific DNA repair endonuclease. Cell 86:811-822
97. Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209-219
98. Snyderwine EG, Bohr VA (1992) Gene- and strand-specific damage and repair in Chinese hamster ovary cells treated with 4-nitroquinoline 1-oxide. Cancer Res 52:4183-4189
99. Sugasawa K, Ng JM, Masutani C, Maekawa T, Uchida A, van der Spek PJ, Eker AP, Rademakers S, Visser C, Aboussekhra A, Wood RD, Hanaoka F, Bootsma D, Hoeijmakers JH (1997) Two human homologs of Rad23 are functionally interchangeable in complex formation and stimulation of XPC repair activity. Mol Cell Biol 17:6924-6931
100. Sugasawa K, Ng JMY, Masutani C, Iwai S, van der Spek PJ, Eker APM, Hanaoka F, Bootsma D, Hoeijmakers JHJ (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2:223-232
101. Sugasawa K, Okamoto T, Shimizu Y, Masutani C, Iwai S, Hanaoka F (2001) A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev 15:507-521
102. Sugasawa K, Okuda Y, Saijo M, Nishi R, Matsuda N, Chu G, Mori T, Iwai S, Tanaka K, Tanaka K, Hanaoka F (2005) UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121:387-400
103. Sugasawa K, Shimizu Y, Iwai S, Hanaoka F (2002) A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair 1:95-107
104. Takao M, Abramic M, Moos M Jr, Otrin VR, Wootton JC, McLenigan M, Levine AS, Protic M (1993) A 127 kDa component of a UV-damaged DNA-binding complex, which is defective in some xeroderma pigmentosum group E patients, is homologous to a slime mold protein. Nucleic Acids Res 21:4111-4118
105. Tan P, Fuchs SY, Chen A, Wu K, Gomez C, Ronai Z, Pan ZQ (1999) Recruitment of a ROC1-CUL1 ubiquitin ligase by Skp1 and HOS to catalyze the ubiquitination of IκBα. Mol Cell 3:527-533
106. Tang J, Chu G (2002) Xeroderma pigmentosum complementation group E and UV-damaged DNA-binding protein. DNA Repair 1:601-616
107. Tang JY, Hwang BJ, Ford JM, Hanawalt PC, Chu G (2000) Xeroderma pigmentosum p48 gene enhances global genomic repair and suppresses UV-induced mutagenesis. Mol Cell 5:737-744
108. Tang MS, Bohr VA, Zhang XS, Pierce J, Hanawalt PC (1989) Quantification of aminofluorene adduct formation and repair in defined DNA sequences in mammalian cells using the UVRABC nuclease. J Biol Chem 264:14,455-14,462
109. Tornaletti S, Hanawalt PC (1999) Effect of DNA lesions on transcription elongation. Biochimie 81:139-146
110. Treiber DK, Chen Z, Essigmann JM (1992) An ultraviolet light-damaged DNA recognition protein absent in xeroderma pigmentosum group E cells binds selectively to pyrimidine (6-4) pyrimidone photoproducts. Nucleic Acids Res 20:5805-5810
111. Ulane CM, Horvath CM (2002) Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 304:160-166
112. van der Spek PJ, Eker A, Rademakers S, Visser C, Sugasawa K, Masutani C, Hanaoka F, Bootsma D, Hoeijmakers JH (1996a) XPC and human homologs of RAD23: intracellular localization and relationship to other nucleotide excision repair complexes. Nucleic Acids Res 24:2551-2559
113. van der Spek PJ, Visser CE, Hanaoka F, Smit B, Hagemeijer A, Bootsma D, Hoeijmakers JH (1996b) Cloning, comparative mapping, and RNA expression of the mouse homologues of the Saccharomyces cerevisiae nucleotide excision repair gene RAD23. Genomics 31:20-27
114. van Hoffen A, Natarajan AT, Mayne LV, van Zeeland AA, Mullenders LHF, Venema J (1993) Deficient repair of the transcribed strand of active genes in Cockayne syndrome cells. Nucleic Acids Res 21:5890-5895
115. van Oosten M, Rebel H, Friedberg EC, van Steeg H, van der Horst GTJ, van Kranen HJ, Westerman A, van Zeeland AA, Mullenders LHF, de Gruijl FR (2000) Differential role of transcription-coupled repair in UVB-induced G2 arrest and apoptosis in mouse epidermis. Proc Natl Acad Sci USA 97:11,268-11,273
116. Venema J, Mullenders LHF, Natarajan AT, van Zeeland AA, Mayne LV (1990) The genetic defect in Cockayne's syndrome is associated with a defect in repair of UV-induced DNA damage in transcriptionally active DNA. Proc Natl Acad Sci USA 87:4704-4711
117. Venema J, van Hoffen A, Karcagi V, Natarajan AT, van Zeeland AA, Mullenders LHF (1991) Xeroderma pigmentosum complementation group C cells remove pyrimidine dimers selectively from the transcribed strand of active genes. Mol Cell Biol 11:4128-4134
118. Volker M, Moné MJ, Karmakar P, van Hoffen A, Schul W, Vermeulen W, Hoeijmakers JHJ, van Driel R, van Zeeland AA, Mullenders LHF (2001) Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 8:213-224
119. Wakasugi M, Kawashima A, Morioka H, Linn S, Sancar A, Mori T, Nikaido O, Matsunaga T (2002) DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J Biol Chem 277:1637-1640
120. Wakasugi M, Reardon J, Sancar A (1997) The non-catalytic function of XPG protein during dual incision in human nucleotide excision repair. J Biol Chem 272:16,030-16,034
121. Wakasugi M, Shimizu M, Morioka H, Linn S, Nikaido O, Matsunaga T (2001) Damaged DNA-binding protein DDB stimulates the excision of cyclobutane pyrimidine dimers in vitro in concert with XPA and replication protein A. J Biol Chem 276:15434-15440
122. Wang H, Zhai L, Xu J, Joo H-Y, Jackson S, Erdjument-Bromage H, Tempst P, Xiong Y, Zhang Y (2006) Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell 22:383-394
123. Wertz IE, O'Rourke KM, Zhang Z, Dornan D, Arnott D, Deshaies RJ, Dixit VM (2004) Human De-etiolated-1 regulates c-Jun by assembling a CUL4A ubiquitin ligase. Science 303:1371-1374
124. Wilkinson CR, Seeger M, Hartmann-Petersen R, Stone M, Wallace M, Semple C, Gordon C (2001) Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nat Cell Biol 3:939-943
125. Wittschieben BØ, Iwai S, Wood RD (2005) 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 280:39,982-39,989
126. Yokoi M, Masutani C, Maekawa T, Sugasawa K, Ohkuma Y, Hanaoka F (2000) The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA. J Biol Chem 275:9870-9875
127. Zheng J, Yang X, Harrell JM, Ryzhikov S, Shim EH, Lykke-Andersen K, Wei N, Sun H, Kobayashi R, Zhang H (2002) CAND1 binds to unneddylated CUL1 and regulates the formation of SCF ubiquitin E3 ligase complex. Mol Cell 10:1519-1526
128. Zhong W, Feng H, Santiago FE, Kipreos ET (2003) CUL-4 ubiquitin ligase maintains genome stability by restraining DNA-replication licensing. Nature 423:885-889