The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation

Cell

Volumn 147, Issue 5, 2011, Pages 1024-1039

  Fischer, Eric S ^a,g   Scrima, Andrea ^a,h   Böhm, Kerstin ^a   Matsumoto, Syota ^b   Lingaraju, Gondichatnahalli M ^a   Faty, Mahamadou ^a   Yasuda, Takeshi ^c   Cavadini, Simone ^a   Wakasugi, Mitsuo ^d   Hanaoka, Fumio ^e   Iwai, Shigenori ^f   Gut, Heinz ^a   Sugasawa, Kaoru ^b   Thomä, Nicolas H ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b KOBE UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^d KANAZAWA UNIVERSITY   (Japan)

^e GAKUSHUIN UNIVERSITY   (Japan)

^f OSAKA UNIVERSITY   (Japan)

^g UNIVERSITY OF BASEL   (Switzerland)

^h HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COP9 SIGNALOSOME; PYRIMIDINE DIMER; SINGLE STRANDED DNA; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE CRL4; UNCLASSIFIED DRUG; CUL4A PROTEIN, HUMAN; CULLIN; DDB1 PROTEIN, HUMAN; DDB2 PROTEIN, HUMAN; DNA BINDING PROTEIN; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

ARTICLE; CHROMATIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; ENZYME ACTIVATION; ENZYME BINDING; ENZYME INHIBITION; ENZYME STRUCTURE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN TARGETING; UBIQUITINATION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; CULLIN PROTEINS; DNA DAMAGE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HUMANS; MODELS, MOLECULAR; UBIQUITIN-PROTEIN LIGASES; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

EID: 81855227619     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.10.035     Document Type: Article

References (95)

1. A. Aboussekhra, M. Biggerstaff, M.K. Shivji, J.A. Vilpo, V. Moncollin, V.N. Podust, M. Protić, U. Hübscher, J.M. Egly, and R.D. Wood Mammalian DNA nucleotide excision repair reconstituted with purified protein components Cell 80 1995 859 868
2. S. Angers, T. Li, X. Yi, M.J. MacCoss, R.T. Moon, and N. Zheng Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery Nature 443 2006 590 593
3. D. Batty, V. Rapic Otrin, A. Levine, and R. Wood Stable binding of human XPC complex to irradiated DNA confers strong discrimination for damaged sites J. Mol. Biol. 300 2000 275 290
4. E.J. Bennett, J. Rush, S.P. Gygi, and J.W. Harper Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics Cell 143 2010 951 965
5. G. Bornstein, D. Ganoth, and A. Hershko Regulation of neddylation and deneddylation of cullin1 in SCFSkp2 ubiquitin ligase by F-box protein and substrate Proc. Natl. Acad. Sci. USA 103 2006 11515 11520
6. A. Brunger, P. Adams, G. Clore, W. DeLano, P. Gros, R. Grosse-Kunstleve, J. Jiang, J. Kuszewski, M. Nilges, and N. Pannu Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
7. T.E. Creighton Proteins: Structures and Molecular Properties second edition 1992 W. H. Freeman and Company
8. M.-R. Duan, and M.J. Smerdon UV damage in DNA promotes nucleosome unwrapping J. Biol. Chem. 285 2010 26295 26303
9. D. Duda, L. Borg, D. Scott, H. Hunt, M. Hammel, and B. Schulman Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation Cell 134 2008 995 1006
10. R.I. Enchev, A. Schreiber, F. Beuron, and E.P. Morris Structural insights into the COP9 signalosome and its common architecture with the 26S proteasome lid and eIF3 Structure 18 2010 518 527
11. M. Fousteri, and L.H.F. Mullenders Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects Cell Res. 18 2008 73 84
12. M. Fousteri, W. Vermeulen, A.A. van Zeeland, and L.H. Mullenders 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 2006 471 482
13. E.C. Friedberg How nucleotide excision repair protects against cancer Nat. Rev. Cancer 1 2001 22 33
14. Y. Fukumoto, N. Dohmae, and F. Hanaoka Schizosaccharomyces pombe Ddb1 recruits substrate-specific adaptor proteins through a novel protein motif, the DDB-box Mol. Cell. Biol. 28 2008 6746 6756
15. M. Furukawa, Y. Zhang, J. McCarville, T. Ohta, and Y. Xiong The CUL1 C-terminal sequence and ROC1 are required for efficient nuclear accumulation, NEDD8 modification, and ubiquitin ligase activity of CUL1 Mol. Cell. Biol. 20 2000 8185 8197
16. J.M. Gale, and M.J. Smerdon Photofootprint of nucleosome core DNA in intact chromatin having different structural states J. Mol. Biol. 204 1988 949 958
17. R. Groisman, I. Kuraoka, O. Chevallier, N. Gaye, T. Magnaldo, K. Tanaka, A.F. Kisselev, A. Harel-Bellan, and Y. Nakatani CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome Genes Dev. 20 2006 1429 1434
18. R. Groisman, J. Polanowska, I. Kuraoka, J. Sawada, M. Saijo, R. Drapkin, A. Kisselev, K. Tanaka, and Y. Nakatani The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage Cell 113 2003 357 367
19. J. Guerrero-Santoro, M. Kapetanaki, C. Hsieh, I. Gorbachinsky, A. Levine, and V. Rapic-Otrin The cullin 4B-based UV-damaged DNA-binding protein ligase binds to UV-damaged chromatin and ubiquitinates histone H2A Cancer Res. 68 2008 5014 5022
20. R. Hannss, and W. Dubiel COP9 signalosome function in the DDR FEBS Lett. 585 2011 2845 2852
21. Y. He, C. McCall, J. Hu, Y. Zeng, and Y. Xiong DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases Genes Dev. 20 2006 2949 2954
22. L. Higa, M. Wu, T. Ye, R. Kobayashi, H. Sun, and H. Zhang CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation Nat. Cell Biol. 8 2006 1277 1283
23. J.H.J. Hoeijmakers DNA damage, aging, and cancer N. Engl. J. Med. 361 2009 1475 1485
24. B.J. Hwang, S. Toering, U. Francke, and G. Chu 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 1998 4391 4399
25. S. Jackson, and Y. Xiong CRL4s: the CUL4-RING E3 ubiquitin ligases Trends Biochem. Sci. 34 2009 562 570
26. J. Jin, E. Arias, J. Chen, J. Harper, and J. Walter A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1 Mol. Cell 23 2006 709 721
27. Y. Jing, J.F. Kao, and J.S. Taylor Thermodynamic and base-pairing studies of matched and mismatched DNA dodecamer duplexes containing cis-syn, (6-4) and Dewar photoproducts of TT Nucleic Acids Res. 26 1998 3845 3853
28. M.G. Kapetanaki, J. Guerrero-Santoro, D.C. Bisi, C.L. Hsieh, V. Rapić-Otrin, and A.S. Levine 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 103 2006 2588 2593
29. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
30. J. Lee, and P. Zhou DCAFs, the missing link of the CUL4-DDB1 ubiquitin ligase Mol. Cell 26 2007 775 780
31. T. Li, X. Chen, K.C. Garbutt, P. Zhou, and N. Zheng Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase Cell 124 2006 105 117
32. T. Li, E.I. Robert, P.C. van Breugel, M. Strubin, and N. Zheng A promiscuous α-helical motif anchors viral hijackers and substrate receptors to the CUL4-DDB1 ubiquitin ligase machinery Nat. Struct. Mol. Biol. 17 2010 105 111
33. M.S. Luijsterburg, J. Goedhart, J. Moser, H. Kool, B. Geverts, A.B. Houtsmuller, L.H.F. Mullenders, W. Vermeulen, and R. van Driel Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC J. Cell Sci. 120 2007 2706 2716
34. D.L. Mitchell, G.M. Adair, and R.S. Nairn Inhibition of transient gene expression in Chinese hamster ovary cells by triplet-sensitized UV-B irradiation of transfected DNA Photochem. Photobiol. 50 1989 639 646
35. J. Moser, M. Volker, H. Kool, S. Alekseev, H. Vrieling, A. Yasui, A. van Zeeland, and L. Mullenders The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions DNA Repair (Amst.) 4 2005 571 582
36. R. Nishi, S. Alekseev, C. Dinant, D. Hoogstraten, A.B. Houtsmuller, J.H. Hoeijmakers, W. Vermeulen, F. Hanaoka, and K. Sugasawa UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells DNA Repair (Amst.) 8 2009 767 776
37. A. Payne, and G. Chu Xeroderma pigmentosum group E binding factor recognizes a broad spectrum of DNA damage Mutat. Res. 310 1994 89 102
38. V. Rapić-Otrin, M.P. McLenigan, D.C. Bisi, M. Gonzalez, and A.S. Levine Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation Nucleic Acids Res. 30 2002 2588 2598
39. M.W. Schmidt, P.R. McQuary, S. Wee, K. Hofmann, and D.A. Wolf F-box-directed CRL complex assembly and regulation by the CSN and CAND1 Mol. Cell 35 2009 586 597
40. A. Scrima, E.S. Fischer, G.M. Lingaraju, K. Böhm, S. Cavadini, and N.H. Thomä Detecting UV-lesions in the genome: The modular CRL4 ubiquitin ligase does it best! FEBS Lett. 585 2011 2818 2825
41. A. Scrima, R. Konícková, B.K. Czyzewski, Y. Kawasaki, P.D. Jeffrey, R. Groisman, Y. Nakatani, S. Iwai, N.P. Pavletich, and N.H. Thomä Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex Cell 135 2008 1213 1223
42. K. Sugasawa UV-induced ubiquitylation of XPC complex, the UV-DDB-ubiquitin ligase complex, and DNA repair J. Mol. Histol. 37 2006 189 202
43. K. Sugasawa Regulation of damage recognition in mammalian global genomic nucleotide excision repair Mutat. Res. 685 2010 29 37
44. K. Sugasawa, T. Okamoto, Y. Shimizu, C. Masutani, S. Iwai, and F. Hanaoka A multistep damage recognition mechanism for global genomic nucleotide excision repair Genes Dev. 15 2001 507 521
45. K. Sugasawa, Y. Okuda, M. Saijo, R. Nishi, N. Matsuda, G. Chu, T. Mori, S. Iwai, K. Tanaka, and K. Tanaka UV-Induced Ubiquitylation of XPC Protein Mediated by UV-DDB-Ubiquitin Ligase Complex Cell 121 2005 387 400
46. A. Takedachi, M. Saijo, and K. Tanaka DDB2 complex-mediated ubiquitylation around DNA damage is oppositely regulated by XPC and Ku and contributes to the recruitment of XPA Mol. Cell. Biol. 30 2010 2708 2723
47. J. Tang, and G. Chu Xeroderma pigmentosum complementation group E and UV-damaged DNA-binding protein DNA Repair (Amst.) 1 2002 601 616
48. J.Y. Tang, B.J. Hwang, J.M. Ford, P.C. Hanawalt, and G. Chu Xeroderma pigmentosum p48 gene enhances global genomic repair and suppresses UV-induced mutagenesis Mol. Cell 5 2000 737 744
49. S. Tornaletti DNA repair in mammalian cells: Transcription-coupled DNA repair: directing your effort where it's most needed Cell. Mol. Life Sci. 66 2009 1010 1020
50. C. Troelstra, A. van Gool, J. de Wit, W. Vermeulen, D. Bootsma, and J.H. Hoeijmakers ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne's syndrome and preferential repair of active genes Cell 71 1992 939 953
51. M. Volker, M. Mone, P. Karmakar, A. van Hoffen, W. Schul, W. Vermeulen, J. Hoeijmakers, R. van Driel, A. van Zeeland, and L. Mullenders Sequential assembly of the nucleotide excision repair factors in vivo Mol. Cell 8 2001 213 224
52. H. Wang, L. Zhai, J. Xu, H. Joo, S. Jackson, H. Erdjument-Bromage, P. Tempst, Y. Xiong, and Y. Zhang Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage Mol. Cell 22 2006 383 394
53. B. Wittschieben, S. Iwai, and R. Wood 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 2005 39982 39989
54. T. Yasuda, K. Sugasawa, Y. Shimizu, S. Iwai, T. Shiomi, and F. Hanaoka Nucleosomal structure of undamaged DNA regions suppresses the nonspecific DNA binding of the XPC complex DNA Repair (Amst.) 4 2005 389 395
55. C. Zhou, S. Wee, E. Rhee, M. Naumann, W. Dubiel, and D.A. Wolf Fission yeast COP9/signalosome suppresses cullin activity through recruitment of the deubiquitylating enzyme Ubp12p Mol. Cell 11 2003 927 938
56. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221.
57. Angers, S., Li, T., Yi, X., MacCoss, M.J., Moon, R.T., and Zheng, N. (2006). Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443, 590-593.
58. Bricogne, G., Blanc, E., and Brandl, M. C., F., Keller, P., Paciorek, P., Roversi, P., Sharff, A., Smart, O., Vonrhein, C., et al. (2010). BUSTER version 2.9. Cambridge, United Kingdom: Global Phasing Ltd.
59. Brunger, A., Adams, P., Clore, G., DeLano, W., Gros, P., Grosse-Kunstleve, R., Jiang, J., Kuszewski, J., Nilges, M., Pannu, N., et al. (1998). Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921.
60. Collaborative Computational Project, N. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763.
61. Cronin, C.N., Lim, K.B., and Rogers, J. (2007). Production of selenomethionyl-derivatized proteins in baculovirus-infected insect cells. Protein Sci. 16, 2023-2029.
62. Duda, D., Borg, L., Scott, D., Hunt, H., Hammel, M., and Schulman, B. (2008). Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134, 995-1006.
63. Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
64. Enchev, R.I., Schreiber, A., Beuron, F., and Morris, E.P. (2010). Structural insights into the COP9 signalosome and its common architecture with the 26S proteasome lid and eIF3. Structure 18, 518-527.
65. Eswar, N., Webb, B., Marti-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M.Y., Pieper, U., and Sali, A. (2006). Comparative protein structure modeling using Modeler. Curr Protoc Bioinformatics Chapter 5, Unit 5 6.
66. Goldenberg, S.J., Cascio, T.C., Shumway, S.D., Garbutt, K.C., Liu, J., Xiong, Y., and Zheng, N. (2004). Structure of the Cand1-Cul1-Roc1 complex reveals regulatory mechanisms for the assembly of the multisubunit cullin-dependent ubiquitin ligases. Cell 119, 517-528.
67. Isidor, B., Pichon, O., Baron, S., David, A., and Le Caignec, C. (2010). Deletion of the CUL4B gene in a boy with mental retardation, minor facial anomalies, short stature, hypogonadism, and ataxia. Am. J. Med. Genet. A. 152A, 175-180.
68. Iwai, S., Shimizu, M., Kamiya, H., and Ohtsuka, E. (1996). Synthesis of a phosphoramidite coupling unit of the pyrimidine (6-4) pyrimidone photoproduct and its incorporation into oligodeoxynucleotides. J. Am. Chem. Soc. 118, 7642-7643.
69. Jin, J., Arias, E., Chen, J., Harper, J., and Walter, J. (2006). A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23, 709-721.
70. Kabsch, W. (1993). Automatic Processing of Rotation Diffraction Data from Crystals of Initially Unknown Symmetry and Cell Constants. J. Appl. Cryst. 26, 795-800.
71. Kelley, L.A., and Sternberg, M.J. (2009). Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371.
72. Kerzendorfer, C., Hart, L., Colnaghi, R., Carpenter, G., Alcantara, D., Outwin, E., Carr, A.M., and O'Driscoll, M. (2011). CUL4B-deficiency in humans: Understanding the clinical consequences of impaired Cullin 4-RING E3 ubiquitin ligase function. Mechanisms of aging and development 132, 366-373.
73. Kerzendorfer, C., Whibley, A., Carpenter, G., Outwin, E., Chiang, S.-C., Turner, G., Schwartz, C., El-Khamisy, S., Raymond, F.L., and O'Driscoll, M. (2010). Mutations in Cullin 4B result in a human syndrome associated with increased camptothecin-induced topoisomerase I-dependent DNA breaks. Hum. Mol. Genet. 19, 1324-1334.
74. Klock, H.E., and Lesley, S.A. (2009). The Polymerase Incomplete Primer Extension (PIPE) method applied to high-throughput cloning and site-directed mutagenesis. Methods Mol. Biol. 498, 91-103.
75. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
76. Laugel, V., Dalloz, C., Durand, M., Sauvanaud, F., Kristensen, U., Vincent, M.C., Pasquier, L., Odent, S., Cormier-Daire, V., Gener, B., et al. (2010). Mutation update for the CSB/ERCC6 and CSA/ERCC8 genes involved in Cockayne syndrome. Hum. Mutat. 31, 113-126.
77. Li, T., Chen, X., Garbutt, K.C., Zhou, P., and 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.
78. Losa, R., Omari, S., and Thoma, F. (1990). Poly(dA).poly(dT) rich sequences are not sufficient to exclude nucleosome formation in a constitutive yeast promoter. Nucleic Acids Res. 18, 3495-3502.
79. Lu, X., and Olson, W. (2008). 3DNA: a versatile, integrated software system for the analysis, rebuilding and visualization of three-dimensional nucleic-acid structures. Nat. Protoc. 3, 1213-1227.
80. Luger, K., Rechsteiner, T.J., Flaus, A.J., Waye, M.M., and Richmond, T.J. (1997). Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 272, 301-311.
81. McCoy, A., Grosse-Kunstleve, R., Adams, P., Winn, M., Storoni, L., and Read, R. (2007). Phaser crystallographic software. J. Appl. Cryst. 40, 658-674.
82. Mees, A., Klar, T., Gnau, P., Hennecke, U., Eker, A.P.M., Carell, T., and Essen, L.-O. (2004). Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science (New York, NY) 306, 1789-1793.
83. Melandri, F., Grenier, L., Plamondon, L., Huskey, W.P., and Stein, R.L. (1996). Kinetic studies on the inhibition of isopeptidase T by ubiquitin aldehyde. Biochemistry 35, 12893-12900.
84. Murshudov, G., Vagin, A., and Dodson, E. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255.
85. Notredame, C., Higgins, D., and Heringa, J. (2000). T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217.
86. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Macromolecular Crystallography. Pt A 276, 307-326.
87. Perkins, D.N., Pappin, D.J., Creasy, D.M., and Cottrell, J.S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567.
88. Scrima, A., Konícková, R., Czyzewski, B.K., Kawasaki, Y., Jeffrey, P.D., Groisman, R., Nakatani, Y., Iwai, S., Pavletich, N.P., and Thomä, N.H. (2008). Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135, 1213-1223.
89. Sugasawa, K. (2006). The xeroderma pigmentosum group C protein complex and ultraviolet-damaged DNA-binding protein: functional assays for damage recognition factors involved in global genome repair. Methods Enzymol. 408, 171-188.
90. Tarpey, P.S., Raymond, F.L., O'Meara, S., Edkins, S., Teague, J., Butler, A., Dicks, E., Stevens, C., Tofts, C., Avis, T., et al. (2007). Mutations in CUL4B, which encodes a ubiquitin E3 ligase subunit, cause an X-linked mental retardation syndrome associated with aggressive outbursts, seizures, relative macrocephaly, central obesity, hypogonadism, pes cavus, and tremor. Am. J. Hum. Genet. 80, 345-352.
91. Vagin, A., and Teplyakov, A. (1997). MOLREP: an automated program for molecular replacement. Journal of Applied Crystallography.
92. Vassylyev, D.G., Kashiwagi, T., Mikami, Y., Ariyoshi, M., Iwai, S., Ohtsuka, E., and Morikawa, K. (1995). Atomic model of a pyrimidine dimer excision repair enzyme complexed with a DNA substrate: structural basis for damaged DNA recognition. Cell 83, 773-782.
93. Yang, W. (2008). Structure and mechanism for DNA lesion recognition. Cell Res. 18, 184-197.
94. Yasuda, T., Sugasawa, K., Shimizu, Y., Iwai, S., Shiomi, T., and Hanaoka, F. (2005). Nucleosomal structure of undamaged DNA regions suppresses the non-specific DNA binding of the XPC complex. DNA Repair (Amst.) 4, 389-395.
95. Zhou, C., Wee, S., Rhee, E., Naumann, M., Dubiel, W., and Wolf, D.A. (2003). Fission yeast COP9/signalosome suppresses cullin activity through recruitment of the deubiquitylating enzyme Ubp12p. Mol. Cell 11, 927-938.