Structural and functional evidence that Rad4 competes with Rad2 for binding to the Tfb1 subunit of TFIIH in NER

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2736-2745

  Lafrance Vanasse, Julien ^a   Arseneault, Genevie Ve ^a   Cappadocia, Laurent ^a   Legault, Pascale ^a   Omichinski, James G ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEIC ACID BINDING PROTEIN; PROTEIN RAD2; PROTEIN RAD4; PROTEIN TFB1; TRANSCRIPTION FACTOR IIH; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; EXCISION REPAIR; IN VIVO STUDY; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; ULTRAVIOLET IRRADIATION;

AMINO ACID SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; DNA REPAIR; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; MICROBIAL VIABILITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS, TFII; ULTRAVIOLET RAYS;

EID: 84876384740     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1321     Document Type: Article

References (57)

1. Friedberg, E.C., Walker, G.C., Siede, W., Wood, R.D., Schultz, T. and Ellenberger, T. (2005) DNA Repair and Mutagenesis. ASM Press, Washington, DC.
2. Lehmann, A.R. (2003) DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie, 85, 1101-1111.
3. Cartault, F., Nava, C., Malbrunot, A.C., Munier, P., Hebert, J.C., N'Guyen, P., Djeridi, N., Pariaud, P., Pariaud, J., Dupuy, A. et al. (2011) A new XPC gene splicing mutation has lead to the highest worldwide prevalence of xeroderma pigmentosum in black Mahori patients. DNA Repair, 10, 577-585.
4. Hoeijmakers, J.H. (2001) Genome maintenance mechanisms for preventing cancer. Nature, 411, 366-374.
5. Sugasawa, K., Ng, J.M., Masutani, C., Iwai, S., van der Spek, P.J., Eker, A.P., Hanaoka, F., Bootsma, D. and Hoeijmakers, J.H. (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell, 2, 223-232.
6. Fitch, M.E., Nakajima, S., Yasui, A. and Ford, J.M. (2003) In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product. J. Biol. Chem., 278, 46906-46910.
7. Tantin, D., Kansal, A. and Carey, M. (1997) Recruitment of the putative transcription-repair coupling factor CSB/ERCC6 to RNA polymerase II elongation complexes. Mol. Cell. Biol., 17, 6803-6814.
8. Sarker, A.H., Tsutakawa, S.E., Kostek, S., Ng, C., Shin, D.S., Peris, M., Campeau, E., Tainer, J.A., Nogales, E. and Cooper, P.K. (2005) Recognition of RNA polymerase II and transcription bubbles by XPG, CSB, and TFIIH: insights for transcriptioncoupled repair and Cockayne syndrome. Mol. Cell, 20, 187-198.
9. Bardwell, A.J., Bardwell, L., Iyer, N., Svejstrup, J.Q., Feaver, W.J., Kornberg, R.D. and Friedberg, E.C. (1994) Yeast nucleotide excision repair proteins Rad2 and Rad4 interact with RNA polymerase II basal transcription factor b (TFIIH). Mol. Cell. Biol., 14, 3569-3576.
10. Araujo, S.J., Nigg, E.A. and Wood, R.D. (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.
11. Yokoi, M., Masutani, C., Maekawa, T., Sugasawa, K., Ohkuma, Y. and 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.
12. Min, J.-H. and Pavletich, N.P. (2007) Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature, 449, 570-575.
13. Miron, S., Duchambon, P., Blouquit, Y., Durand, D. and Craescu, C.T. (2008) The carboxy-terminal domain of xeroderma pigmentosum complementation group C protein, involved in TFIIH and centrin binding, is highly disordered. Biochemistry, 47, 1403-1413.
14. Chen, L. and Madura, K. (2008) Centrin/Cdc31 is a novel regulator of protein degradation. Mol. Cell. Biol., 28, 1829-1840.
15. den Dulk, B., van Eijk, P., de Ruijter, M., Brandsma, J.A. and Brouwer, J. (2008) The NER protein Rad33 shows functional homology to human Centrin2 and is involved in modification of Rad4. DNA Repair, 7, 858-868.
16. Popescu, A., Miron, S., Blouquit, Y., Duchambon, P., Christova, P. and Craescu, C.T. (2003) Xeroderma pigmentosum group C protein possesses a high affinity binding site to human centrin 2 and calmodulin. J. Biol. Chem., 278, 40252-40261.
17. Uchida, A., Sugasawa, K., Masutani, C., Dohmae, N., Araki, M., Yokoi, M., Ohkuma, Y. and Hanaoka, F. (2002) The carboxy-terminal domain of the XPC protein plays a crucial role in nucleotide excision repair through interactions with transcription factor IIH. DNA Repair, 1, 449-461.
18. Coin, F., Oksenych, V. and Egly, J.-M. (2007) Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol. Cell, 26, 245-256.
19. Schärer, O.D. (2008) The molecular basis for different disease states caused by mutations in TFIIH and XPG. DNA Repair, 7, 339-344.
20. Riedl, T., Hanaoka, F. and Egly, J.M. (2003) The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J., 22, 5293-5303.
21. Wakasugi, M. and Sancar, A. (1998) Assembly, subunit composition, and footprint of human DNA repair excision nuclease. Proc. Natl Acad. Sci. USA, 95, 6669-6674.
22. Bernardes de Jesus, B.M., Bjoras, M., Coin, F. and Egly, J.M. (2008) Dissection of the molecular defects caused by pathogenic mutations in the DNA repair factor XPC. Mol. Cell. Biol., 28, 7225-7235.
23. Hohl, M., Dunand-Sauthier, I., Staresincic, L., Jaquier-Gubler, P., Thorel, F., Modesti, M., Clarkson, S.G. and Schärer, O.D. (2007) Domain swapping between FEN-1 and XPG defines regions in XPG that mediate nucleotide excision repair activity and substrate specificity. Nucleic Acids Res., 35, 3053-3063.
24. Iyer, N., Reagan, M.S., Wu, K.J., Canagarajah, B. and Friedberg, E.C. (1996) Interactions involving the human RNA polymerase II transcription/ nucleotide excision repair complex TFIIH, the nucleotide excision repair protein XPG, and Cockayne syndrome group B (CSB) protein. Biochemistry, 35, 2157-2167.
25. Lafrance-Vanasse, J., Arseneault, G., Cappadocia, L., Chen, H.T., Legault, P. and Omichinski, J.G. (2012) Structural and functional characterization of interactions involving the Tfb1 subunit of TFIIH and the NER factor Rad2. Nucleic Acids Res., 40, 5739-5750.
26. Kaiser, C., Michaelis, S. and Mitchell, A. (1994) Methods in Yeast Genetics. Cold Spring Harbor Laborator Press, Cold Spring Harbor, NY.
27. Di Lello, P., Nguyen, B.D., Jones, T.N., Potempa, K., Kobor, M.S., Legault, P. and Omichinski, J.G. (2005) NMR structure of the amino-terminal domain from the Tfb1 subunit of TFIIH and characterization of its phosphoinositide and VP16 binding sites. Biochemistry, 44, 7678-7686.
28. Houtman, J.C., Higashimoto, Y., Dimasi, N., Cho, S., Yamaguchi, H., Bowden, B., Regan, C., Malchiodi, E.L., Mariuzza, R., Schuck, P. et al. (2004) Binding specificity of multiprotein signaling complexes is determined by both cooperative interactions and affinity preferences. Biochemistry, 43, 4170-4178.
29. Nguyen, B.D., Di Lello, P., Legault, P. and Omichinski, J.G. (2005) 1H, 15N, and 13C resonance assignment of the amino-terminal domain of the Tfb1 subunit of yeast TFIIH. J. Biomol. NMR, 31, 173-174.
30. Kay, L.E., Xu, G.Y. and Yamazaki, T. (1994) Enhanced-sensitivity triple-resonance spectroscopy with minimal H2O saturation. J. Magn. Reson. A, 109, 129-133.
31. Wittekind, M. and Mueller, L. (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J. Magn. Reson. B, 101, 201-205.
32. Grzesiek, S. and Bax, A. (1992) Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc., 114, 6291-6293.
33. Logan, T.M., Olejniczak, E.T., Xu, R.X. and Fesik, S.W. (1992) Side chain and backbone assignments in isotopically labeled proteins from two heteronuclear triple resonance experiments. FEBS Lett., 314, 413-418.
34. Ikura, M., Kay, L.E. and Bax, A. (1991) Improved three-dimensional 1H-13C-1H correlation spectroscopy of a 13Clabeled protein using constant-time evolution. J. Biomol. NMR, 1, 299-304.
35. Yamazaki, T., Forman-Kay, J.D. and Kay, L.E. (1993) Two-dimensional NMR experiments for correlating carbon-13 beta and proton delta/epsilon chemical shifts of aromatic residues in 13C-labeled proteins via scalar couplings. J. Am. Chem. Soc., 115, 11054-11055.
36. Zhang, O., Kay, L.E., Olivier, J.P. and Forman-Kay, J.D. (1994) Backbone 1H and 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques. J. Biomol. NMR, 4, 845-858.
37. Pascal, S.M., Muhandiram, D.R., Yamazaki, T., Forman-Kay, J.D. and Kay, L.E. (1994) Simultaneous acquisition of 15N- and 13C-edited NOE spectra of proteins dissolved in H2O. J. Magn. Reson., 103, 197-201.
38. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
39. Johnson, B.A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol., 278, 313-352.
40. Vranken, W.F., Boucher, W., Stevens, T.J., Fogh, R.H., Pajon, A., Llinas, M., Ulrich, E.L., Markley, J.L., Ionides, J. and Laue, E.D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins, 59, 687-696.
41. Shen, Y., Delaglio, F., Cornilescu, G. and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR, 44, 213-223.
42. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
43. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R. and Thornton, J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486.
44. Koradi, R., Billeter, M. and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph., 14, 51-55.
45. Tremblay, M., Teng, Y., Paquette, M., Waters, R. and Conconi, A. (2008) Complementary roles of yeast Rad4p and Rad34p in nucleotide excision repair of active and inactive rRNA gene chromatin. Mol. Cell. Biol., 28, 7504-7513.
46. den Dulk, B., Brandsma, J.A. and Brouwer, J. (2005) The Rad4 homologue YDR314C is essential for strand-specific repair of RNA polymerase I-transcribed rDNA in Saccharomyces cerevisiae. Mol. Microbiol., 56, 1518-1526.
47. Iben, S., Tschochner, H., Bier, M., Hoogstraten, D., Hozak, P., Egly, J.M. and Grummt, I. (2002) TFIIH plays an essential role in RNA polymerase I transcription. Cell, 109, 297-306.
48. den Dulk, B., Sun, S.M., de Ruijter, M., Brandsma, J.A. and Brouwer, J. (2006) Rad33, a new factor involved in nucleotide excision repair in Saccharomyces cerevisiae. DNA Repair, 5, 683-692.
49. Stauffer, M.E. and Chazin, W.J. (2004) Structural mechanisms of DNA replication, repair, and recombination. J. Biol. Chem., 279, 30915-30918.
50. Wilson, S.H. and Kunkel, T.A. (2000) Passing the baton in base excision repair. Nat. Struct. Biol., 7, 176-178.
51. Dunand-Sauthier, I., Hohl, M., Thorel, F., Jaquier-Gubler, P., Clarkson, S.G. and Schärer, O.D. (2005) The spacer region of XPG mediates recruitment to nucleotide excision repair complexes and determines substrate specificity. J. Biol. Chem., 280, 7030-7037.
52. Thorel, F., Constantinou, A., Dunand-Sauthier, I., Nouspikel, T., Lalle, P., Raams, A., Jaspers, N.G., Vermeulen, W., Shivji, M.K., Wood, R.D. et al. (2004) Definition of a short region of XPG necessary for TFIIH interaction and stable recruitment to sites of UV damage. Mol. Cell. Biol., 24, 10670-10680.
53. Okuda, M., Tanaka, A., Satoh, M., Mizuta, S., Takazawa, M., Ohkuma, Y. and Nishimura, Y. (2008) Structural insight into the TFIIE-TFIIH interaction: TFIIE and p53 share the binding region on TFIIH. EMBO J., 27, 1161-1171.
54. Di Lello, P., Miller Jenkins, L.M., Mas, C., Langlois, C., Malitskaya, E., Fradet-Turcotte, A., Archambault, J., Legault, P. and Omichinski, J.G. (2008) p53 and TFIIEalpha share a common binding site on the Tfb1/p62 subunit of TFIIH. Proc. Natl Acad. Sci. USA, 105, 106-111.
55. Tirode, F., Busso, D., Coin, F. and Egly, J.M. (1999) Reconstitution of the transcription factor TFIIH: assignment of functions for the three enzymatic subunits, XPB, XPD and cdk7. Mol. Cell, 3, 87-95.
56. Lu, H., Zawel, L., Fisher, L., Egly, J.M. and Reinberg, D. (1992) Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature, 358, 641-645.
57. Elagoz, A., Callejo, M., Armstrong, J. and Rokeach, L.A. (1999) Although calnexin is essential in S. pombe, its highly conserved central domain is dispensable for viability. J. Cell Sci., 112, 4449-4460.