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 and Development

Volumn 14, Issue 3, 2000, Pages 349-359

  Araújo, Sofia J ^a   Tirode, Franck ^b   Coin, Frederic ^b   Pospiech, Helmut ^c,d   Syväoja, Juhani E ^c,d   Stucki, Manuel ^e   Hübscher, Ulrich ^e   Egly, Jean Marc ^b   Wood, Richard D ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c UNIVERSITY OF OULU   (Finland)

^d UNIVERSITY OF EASTERN FINLAND   (Finland)

^e UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Cisplatin; DNA polymerase; DNA repair; Kinase; Transcription; Xeroderma pigmentosum

Indexed keywords

DNA POLYMERASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RECOMBINANT PROTEIN;

ARTICLE; DNA FLANKING REGION; DNA REPAIR; ENZYME ACTIVITY; EXCISION REPAIR; HELA CELL; HUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; TRANSCRIPTION REGULATION; XERODERMA PIGMENTOSUM;

CYCLIN-DEPENDENT KINASES; DNA REPAIR; HELA CELLS; HUMANS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; TRANSCRIPTION FACTOR TFIIH; TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS, TFII;

EID: 0242605710     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. Aboussekhra, A., M. Biggerstaff, M.K.K. Shivji, J.A. Vilpo, V. Moncollin, V.N. Podust, M. Protic', U. Hübscher, J.-M. Egly, and R.D. Wood. 1995. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80: 859-868.
2. Adamczewski, J.P., M. Rossignol, J.P. Tassan, E.A. Nigg, V. Moncollin, and J.M. Egly. 1996. MAT1, cdk7 and cyclin H form a kinase complex which is UV light-sensitive upon association with TFIIH. EMBO J. 15: 1877-1884.
3. Araújo, S.J. and R.D. Wood. 1999. Protein complexes in nucleotide excision repair. Mutat. Res. 435: 23-33.
4. Ariza, R.R., S.M. Keyse, J.G. Moggs, and R.D. Wood. 1996. Reversible protein phosphorylation modulates nucleotide excision repair of damaged DNA by human cell extracts. Nucleic Acids Res. 24: 433-440.
5. Biggerstaff, M. and R.D. Wood. 1999. Assay for nucleotide excision repair proteins using mammalian cell extracts and UV damaged plasmid DNA. In DNA repair protocols: Eukaryotic systems (ed. D.S. Henderson), pp. 357-372. Humana Press, Totowa, NJ.
6. Botta, E., T. Nardo, B.C. Broughton, S. Marinoni, A.R. Lehmann, and M. Stefanini. 1998. Analysis of mutations in the XPD gene in Italian patients with trichothiodystrophy -Site of mutation correlates with repair deficiency, but gene dosage appears to determine clinical severity. Am. J. Hum. Genet. 63: 1036-1048.
7. Burglen, L., T. Seroz, P. Miniou, S. Lefebvre, P. Burlet, A. Munnich, E. Pequignot, J.-M. Egly, and J. Melki. 1997. The gene encoding p44, a subunit of the transcription factor TFIIH, is involved in large-scale deletions associated with Werdnig-Hoffmann disease. Am. J. Hum. Genet. 60: 72-79.
8. Chui, G. and S. Linn. 1995. Further characterization of HeLa DNA polymerase ∈. J. Biol. Chem. 270: 7799-7808.
9. Coin, F., J.C. Marinoni, C. Rodolfo, S. Fribourg, A.M. Pedrini, and J.M. Egly. 1998. Mutations in the XPD helicase gene result in XP and TTD phenotypes, preventing interaction between XPD and the p44 subunit of TFIIH. Nat. Genet. 20: 184-188.
10. Coin, F., E. Bergmann, A. Tremeau-Bravard, and J.M. Egly. 1999. Mutations in XPB and XPD helicases found in xeroderma pigmentosum patients impair the transcription function of TFIIH. EMBO J. 18: 1357-1366.
11. Constantinou, A., D. Gunz, E. Evans, P. Lalle, P.A. Bates, R.D. Wood, and S.G. Clarkson. 1999. Conserved residues of human XPG protein important for nuclease activity and function in nucleotide excision repair. J. Biol. Chem. 274: 5637-5648.
12. de Laat, W.L., N.G.J. Jaspers, and J.H.J. Hoeijmakers. 1999. Molecular mechanism of nucleotide excision repair. Genes & Dev. 13: 768-785.
13. Drapkin, R., G. Le Roy, H. Cho, S. Akoulitchev, and D. Reinberg. 1996. Human cyclin-dependent kinase-activating kinase exists in three distinct complexes. Proc. Natl. Acad. Sci. 93: 6488-6493.
14. Dubois, M.F., V.T. Nguyen, S. Bellier, and O. Bensaude. 1994. Inhibitors of transcription such as 5,6-dichloro-1-beta-D- ribofuranosylbenzimidazole and isoquinoline sulfonamide derivatives (H-8 and H-7) promote dephosphorylation of the carboxyl-terminal domain of RNA polymerase II largest subunit. J. Biol. Chem. 269: 13331-13336.
15. Evans, E., J. Fellows, A. Coffer, and R.D. Wood. 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.
16. Evans, E., J.G. Moggs, J.R. Hwang, J.-M. Egly, and R.D. Wood. 1997b. Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. EMBO J. 16: 6559-6573.
17. Feaver, W.J., J.Q. Svejstrup, N.L. Henry, and R.D. Kornberg. 1994. Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK. Cell 79: 1103-1109.
18. Gerard, M., L. Fischer, V. Moncollin, J.-M. Chipoulet, P. Chambon, and J.-M. Egly. 1991. Purification and interaction properties of the human RNA polymerase B(II) general transcription factor BTF2. J. Biol. Chem. 266: 20940-20945.
19. Guzder, S.N., Y. Habraken, P. Sung, L. Prakash, and S. Prakash. 1995. Reconstitution of yeast nucleotide excision-repair with purified Rad proteins, replication protein-A, and transcription factor TFIIH. J. Biol. Chem. 270: 12973-12976.
20. Guzder, S.N., P. Sung, L. Prakash, and S. Prakash. 1997. Yeast Rad7-Rad16 complex, specific for the nucleotide excision-repair of the nontranscribed DNA strand, is an ATP-dependent DNA-damage sensor. J. Biol. Chem. 272: 21665-21668.
21. Guzder, S.N., P. Sung, L. Prakash, and S. Prakash. 1998. The DNA-dependent ATPase activity of yeast nucleotide excision-repair factor-4 and its role in DNA-damage recognition. J. Biol. Chem. 273: 6292-6296.
22. He, Z.G., J.M.S. Wong, H.S. Maniar, S.J. Brill, and C.J. Ingles. 1996. Assessing the requirements for nucleotide excision repair proteins of Saccharomyces cerevisiae in an in vitro system. J. Biol. Chem. 271: 28243-28249.
23. Henricksen, L., C. Umbricht, and M. Wold. 1994. Recombinant replication protein-A - Expression, complex-formation, and functional-characterization. J. Biol. Chem. 269: 11121-11132.
24. Hübscher, U., R. Mossi, E. Ferrari, M. Stucki, and Z.O. Jónsson. 1999. Functional analysis of DNA replication accessory proteins. In Eukaryotic DNA replication (ed. S. Cotterill), pp. 119-137. Oxford University Press, Oxford, UK.
25. Hwang, B.J., J.M. Ford, P.C. Hanawalt, and G. Chu. 1999. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl. Acad. Sci. 96: 424-428.
26. Hwang, J.R., V. Moncollin, W. Vermeulen, T. Seroz, H. van Vuuren, J.H.J. Hoeijmakers, and J.M. Egly. 1996. A 3′-5′ XPB helicase defect in repair/transcription factor TFIIH of xeroderma pigmentosum group-B affects both DNA-repair and transcription. J. Biol. Chem. 271: 15898-15904.
27. Johnson, R.T., S. Squires, G.C. Elliott, G.L. Koch, and A.J. Rainbow. 1985. Xeroderma pigmentosum D-HeLa hybrids with low and high ultraviolet sensitivity associated with normal and diminished DNA repair ability, respectively. J. Cell Sci. 76: 115-133.
28. Jones, C.J. and R.D. Wood. 1993. Preferential binding of the xeroderma pigmentosum group A complementing protein to damaged DNA. Biochemistry 32: 12096-12104.
29. Lauder, S., M. Bankmann, S.N. Guzder, P. Sung, L. Prakash, and S. Prakash. 1996. Dual requirement for the yeast mms19 gene in DNA repair and RNA polymerase II transcription. Mol. Cell. Biol. 16: 6783-6793.
30. Lombaerts, M., M. Tijsterman, R.A. Verhage, and J. Brouwer. 1997. Saccharomyces cerevisiae mms19 mutants are deficient in transcription-coupled and global nucleotide excision repair. Nucleic Acids Res. 25: 3974-3979.
31. Mackenney, V.J., D.J. Barnes, and T. Lindahl. 1997. Specific function of DNA ligase I in simian virus 40 DNA replication by human cell-free extracts is mediated by the amino-terminal non-catalytic domain. J. Biol Chem. 272: 11550-11556.
32. Marinoni, J.C., M.E. Rossignol, and J.M. Egly. 1997. Purification of the transcription/repair factor TFIIH and evaluation of its associated activities in vitro. Methods 12: 235-253.
33. Masutani, C., M. Araki, K. Sugasawa, P.J. van der Spek, A. Yamada, A. Uchida, T. Maekawa, D. Bootsma, J.H.J. Hoeijmakers, and F. Hanaoka. 1997. Identification and characterization of XPC-binding domain of hHR23B. Mol. Cell. Biol. 17: 6915-6923.
34. Moggs, J.G., K.J. Yarema, J.M. Essigmann, and R.D. Wood. 1996. Analysis of incision sites produced by human cell extracts and purified proteins during nucleotide excision repair of a 1,3-intrastrand d(GpTpG)-cisplatin adduct. J. Biol. Chem. 271: 7177-7186.
35. Mu, D., C.H. Park, T. Matsunaga, D.S. Hsu, J.T. Reardon, and A. Sancar. 1995. Reconstitution of human DNA-repair excision nuclease in a highly defined system. J. Biol. Chem. 270: 2415-2418.
36. Mu, D., D.S. Hsu, and A. Sancar. 1996. Reaction-mechanism of human DNA-repair excision nuclease. J. Biol. Chem. 271: 8285-8294.
37. Mu, D., M. Wakasugi, D.S. Hsu, and A. Sancar. 1997. Characterization of reaction intermediates of human excision-repair nuclease. J. Biol. Chem. 272: 28971-28979.
38. Podust, V.N. and U. Hübscher. 1993. Lagging strand DNA synthesis by calf thymus DNA polymerases α, β, δ, and ∈ in the presence of auxiliary proteins. Nucleic Acids Res. 21: 841-846.
39. Reardon, J.T., H. Ge, E. Gibbs, A. Sancar, J. Hurwitz, and Z.Q. Pan. 1996. Isolation and characterization of 2 human transcription factor IIH (TFIIH)-related complexes - ERCC2/ CAK and TFIIH. Proc. Natl. Acad. Sci. 93: 6482-6487.
40. Reed, S.H., Z.Y. You, and E.C. Friedberg. 1998. The yeast RAD7 and RAD16 genes are required for postincision events during nucleotide excision-repair - In-vitro and in-vivo studies with rad7 and rad16 mutants and purification of a Rad7/Rad16-containing protein complex. J. Biol. Chem. 273: 29481-29488.
41. Robins, P., D.J.C. Pappin, R.D. Wood, and T. Lindahl. 1994. Structural and functional homology between mammalian DNase IV and the 5′ nuclease domain of Escherichia coli DNA polymerase I. J. Biol. Chem. 269: 28535-28538.
42. Rossignol, M., I. Kolb-Cheynel, and J.M. Egly. 1997. Substrate specificity of the cdk-activating kinase (CAK) is altered upon association with TFIIH. EMBO J. 16: 1628-1637.
43. Roy, R., J.P. Adamczewski, T. Seroz, W. Vermeulen, J.P. Tassan, L. Schaeffer, E.A. Nigg, J.H.J. Hoeijmakers, and J.M. Egly. 1994. The MO15 cell-cycle kinase is associated with the TFIIH transcription DNA-repair factor. Cell 79: 1093-1101.
44. Shivji, M.K.K., V.N. Podust, U. Hübscher, and R.D. Wood. 1995. Nucleotide excision repair DNA synthesis by DNA polymerase ∈ in the presence of PCNA, RFC, and RPA. Biochemistry 34: 5011-5017.
45. Cdnl. Oncogene 17: 2827-2838.
46. Shivji, M.K.K., J.G. Moggs, I. Kuraoka, and R.D. Wood. 1999. Dual incision assays for nucleotide excision repair using DNA with a lesion at a specific site. In DNA repair protocols: Eukaryotic systems (ed. D.S. Henderson), pp. 373-392. Humana Press, Totowa, NJ.
47. Sijbers, A.M., W.L. de Laat, R.R. Ariza, M. Biggerstaff, Y.-F. Wei, J.G. Moggs, K.C. Carter, B.K. Shell, E. Evans, M.C. de Jong et al. 1996. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 86: 811-822.
48. Stefanini, M., W. Vermeulen, G. Weeda, S. Giliani, T. Nardo, M. Mezzina, A. Sarasin, J.I. Harper, C.F. Arlett, J.H.J. Hoeijmakers, and A.R. Lehmann. 1993. A new nucleotide-excisionrepair gene associated with the disorder trichothiodystrophy. Am. J. Hum. Genet. 53: 817-821.
49. Svejstrup, J.Q., Z. Wang, W.J. Feaver, X. Wu, D.A. Bushnell, T.F. Donahue, E.C. Friedberg, and R.D. Kornberg. 1995. Different forms of TFIIH for transcription and DNA repair: Holo-TFIIH and a nucleotide excision repairosome. Cell 80: 21-28.
50. Svejstrup, J., P. Vichi, and J.-M. Egly. 1996. The multiple roles of transcription/repair factor TFIIH. Trends Biochem. Sci. 21: 346-350.
51. Syväoja, J. and S. Linn. 1989. Characterization of a large form of DNA polymerase 8 from HeLa cells that is insensitive to proliferating cell nuclear antigen. J. Biol. Chem. 264: 2489-2497.
52. Takayama, K., E.P. Salazar, A. Lehmann, M. Stefanini, L.H. Thompson, and C.A. Weber. 1995. Defects in the DNA repair and transcription gene ERCC2 in the cancer-prone dis-order xeroderma pigmentosum group D. Cancer Res. 55: 5656-5663.
53. Taylor, E.M., B.C. Broughton, E. Botta, M. Stefanini, A. Sarasin, N.G.J. Jaspers, H. Fawcett, S.A. Harcourt, C.F. Arlett, and A.R. Lehmann. 1997. Xeroderma pigmentosum and trichothiodystrophy are associated with different mutations in the XPD (ERCC2) repair/transcription gene. Proc. Natl. Acad. Sci. 94: 8658-8663.
54. Tirode, F., D. Busso, F. Coin, and J.M. Egly. 1999. Reconstitution of the transcription factor TFIIH: Assignment of functions for the three enzymatic subunits, XPB, XPD, and cdk7. Mol. Cell 3: 87-95.
55. Verhage, R., A. Zeeman, N. de Groot, F. Gleig, D. Bang, P. van de Putte, and J. Brouwer. 1994. The RAD7 and RAD16 genes, which are essential for pyrimidine dimer removal from the silent mating-type loci, are also required for repair of the nontranscribed strand of an active gene in Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 6135-6142.
56. Vermeulen, W., A.J. van Vuuren, M. Chipoulet, L. Schaeffer, E. Appeldoorn, G. Weeda, N.G.J. Jaspers, A. Priestly, C.F. Arlett, A.R. Lehmann et al. 1994. Three unusual repair deficiencies associated with transcription factor BTF2(TFIIH): Evidence for the existence of a transcription syndrome. Cold Spring Harbor Symp. Quant. Biol. 59: 317-329.
57. Wang, Z.G., S.G. Wei, S.H. Reed, X.H. Wu, J.Q. Svejstrup, W.J. Feaver, R.D. Kornberg, and E.C. Friedberg. 1997. The RAD7, RAD16, and RAD23 genes of Saccharomyces cerevisiae -Requirement for transcription-independent nucleotide excision repair in vitro and interactions between the gene products. Mol. Cell. Biol. 17: 635-643.
58. Weeda, G., R.C.A. van Ham, W. Vermeulen, D. Bootsma, A.J. van der Eb, and J.H.J. Hoeijmakers. 1990. A presumed DNA helicase encoded by the excision repair gene ERCC-3 is involved in the human repair disorders xeroderma pigmento-sum and Cockayne's Syndrome. Cell 62: 777-791.
59. Weiser, T., M. Gassmann, P. Thömmes, E. Ferrari, P. Hafkemeyer, and U. Hübscher. 1991. Biochemical and functional comparison of DNA polymerases α, δ, and ∈ from calf thymus. J. Biol. Chem. 266: 10420-10428.
60. Winkler, G.S., S.J. Araújo, U. Fiedler, W. Vermeulen, F. Coin, J.-M. Egly, J.H.J. Hoeijmakers, R.D. Wood, H.T.M. Timmers, and G. Weeda. 2000. TFIIH with inactive XPD helicase functions in transcription initiation but is defective in DNA repair. J. Biol. Chem. 275: (in press).
61. Wood, R.D., P. Robins, and T. Lindahl. 1988. Complementation of the xeroderma pigmentosum DNA repair defect in cell-free extracts. Cell 53: 97-106.