Open complex formation around a lesion during nucleotide excision repair provides a structure for cleavage by human XPG protein

EMBO Journal

Volumn 16, Issue 3, 1997, Pages 625-638

  Evans, Elizabeth ^a   Fellows, Jane ^a   Coffer, Arnold ^a   Wood, Richard D ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Cisplatin; DNA repair; Endonuclease; Footprinting; Xeroderma pigmentosum

Indexed keywords

CISPLATIN; NUCLEASE;

ARTICLE; COMPLEX FORMATION; DNA ADDUCT; DNA CLEAVAGE; DNA FOOTPRINTING; DNA REPAIR; DNA STRUCTURE; DRUG DNA INTERACTION; EXCISION REPAIR; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENTS; ASPERGILLUS NUCLEASE S1; BASE SEQUENCE; CISPLATIN; DNA DAMAGE; DNA FOOTPRINTING; DNA REPAIR; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDONUCLEASES; HUMANS; INTERCALATING AGENTS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; OLIGODEOXYRIBONUCLEOTIDES; PROLIFERATING CELL NUCLEAR ANTIGEN; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

EID: 0031013308     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.3.625     Document Type: Article

References (59)

1. Aboussekhra, A. et al. (1995) Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell, 80, 859-868.
2. Anin, M. and Leng, M. (1990) Distortions induced in double-stranded oligonucleotides by the binding of cis-or trans-diamminedichloroplatinum(II) to the d(GTG) sequence. Nucleic Acids Res., 18, 4395-4400.
3. Asahina, H., Kuraoka, I., Shirakawa, M., Morita, E.H., Miura, N., Miyamoto, I., Ohtsuka, E., Okada, Y. and Tanaka, K. (1994) The XPA protein is a zinc metalloprotein with an ability to recognize various kinds of DNA-damage. Mutat. Res., 315, 229-237.
4. Bardwell, A.J., Bardwell, L., Tomkinson, A.E. and Friedberg, E.C. (1994) Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science, 265, 2082-2085.
5. Barone, F., Bonincontro, A., Mazzei, F., Minoprio, A. and Pedone, F. (1995) Effect of thymine dimer introduction in a 21 base pair oligonucleotide Photochem. Photobiol., 61, 61-67.
6. Bellon, S.F., Coleman, J.H. and Lippard, S.J. (1991) DNA unwinding produced by site-specific intrastrand crosslinks of the antitumor drug cis-diamminedichloroplatinum(II). Biochemistry, 30, 8026-8035.
7. Blackwell, L.J. and Borowiec, J.A. (1994) Human replication protein A binds single-stranded DNA in two distinct complexes. Mol. Cell. Biol., 14, 3993-4001.
8. Borowiec, J.A., Zhang, L., Sasse-Dwight, S. and Gralla, J.D. (1987) DNA supercoiling promotes formation of a bent repression loop in lac DNA. J. Mol. Biol., 196, 101-111.
9. Borowiec, J.A., Dean, F.B., Bullock, P.A. and Hurwitz, J. (1988) Localized melting and structural changes in the SV40 origin of replication induced by T antigen. EMBO J., 7, 3149-3158.
10. Bowater, R.P., Aboul-ela, F. and Lilley, D.M. (1994) Large-scale opening of A + T rich regions within supercoiled DNA molecules is suppressed by salt. Nucleic Acids Res., 22, 2042-2050.
11. Bramhill, D. and Kornberg, A. (1988) Duplex opening by DnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell, 52, 743-755.
12. Calsou, P. and Salles, B. (1994) Properties of damage-dependent DNA incision by nucleotide excision-repair in human cell-free-extracts. Nucleic Acids Res., 22, 4937-4942.
13. Carr, A.M., Sheldrick, K.S., Murray, J.M., Al-Harithy, R., Watts, F.Z. and Lehmann, A.R. (1993) Evolutionary conservation of excision repair in Schizosaccharomyces pombe-evidence for a family of sequences related to the Saccharomyces cerevisiae RAD2 gene. Nucleic Acids Res., 21, 1345-1349.
14. Cloud, K., Shen, B., Strniste, G. and Park, M. (1995) XPG protein has structure-specific endonuclease activity. Mutat. Res., 347, 55-60.
15. Coverley, D., Kenny, M.K., Lane, D.P. and Wood, R.D. (1992) A role for the human single-stranded DNA binding protein HSSB/RPA in an early stage of nucleotide excision repair. Nucleic Acids Res., 20, 3873-3880.
16. Davies, A.A., Friedberg, E.C., Tomkinson, A.E., Wood, R.D. and West, S.C. (1995) Role of the Rad1 and Rad10 proteins in nucleotide excision repair and recombination. J. Biol. Chem., 270, 24638-24641.
17. Friedberg, E.C., Walker, G.C. and Siede, W. (1995) DNA Repair and Mutagenesis. ASM Press, Washington, DC, p. 247.
18. Georgaki, A., Strack, B., Podust, V. and Hübscher, U. (1992) DNA unwinding activity of replication protein A. FEBS Lett., 308, 240-244.
19. Gold, L., Polisky, B., Uhlenbeck, O. and Yarus, M. (1995) Diversity of oligonucleotide functions. Annu. Rev. Biochem., 64, 763-797.
20. Habraken, Y., Sung, P. Prakash, L. and Prakash, S. (1994a) A conserved 5′ to 3′ exonuclease activity in the yeast and human nucleotide excision repair proteins Rad2 and XPG. J. Biol. Chem., 269, 31342-31345.
21. Habraken, Y., Sung, P., Prakash, L. and Prakash, S. (1994b) Human xeroderma pigmentosum group G gene encodes a DNA endonuclease. Nucleic Acids Res., 22, 3312-3316.
22. Habraken, Y., Sung, P., Prakash, L. and Prakash, S. (1995) Structure-specific nuclease activity in yeast nucleotide excision-repair protein Rad2. J. Biol. Chem., 270, 30194-30198.
23. Harrington, J.J. and Lieber, M.R. (1994) Functional domains within FEN-1 and Rad2 define a family of structure-specific endonucleases -implications for nucleotide excision-repair. Genes Dev., 8, 1344-1355.
24. He, Z., Henricksen, L.A., Wold, M.S. and Ingles, C.J. (1995) RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature, 374, 566-569.
25. Hoeijmakers, J.H.J., Egly, J.M. and Vermeulen, W. (1996) TFIIH - a key component in multiple DNA transactions. Curr. Opin. Genet. Dev., 6, 26-33.
26. Ishimi, Y. and Matsumoto, K. (1994) Loading of a DNA helicase on the DNA unwinding element in the yeast replication origin: mechanism of DNA replication in a model system. Biochemistry, 33, 2733-2740.
27. Jiang, Y. and Gralla, J.D. (1995) Nucleotide requirement for activated RNA polymerase II open complex formation in vitro. J. Biol. Chem., 270, 1277-1281.
28. Jones, C.J. and Wood, R.D. (1993) Preferential binding of the xeroderma pigmentosum group A complementing protein to damaged DNA. Biochemistry, 32, 12096-12104.
29. Kim, C. Snyder, R.O. and Wold, M.S. (1992) Binding properties of replication protein-A from human and veast cells. Mol. Cell. Biol., 12, 3050-3059.
30. Kim, J.-K. and Choi, B. (1995) The solution structure of DNA duplex-decamer containing the (6-4) photoproduct of thymidylyl(3′→5′)thymidine by NMR and relaxation matrix refinement. Eur. J. Biochem., 228, 849-854.
31. Kowalski, D. (1984) Changes in site specificity of single-strand-specific endonucleases on supercoiled PM2 DNA with temperature and ionic environment. Nucleic Acids Res., 12, 7071-7086.
32. Li, L., Lu, X.Y., Peterson, C.A. and Legerski, R.J. (1995a) An interaction between the DNA-repair factor XPA and replication protein-A appears essential for nucleotide excision-repair. Mol. Cell. Biol., 15, 5396-5402.
33. Li, L., Peterson, C.A., Lu, X.Y. and Legerski, R.J. (1995b) Mutations in XPA that prevent association with ERCC1 are defective in nucleotide excision-repair. Mol. Cell. Biol., 15, 1993-1998.
34. Li, X., Li, J., Harrington, J., Lieber, M.R. and Burgers, P.M.J. (1995) Lagging strand DNA synthesis at the eukaryotic replication fork involves binding and stimulation of FEN-1 by proliferating cell nuclear antigen. J. Biol. Chem., 270, 22109-22112.
35. Lyamichev, V., Brow, M.A.D. and Dahlberg, J.E. (1993) Structure-specific endonucleolytic cleavage of nucleic acids by eubacterial DNA polymerases. Science, 260, 778-783.
36. MacInnes, M.A. et al. (1993) Human ERCC5 cDNA-cosmid complementation for excision repair and bipartite amino acid domains conserved with RAD proteins of Saccharomyces cerevisiae and Schizosaccharomyces pombe. Mol. Cell. Biol., 13, 6393-6402.
37. Matsuda, T. et al. (1995) DNA-repair protein XPA binds replication protein-A (RPA). J. Biol. Chem., 270, 4152-4157.
38. Matsunaga, T., Park, C.H., Bessho, T., Mu, D. and Sancar, A. (1996) Replication protein-A confers structure-specific endonuclease activities to the XPF-ERCC1 and XPG subunits of human DNA-repair excision nucleases. J. Biol. Chem., 271, 11047-11050.
39. Moggs, J.G., Yarema, K.J., Essigmann, J.M. and Wood, R.D. (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.
40. Mu, D., Park, C.H., Matsunaga, T. Hsu, D.S., Reardon, J.T. and Sancar, A. (1995) Reconstitution of human DNA-repair excision nuclease in a highly defined system. J. Biol. Chem., 270, 2415-2418.
41. Mu, D., Hsu, D.S. and Sancar, A. (1996) Reaction-mechanism of human DNA-repair excision nuclease. J. Biol. Chem., 271, 8285-8294.
42. Murante, R., Rust, L. and Bambara, R. (1995) Calf 5′ to 3′ exo/ endonuclease must slide from a 5′ end of the substrate to perform structure-specific cleavage. J. Biol. Chem., 270, 30377-30383.
43. Nagai, A. et al. (1995) Enhancement of damage-specific DNA binding of XPA by interaction with the ERCC1 DNA repair protein. Biochem. Biophys. Res. Commun., 211, 960-966.
44. O'Donovan, A., Davies, A.A., Moggs, J.G., West, S.C. and Wood, R.D. (1994a) XPG endonuclease makes the 3′ incision in human DNA nucleotide excision repair. Nature, 371, 432-435.
45. O'Donovan, A., Scherly, D., Clarkson, S.G. and Wood, R.D. (1994b) Isolation of active recombinant XPG protein, a human DNA repair endonuclease. J. Biol. Chem., 269, 15965-15968.
46. Park, C.H. and Sancar, A. (1994) Formation of a ternary complex by human XPA, ERCC1, and ERCC4(XPF) excision-repair proteins. Proc. Natl Acad. Sci. USA, 91, 5017-5021.
47. Park, C.H., Mu, D., Reardon, J.T. and Sancar, A. (1995) The general transcription-repair factor TFIIH is recruited to the excision-repair complex by the XPA protein independent of the TFIIE transcription factor. J. Biol. Chem., 270, 4896-4902.
48. Robins, P., Jones, C.J., Biggerstaff, M., Lindahl, T. and Wood, R.D. (1991) Complementation of DNA repair in xeroderma pigmentosum group A cell extracts by a protein with affinity for damaged DNA EMBO J., 10, 3913-3921.
49. Robins, P. Pappin, D.J.C. Wood, R.D. and Lindahl, T. (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.
50. Schaeffer, L., Roy, R., Humbert, S., Moncollin, V., Vermeulen, W., Hoeijmakers, J.H.J., Chambon, P. and Egly, J.M. (1993) DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science, 260, 58-63.
51. Scherly, D., Nouspikel, T., Corlet, J., Ucla, C., Bairoch, A. and Clarkson, S.G. (1993) Complementation of the DNA repair defect in xeroderma pigmentosum group G cells by a human cDNA related to yeast RAD2. Nature, 363, 182-185.
52. Schwartz, A. and Leng, M. (1994) DNase-I footprinting of cis-or trans-diamminedichloroplatinum(II)-modified DNA. J. Mol. Biol., 236, 969-974.
53. Shivji, M.K.K., Kenny, M.K. and Wood, R.D. (1992) Proliferating cell nuclear antigen is required for DNA excision repair. Cell, 69, 367-374.
54. Sijbers, A.M. et al. (1996) Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell, 86, 811-822.
55. 2[d(-GTG-)-N7(G), N7(G)] adduct, as determined with high-field NMR and molecular mechanics/ dynamics. Eur. J. Biochem., 225, 1169-1179.
56. Visse, R., King, A., Moolenaar, G.F., Goosen, N. and van de Putte, P. (1994) Protein-DNA interactions and alterations in the DNA-structure upon UvrB DNA preincision complex formation during nucleotide excision repair in Escherichia coli. Biochemistry, 33, 9881-9888.
57. Wood, R.D., Robins, P. and Lindahl, T. (1988) Complementation of the xeroderma pigmentosum DNA repair defect in cell-free extracts. Cell, 53, 97-106.
58. Wood, R.D., Biggerstaff, M. and Shivji, M.K.K. (1995) Detection and measurement of nucleotide excision repair synthesis by mammalian cell extracts in vitro. Methods, 7, 163-175.
59. Wu, X., Li, J., Li, X., Hsieh, C., Burgers, P. and Lieber, M. (1996) Processing of branched DNA intermediates by a complex of human FEN-1 and PCNA. Nucleic Acids Res., 24, 2036-2043.