Initiation of DNA interstrand cross-link repair in humans: The nucleotide excision repair system makes dual incisions 5' to the cross- linked base and removes a 22- to 28-nucleotide-long damage-free strand

Molecular and Cellular Biology

Volumn 17, Issue 12, 1997, Pages 6822-6830

  Bessho, Tadayoshi ^a   Mu, David ^a   Sancar, Aziz ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEASE; NUCLEOTIDE;

ANIMAL CELL; ARTICLE; CHO CELL; CROSS LINKING; DNA CROSS LINKING; DNA REPAIR; DNA STRAND; EXCISION REPAIR; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANIMALIA; MAMMALIA; RODENTIA;

EID: 0030667311     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.12.6822     Document Type: Article

References (70)

1. Bardwell, A. J., L. Bardwell, A. E. Tomkinson, and E. C. Friedberg. 1994. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science 265:2082-2085.
2. Bessho, T., A. Sancar, L. H. Thompson, and M. P. Thelen. 1997. Reconstitution of human excision nuclease with recombinant XPF-ERCC1 complex. J. Biol. Chem. 272:3833-3837.
3. Bredberg, A., and S. Söderhall. 1985. Normal rate of DNA breakage in xeroderma pigmentosum complementation group E cells treated with 8-methoxypsoralen plus near-ultraviolet radiation. Biochim. Biophys. Acta 824:268-271.
4. Calsou, P., E. Sage, E. Moustacchi, and B. Salles. 1996. Preferential repair incision of crosslink versus monoadducts in psoralen-damaged plasmid DNA by human cell-free extracts. Biochemistry 35:14963-14969.
5. Chatterjee, P. K., and C. R. Cantor. 1978. Photochemical production of psoralen-DNA monoadducts capable of subsequent photocrosslinking. Nucleic Acids Res. 5:3619-3633.
6. Cheng, S., A. Sancar, and J. E. Hearst. 1991. RecA-dependent incision of psoralen-crosslinked DNA by (A)BC excinuclease. Nucleic Acids Res. 19: 657-663.
7. Cheng, S., B. Van Houten, H. B. Gamper, A. Sancar, and J. E. Hearst. 1988. Use of psoralen-modified oligonucleotidcs to trap three-stranded RecA-DNA complexes and repair of these cross-linked complexes by ABC excinuclease. J. Biol. Chem. 263:15110-15117.
8. Cimino, G. D., H. B. Gamper, S. T. Isaacs, and J. E. Hearst. 1985. Psoralens as photoactive probes of nucleic acid structure and function: organic chemistry, photochemistry, and biochemistry. Annu. Rev. Biochem. 54:1151-1194.
9. Cole, R. S. 1973. Repair of DNA containing interstrand cross-links in Escherichia coli: sequential excision and recombination. Proc. Natl. Acad. Sci. USA 70:1064-1068.
10. Dardalhon, M., and D. Averbeck. 1995. Pulsed-field gel electrophoresis analysis of the repair of psoralen plus UVA induced DNA photoadducts in Saccharomyces cerevisiae. Mutat. Res. 336:49-60.
11. Digweed, M., and K. Sperling. 1996. Molecular analysis of Fanconi anemia. BioEssays 18:579-585.
12. Evans, E., J. Fellows, A. Coffer, and R. D. Wood. 1997. Open complex formation around a lesion during nucleotide excision repair provides a structure for cleavage by human XPG protein. EMBO J. 16:625-638.
13. Faruqi, A. F., M. M. Seidman, D. J. Segal, D. Carroll, and P. M. Glazer. 1996. Recombination induced by triple-helix targeted DNA damage in mammalian cells. Mol. Cell. Biol. 16:6820-6828.
14. Fendrick, J. L., and L. M. Hallick. 1984. Psoralen photoinactivation of herpes simplex virus: monoadduct and cross-link repair by xeroderma pigmentosum and Fanconi's anemia cells. J. Invest. Dermatol. 83:968-1015.
15. Fishman-Lobell, J., and J. E. Haber. 1992. Removal of non-homologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258:480-484.
16. Fornace, A. J., J. B. Little, and R. R. Weichselbaum. 1979. DNA repair in a Fanconi anemia fibroblast cell strain. Biochim. Biophys. Acta 561:99-109.
17. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA repair and mutagenesis. American Society for Microbiology, Washington, D.C.
18. Fujiwara, Y., M. Tatsumi, and M. S. Sasaki. 1977. Crosslink repair in human cells and its possible defect in Fanconi's anemia cells. J. Mol. Biol. 113:635-649.
19. Fujiwara, Y., M. Nakamura, and S. Yokoo. 1993. A new anticancer platinum compound, (-)-(R)-2-aminomethyl-pyrrolidine(1,1-cyclobutanedicarboxylate) platinum (II): DNA interstrand crosslinking, repair and lethal effects in normal human, Fanconi's anemia and xeroderma pigmentosum cells. Br. J. Cancer 67:1285-1292.
20. Hoy, C. A., L. H. Thompson, C. L. Mooney, and E. P. Salazar. 1985. Defective DNA cross-link removal in Chinese hamster cell mutants hypersensitive to bifunctional alkylating agents. Cancer Res. 45:1737-1743.
21. Huang, J. C., D. L. Svoboda, J. T. Reardon, and A. Sancar. 1992. Human nucleotide excision nuclease removes thymine dimers by hydrolyzing the 22nd phosphodiester bond 5′ and the 6th phosphodiester bond 3′ to the photodimer. Proc. Natl. Acad. Sci. USA 89:3664-3668.
22. Huang, J. C., D. S. Hsu, A. Kazantsev, and A. Sancar. 1994. Substrate spectrum of human excinuclease: repair of abasic sites, methylated bases, mismatches, and bulky adducts. Proc. Natl. Acad. Sci. USA 91:12213-12217.
23. Huang, J. C., and A. Sancar. 1994. Determination of minimum size substrate for human excinuclease. J. Biol. Chem. 269:19034-19040.
24. Islas, A. L., J. M. H. Vos, and P. C. Hanawalt. 1991. Differential introduction and repair of psoralen photoadducts to DNA in specific human genes. Cancer Res. 51:2867-2873.
25. Ivanov, E. L., and J. E. Haber. 1995. RAD1 and RAD10, but not other excision repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:2245-2251.
26. Jachymczyk, W. J., R. C. von Borstel, M. R. Mowat, and P. J. Hastings. 1981. Repair of interstrand cross-links in DNA of Saccharomyces cerevisiae requires two systems for DNA repair: the RAD3 system and the RAD51 system. Mol. Gen. Genet. 182:196-205.
27. Jeggo, P. A., G. E. Taccioli, and S. P. Jackson. 1995. Menage a trois: double-strand break repair, V(D)J recombination and DNA-PK. BioEssays 17:949-957.
28. Jones, B. K., and A. T. Yeung. 1990. DNA base composition determines the specificity of UvrABC endonuclease incision of a psoralen cross-link. J. Biol. Chem. 265:3489-3496.
29. Jones, N. J. 1994. Genetic analysis of mitomycin C-hypersensitive Chinese hamster cell mutants. Mutagenesis 9:477-482.
30. Kaye, J., C. A. Smith, and C. A. Hanawalt. 1980. DNA repair in human cells containing photoadducts of 8-methoxypsoralen or angelicin. Cancer Res. 40:696-702.
31. Kohn, K. W. 1996. Beyond DNA cross-linking: history and prospects of DNA-targeted cancer treatment. Cancer Res. 56:5533-5546.
32. Kumaresan, K., B. Hang, and M. W. Lambert. 1995. Human endonucleolytic incision of DNA 3′ and 5′ to a site-directed psoralen monoadduct and interstrand cross-link. J. Biol. Chem. 270:30709-30716.
33. Magana-Schwencke, N., J. A. Henriques, R. Chanet, and E. Moustacchi. 1982. The fate of 8-methoxypsoralen photoinduced crosslinks in nuclear and mitochondrial yeast DNA: comparison of wild-type and repair-deficient strains Proc. Natl. Acad. Sci. USA 79:1722-1726.
34. Matsunaga, T., D. Mu, C. H. Park, J. T. Reardon, and A. Sancar. 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. 270:20862-20869.
35. Matsunaga, T., C. H. Park, T. Bessho, D. Mu, and A. Sancar. 1996. Replication protein A confers structure-specific endonuclease activities to the XPF-ERCC1 and XPG subunits of human DNA repair excision nuclease. J. Biol. Chem. 271:11047-11050.
36. Miller, R. D., L. Prakash, and S. Prakash. 1982. Genetic control of Saccharomyces cerevisiae interstrand DNA cross-link induced by psoralen plus near-UV light. Mol. Cell. Biol. 2:939-948.
37. 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.
38. Mu, D., D. S. Hsu, and A. Sancar. 1996. Reaction mechanism of human DNA repair excision nuclease. J. Biol. Chem. 271:8285-8294.
39. Mu, D., and A. Sancar. 1997. Model for XPC-independent transcription-coupled repair of pyrimidine dimers in humans. J. Biol. Chem. 272:7570-7573.
40. Mu, D., M. Tursun, D. R. Duckett, J. T. Drummond, P. Modrich, and A. Sancar. 1997. Recognition and repair of compound DNA lesions (base damage and mismatch) by human mismatch repair and excision repair systems. Mol. Cell. Biol. 17:760-769.
41. Munn, M. M., and W. D. Rupp. 1991. Interaction of the UvrABC endonuclease with DNA containing a psoralen monoadduct or crosslink. J. Biol. Chem. 266:24748-24756.
42. Nichols, A. F. 1994. Characterization of mammalian excision nuclease. Ph.D. dissertation University of North Carolina, Chapel Hill.
43. Park, C. H., T. Bessho, T. Matsunaga, and A. Sancar. 1995. Purification and characterization of the XPF-ERCC1 complex of human DNA repair excision nuclease. J. Biol. Chem. 270:22651-22660.
44. Prakash, S., P. Sung, and L. Prakash. 1993. DNA repair genes and proteins of Saccharomyces cerevisiae. Annu. Rev. Genet. 263:12228-12234.
45. Reardon, J. T., P. Spielmann, J. C. Huang, S. Sastry, J. E. Hearst, and A. Sancar. 1991. Removal of psoralen monoadducts and crosslinks by human cell free extracts. Nucleic Acids Res. 19:4623-4629.
46. Reardon, J. T., L. H. Thompson, and A. Sancar. 1993. Excision repair in man and the molecular basis of xeroderma pigmentosum syndrome. Cold Spring Harbor Symp. Quant. Biol. 58:605-617.
47. Saffran, W. A., R. B. Greenberg, M. S. Thaler-Scheer, and M. M. Jones. 1994. Single strand and double strand DNA damage-induced reciprocal recombination in yeast: dependence on nucleotide excision repair and RAD1 recombination. Nucleic Acids Res. 22:2823-2829.
48. Sage, E., E. A. Drobetsky, and E. Moustacchi. 1993. 8-Methoxypsoralen induced mutations are highly targeted at crosslinkable sites of photoaddition on the non-transcribed strand of a mammalian chromosomal gene. EMBO J. 12:397-402.
49. Sancar, A. 1996. DNA excision repair. Annu. Rev. Biochem. 65:43-81.
50. Sasaki, M. S., and A. Tonomura. 1973. A high susceptibility of Fanconi's anemia to chromosome breakage by DNA cross-linking agents. Cancer Res. 33:1829-1836.
51. Schiestl, R. H., and S. Prakash. 1988. RAD1, an excision repair gene of Saccharomyces cerevisiae, is also involved in recombination. Mol. Cell. Biol. 8:3619-3626.
52. Schiestl, R. H., and S. Prakash. 1990. RAD10, an excision repair gene of Saccharomyces cerevisiae, is involved in the RAD1 pathway of mitotic recombination. Mol. Cell. Biol. 10:2485-2491.
53. Sekelsky, J. J., K. S. McKim, G. M. Chin, and R. S. Hawley. 1995. The Drosophila meiotic recombination gene mei-9 encodes a homologue of the yeast excision repair protein Rad1. Genetics 141:619-627.
54. Shi, Y. B., H. Gamper, and J. E. Hearst. 1987. The effects of covalent additions of a psoralen on transcription by E. coli RNA polymerase. Nucleic Acids Res. 15:6843-6864.
55. Sladek, F. M., M. M. Munn, W. D. Rupp, and P. Howard-Flanders. 1989. In vitro repair of psoralen-DNA cross-links by RecA, UvrABC, and the 5′-exonuclease of DNA polymerase I. J. Biol. Chem. 264:6755-6765.
56. Stahl, F. W. 1996. Meiotic recombination in yeast: coronation of the double-strand-break repair model. Cell 87:965-968.
57. Sung, P., P. Reynolds, L. Prakash, and S. Prakash. 1993. Purification and characterization of the Saccharomyces cerevisiae RAD1/RAD10 endonuclease. J. Biol. Chem. 268:26391-26399.
58. Svoboda, D. L., J. S. Taylor, J. E. Hearst, and A. Sancar. 1993. DNA repair by eukaryotic nucleotide excision nuclease: removal of thymine dimer and psoralen monoadduct by HeLa cell free extract and of thymine dimer by Xenopus oocytes. J. Biol. Chem. 268:1931-1936.
59. Szostak, J. W., T. L. Orr-Weaver, R. J. Rothstein, and F. W. Stahl. 1983. The double strand break model for recombination. Cell 33:24.
60. Thompson, L. H. 1996. Evidence that mammalian cells possess homologous recombinational repair pathways. Mutat. Res. 363:77-88.
61. Tomkinson, A. E., A. Bardwell, L. Bardwell, N. J. Tappe, and E. C. Friedberg. 1993. Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-stranded DNA endonuclease. Nature 263:860-862.
62. Van Houten, B., H. Gamper, S. R. Holbrook, J. E. Hearst, and A. Sancar. 1986. Action mechanism of ABC excision nuclease on a DNA substrate containing a psoralen crosslink at a defined position. Proc. Natl. Acad. Sci. USA 83:8077-8081.
63. Vos, J.-M., and P. C. Hanawalt. 1987. Processing of psoralen adducts in an active gene: repair and replication of DNA containing monoadducts and interstrand cross-links. Cell 50:789-799.
64. Vos, J.-M., and P. C. Hanawalt. 1989. DNA interstrand cross-links promote chromosomal integration of a selected gene in human cells. Mol. Cell. Biol. 9:2897-2905.
65. Vuksanovic, L., and J. E. Cleaver. 1987. Unique cross-link and monoadduct repair characteristic of a xeroderma pigmentosum revertant cell line. Mutat. Res. 184:255-263.
66. Wood, R. 1996. DNA repair in eukaryotes. Annu. Rev. Biochem. 65:135-167.
67. Zamble, D. B., D. Mu, J. T. Reardon, and S. J. Lippard. 1996. Repair of cisplatin-DNA adducts by the mammalian excision nuclease. Biochemistry 35:10004-10013.
68. Zdzienicka, M. Z. 1995. Mammalian mutants defective in the response to ionizing radiation-induced DNA damage. Mutat. Res. 336:203-213.
69. Zhen, W., M. K. Evans, C. M. Haggerty, and V. A. Bohr. 1993. Deficient gene specific repair of cisplatin-induced lesions in xeroderma pigmentosum and Fanconi's anemia cell lines. Carcinogenesis 14:919-924.
70. Zwelling, L. A., S. Michaels, S. Schwartz, P. P. Dobson, and K. W. Kohn. 1981. DNA cross-linking as an indicator of sensitivity and resistance of mouse L1210 leukemia to cis-diaminedichloroplatinum (II) and L-phenylalanine mustard. Cancer Res. 41:640-649.