Mechanism of double-base lesion bypass catalyzed by a Y-family DNA polymerase

Nucleic Acids Research

Volumn 36, Issue 12, 2008, Pages 3867-3878

  Brown, Jessica A ^a   Newmister, Sean A ^a   Fiala, Kevin A ^a   Suo, Zucai ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; DNA POLYMERASE; NUCLEOTIDE;

ARTICLE; CANCER PATIENT; CANCER RESISTANCE; CATALYSIS; CROSS LINKING; DNA ADDUCT; DNA DAMAGE; ENZYME BINDING; GEL MOBILITY SHIFT ASSAY; HUMAN; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SULFOLOBUS SOLFATARICUS;

ANTINEOPLASTIC AGENTS; CATALYSIS; CISPLATIN; DINUCLEOSIDE PHOSPHATES; DNA; DNA DAMAGE; DNA POLYMERASE BETA; DRUG RESISTANCE, NEOPLASM; KINETICS; NUCLEOTIDES; SULFOLOBUS SOLFATARICUS;

SULFOLOBUS SOLFATARICUS;

EID: 47249163382     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn309     Document Type: Article

References (59)

1. Eastman,A. (1983) Characterization of the adducts produced in DNA by cis-diamminedichloroplatinum(II) and cis-dichloro(ethylenediamine)platinum(II). Biochemistry, 22, 3927-3933.
2. Fichtinger-Schepman,A. M., van der Veer,J.L., den Hartog,J.H., Lohman,P.H. and Reedijk,J. (1985) Adducts of the antitumor drug cis-diamminedichloroplatinum(II) with DNA: Formation, identification, and quantitation. Biochemistry, 24, 707-713.
3. Fichtinger-Schepman,A.M., van Oosterom,A.T., Lohman,P.H. and Berends,F. (1987) cis-Diamminedichloroplatinum(II)-induced DNA adducts in peripheral leukocytes from seven cancer patients: Quantitative immunochemical detection of the adduct induction and removal after a single dose of cis-diamminedichloroplatinum(II). Cancer Res., 47, 3000-3004.
4. Dijt,F.J., Fichtinger-Schepman,A.M., Berends,F. and Reedijk,J. (1988) Formation and repair of cisplatin-induced adducts to DNA in cultured normal and repair-deficient human fibroblasts. Cancer Res., 48 6058-6062.
5. Villani,G., Hubscher,U. and Butour,J.L. (1988) Sites of termination of in vitro DNA synthesis on cis-diamminedichloroplatinum(II) treated single-stranded DNA: A comparison between E. coli DNA polymerase I and eucaryotic DNA polymerases alpha. Nucleic Acids Res., 16, 4407-4418.
6. Hoffinann,J.S., Pillaire,M.J., Maga,G., Podust,V., Hubscher,U. and Villani,G. (1995) DNA polymerase beta bypasses in vitro a single d(GpG)-cisplatin adduct placed on codon 13 of the HRAS gene. Proc. Natl Acad. Sci. USA, 92, 5356-5360.
7. Huang,L., Turchi,J.J., Wahl,A.F. and Dambara,R.A. (1993) Effects of the anticancer drug cis-diamminedichloroplatinum(II) on the activities of calf thymus DNA polymerase epsilon. Biochemistry, 32, 841-848.
8. Vaisman,A., Masutani,C., Hanaoka,F. and Chaney,S.G. (2000) Efficient translesion replication past oxaliplatin and cisplatin GpG adducts by human DNA polymerase eta. Biochemistry, 39, 4575-4580.
9. Masutani,C., Kusumato,R., Iwai,S. and Hanaoka,F. (2000) Mechanisms of accurate translesion synthesis by human polymerase eta. EMBO J., 19, 3100-3109.
10. Bassett,E., Vaisman,A., Tropea,K.A., McCall,C.M., Masutani,C., Hanaoka,F. and Chaney,S.G. (2002) Frameshifts and deletions during in vitro translesion synthesis past Pt-DNA adducts by DNA polymerases beta and eta. DNA Repair, 1, 1003-1116.
11. Bassett,E., Vaisman,A., Havener,J.M., Masutani,C., Hanaoka,F. and Chaney,S.G. (2003) Efficiency of extension of mismatched primer termini across from cisplatin and oxaliplatin adducts by human DNA polymerases beta and eta in vitro. Biochemistry, 42, 14197-14206.
12. Yamada,K., Takezawa,J. and Ezaki,O. (2003) Translesion replication in cisplatin-treated xeroderma pigmentosum variant cells is also caffeine-sensitive: Features of the error-prone DNA polymerase(s) involved in UV-mutagenesis. DNA Repair, 2, 909-924.
13. Bassett,E., King,N.M., Bryant,M.F., Hector,S., Pendyala,L., Chaney,S.G. and Cordeiro-Stone,M. (2004) The role of DNA polymerase eta in translesion synthesis past platinum-DNA adducts in human fibroblasts. Cancer Res., 64, 6469-6475.
14. Albertella,M.R., Green,C.M., Lehmann,A.R. and O'Connor,M.J. (2005) A role for polymerase eta in the cellular tolerance to cisplatin-induced damage. Cancer Res., 65, 9799-9806.
15. McDonald,J.P., Tissier,A., Frank,E.G., Iwai,S., Hanaoka,F. and Woodgate,R. (2001) DNA polymerase iota and related rad30-like enzymes. Philos. Trans. R. Soc. Lond. B Biol. Sci., 356, 53-60.
16. Ohashi,E., Ogi,T., Kusumoto,R., Iwai,S., Masutani,C., Hanaoka,F. and Ohmori,H. (2000) Error-prone bypass of certain DNA lesions by the human DNA polymerase kappa. Genes Dev., 14, 1599-1594.
17. Gerlach,V.L., Feaver,W.J., Fischhaber,P.L. and Friedberg,E.C. (2001) Purification and characterization of pol kappa, a DNA polymerase encoded by the human DINBI gene. J. Biol. Chem., 276, 92-98.
18. Gao,D., Wu,X., Rajpal,D. K., Taylor,J.S. and Wang,Z. (2001) Translesion synthesis by yeast DNA polymerase zeta from templates containing lesions of ultraviolet radiation and acetylaminofluorene. Nucleic Acids Res. 29, 2875-2883.
19. Johnson,R.E., Washington,M.T., Haracska,L., Prakash,S. and Prakash,L. (2000) Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions. Nature, 406, 1015-1019.
20. Okuda,T., Lin,X., Trang,J. and Howell,S.B. (2005) Suppression of hREV1 expression reduces the rate at which human ovarian carcinoma cells acquire resistance to cisplatin. Mol. Pharmacol., 67, 1852-1860.
21. Lin,X, Okuda,T., Trang,J. and Howell,S.B. (2006) Human REV1 modulates the cytotoxicity and mutagenicity of cisplatin in human ovarian carcinoma cells. Mol. Pharmacol., 69, 1748-1754.
22. Ross,A.L., Simpson,L.J. and Sale,J.E. (2005) Vertebrate DNA damage tolerance requires the C-terminus but not BRCT or transferase domains of REV1. Nucleic Acids Res., 33, 1280-1289.
23. Vaisman,A., Lim,S.E., Patrick,S.M., Copeland,W.C., Hinkle,D.C., Turchi,J.J. and Chaney,S.G. (1999) Effect of DNA polymerases and high mobility group protein 1 on the carrier ligand specificity for translesion synthesis past platinum-DNA adducts. Biochemistry, 38, 11026-11039.
24. Wu,F., Lin,X., Okuda,T. and Howell,S.B. (2004) DNA polymerase zeta regulates cisplatin cytotoxicity, mutagenicity, and the rate of development of cisplatin resistance. Cancer Res., 64, 8029-8035.
25. Lin,X., Trang,J., Okuda,T. and Howell,S.B. (2006) DNA polymerase zeta accounts for the reduced cytotoxicity and enhanced mutagenicity of cisplatin in human colon carcinoma cells that have lost DNA mismatch repair. Clin. Cancer Res., 12, 563-568.
26. Hoffmann,J.S., Pillaire,M.J., Garcia-Estefania,D., Lapalu,S. and Villani,G. (1996) In vitro bypass replication of the cisplatin-d(GpG) lesion by calf thymus DNA polymerase beta and human immunodeficiency virus type I reverse transcriptase is highly mutagenic. J. Biol. Chem., 271, 15386-92.
27. Vaisman,A. and Chaney,S.G. (2000) The efficiency and fidelity of translesion synthesis past cisplatin and oxaliplatin GpG adducts by human DNA polymerase beta. J. Biol. Chem., 275, 13017-13025.
28. Vaisman,A., Warren,M.W. and Chaney,S.G. (2001) The effect of DNA structure on the catalytic efficiency and fidelity of human DNA polymerase beta on templates with platinum-DNA adducts. J. Biol. Chem., 276, 18999-19005.
29. Havener,J.M., McElhinny,S.A., Bassett,E., Gauger,M., Ramsden,D.A. and Chaney,S.G. (2003) Translesion synthesis past platinum DNA adducts by human DNA polymerase mu. Biochemistry, 42, 1777-1788.
30. Siddik,Z.H. (2003) Cisplatin: Mode of cytotoxic action and molecular basis of resistance. Oncogene, 22, 7265-7279.
31. Bouhkas,T. and Vougiouka,M. (2003) Cisplatin and platinum drugs at the molecular level. (Review). Oncol. Rep., 10, 1663-1682.
32. Chaney,S.G., Campbell,S.L., Bassett,E. and Wu,Y. (2005) Recognition and processing of cisplatin- and oxaliplatin-DNA adducts. Crit. Rev. Oncol. Hematol., 53, 3-11.
33. Wang,D. and Lippard,S.J. (2005) Cellular processing of platinum anticancer drugs. Nat. Rev. Drug Discov., 4, 307-320.
34. Rabik,C.A. and Dolan,M.E. (2007) Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat Rev., 33, 9-23.
35. Fiala,K.A. and Suo,Z. (2004) Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry, 43, 2116-2125.
36. Fiala,K.A. and Suo,Z. (2004) Pre-steady-state kinetic studies of the fidelity of Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry, 43, 2106-2115.
37. Fiala,K.A., Hypes,C.D. and Suo,Z. (2007) Mechanism of abasic lesion bypass catalyzed by a Y-family DNA polymerase. J. Biol. Chem., 282, 8188-8198.
38. Reed,E., Ozols,R.F., Tarone,R., Yuspa,S.H. and Poirier,M.C. (1987) Platinum-DNA adducts in leukocyte DNA correlate with disease response in ovarian cancer patients receiving platinum-based chemotherapy. Proc. Natl Acad. Sci. USA, 849 5024-5028.
39. Reed,E., Ozols,R.F., Tarone,R., Yuspa,S.H. and Poirier,M.C. (1988) The measurement of cisplatin-DNA adduct levels in testicular cancer patients. Carcinogenesis, 9, 1909-1911.
40. Boudsocq,F., Iwai,S., Hanaoka,F. and Woodgate,R. (2001) Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): An archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic poleta. Nucleic Acids Res., 29, 4607-4616.
41. Suo,Z., Lippard,S.J. and Johnson,K.A. (1999) Single d(GpG)/ cis-diammineplatinum(II) adduct-induced inhibition of DNA polymerization. Biochemistry, 38, 715-726.
42. Fiala,K.A., Brown,J.A., Ling,H., Kshetry,A.K., Zhang,J., Taylor,J.S., Yang,W. and Suo,Z. (2007) Mechanism of template-independent nucleotide incorporation catalyzed by a template-dependent DNA polymerase. J. Mol. Biol., 365, 590-602.
43. de Boer,J.G. and Glickman,B.W. (1989) Sequence specificity of mutation induced by the anti-tumor drug cisplatin in the CHO aprt gene. Carcinogenesis, 10, 1363-1367.
44. Mis,JR. and Kunz,B.A. (1990) Analysis of mutations induced in the SUP4-o gene of Saccharomyces cerevisiae by cis-diammine dichloroplatinum(II). Carcinogenesis, 11, 633-638.
45. Cariello,N.F., Swenberg,J.A. and Skopek,T.R. (1992) In vitro mutational specificity of cisplatin in the human hypoxanthine guanine phosphoribosyltransferase gene. Cancer Res., 52, 2866-2873.
46. Pillaire,M.J., Margot,A., Villani,G., Sarasin,A., Defais,M. and Gentil,A. (1994) Mutagenesis in monkey cells of a vector containing a single d(GPG) cis-diamminedichloroplatinum(II) adduct placed on codon 13 of the human H-ras proto-oncogene. Nucleic Acids Res., 22, 2519-2524.
47. Louro,H., Silva,M.J. and Boavida,M.G. (2002) Mutagenic activity of cisplatin in the lacZ plasmid-based transgenic mouse model. Environ. Mol. Mutagen., 40, 283-291.
48. Takahara,P.M., Rosenzweig,A.C., Frederick,C.A. and Lippard,S.J. (1995) Crystal structure of double-stranded DNA containing the major adduct of the anticancer drug cisplatin. Nature, 377, 649-652.
49. Takahara,P.M., Frederick,C.A. and Lippard,S.J. (1996) Crystal structure of the anticancer drug cisplatin bound to duplex DNA. J. Am. Chem. Soc., 118, 12309-12321.
50. Gelasco,A. and Lippard,S.J. (1998) NMR solution structure of a DNA dodecamer duplex containing a cis-diammineplatinum(II) d(GpG) intrastrand cross-link, the major adduct of the anticancer drug cisplatin. Biochemistry, 37, 9230-9239.
51. Comess,K.M., Burstyn,J.N., Essigmann,J.M. and Lippard,S.J. (1992) Replication inhibition and translesion synthesis on templates containing site-specifically placed cis-diamminedichloroplatinum(II) DNA adducts. Biochemistry, 31, 3975-3990.
52. Mamenta,E.L., Poma,E.E., Kaufmann,W.K., Delmastro,D.A., Grady,H.L. and Chaney,S.G. (1994) Enhanced replicative bypass of platinum-DNA adducts in cisplatin-resistant human ovarian carcinoma cell lines. Cancer Res., 54, 3500-3505.
53. Canitrot,Y., Cazaux,C., Frechet,M., Bouayadi,K., Lesca,C., Salles,B. and Hoffmann,J.S. (1998) Overexpression of DNA polymerase beta in cell results in a mutator phenotype and a decreased sensitivity to anticancer drugs. Proc. Natl Acad. Sci. USA, 95, 12596-12590.
54. Alt,A., Lammens,K., Chiocchini,C., Lammens,A., Pieck,J.C., Kuch,D., Hopfner,K.P. and Carell,T. (2007) Bypass of DNA lesions generated during anticancer treatment with cisplatin by DNA polymerase eta. Science 318, 967-970.
55. Yamada,M., O'Regan,E., Brown,R. and Karran,P. (1997) Selective recognition of a cisplatin-DNA adduct by human mismatch repair proteins. Nucleic Acids Res., 25, 491-496.
56. Fourrier,L., Brooks,P. and Malinge,J.M. (2003) Binding discrimination of MutS to a set of lesions and compound lesions (base damage and mismatch) reveals its potential role as a cisplatin-damaged DNA sensing protein. J. Biol. Chem., 278, 21267-21275.
57. Washington,M.T., Prakash,L. and Prakash,S. (2003) Mechanism of nucleotide incorporation opposite a thymine-thymine dimer by yeast DNA polymerase eta. Proc. Natl Acad. Sci. USA, 100, 12093-12098.
58. Park,H., Zhang,K., Ren,Y., Yikdji,S., Sinha,N., Taylor,J.S. and Kang,C. (2002) Crystal structure of a DNA decamer containing a cis-syn thymine dimer. Proc. Natl Acad. Sci. USA, 99, 15965-15970.
59. Ling,H., Boudsocq,F., Plosky,B.S., Woodgate,R. and Yang,W. (2003) Replication of a cis-syn thymine dimer at atomic resolution. Nature 424, 1083-1087.