Efficient and erroneous incorporation of oxidized DNA precursors by human DNA polymerase η

Biochemistry

Volumn 46, Issue 18, 2007, Pages 5515-5522

  Shimizu, Masatomi ^a,e   Gruz, Petr ^a   Kamiya, Hiroyuki ^b   Masutani, Chikahide ^c   Xu, Yan ^d   Usui, Yukio ^e   Sugiyama, Hiroshi ^d,f   Harashima, Hideyoshi ^b   Hanaoka, Fumio ^c   Nohmi, Takehiko ^a  

^a NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e TOKYO HEALTHCARE UNIVERSITY   (Japan)

^f KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DNA PRECURSORS; THYMINE;

CARCINOGENS; ENZYMES; METABOLISM; MUTAGENESIS; OXIDATION; SYNTHESIS (CHEMICAL); TUMORS;

DNA;

ADENINE; CYTOSINE; DEOXYADENOSINE TRIPHOSPHATE; DEOXYGUANOSINE TRIPHOSPHATE; DNA; DNA DIRECTED DNA POLYMERASE ETA; GUANINE; THYMINE;

ARTICLE; DNA STRAND; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; DEOXYGUANINE NUCLEOTIDES; DNA DAMAGE; DNA-DIRECTED DNA POLYMERASE; HUMANS; MUTAGENESIS; OXIDATION-REDUCTION;

EID: 34248356804     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi062238r     Document Type: Article

References (56)

1. Ames, B. N., and Gold, L. S. (1991) Endogenous mutagens and the causes of aging and cancer, Mutat. Res. 250, 3-16.
2. Henle, E. S., and Linn, S. (1997) Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide, J. Biol. Chem. 272, 19095-19098.
3. Bjelland, S., and Seeberg, E. (2003) Mutagenicity, toxicity and repair of DNA base damage induced by oxidation, Mutat. Res. 531, 37-80.
4. Kamiya, H. (2003) Mutagenic potentials of damaged nucleic acids produced by reactive oxygen/nitrogen species: approaches using synthetic oligonucleotides and nucleotides: survey and summary, Nucleic Acids Res. 31, 517-531.
5. Ames, B. N. (1983) Dietary carcinogens and anticarcinogens. Oxygen radicals and degenerative diseases, Science 221, 1256-1264.
6. Jackson, A. L., and Loeb, L. A. (2001) The contribution of endogenous sources of DNA damage to the multiple mutations in cancer, Mutat. Res. 477, 7-21.
7. Sekiguchi, M., and Tsuzuki, T. (2002) Oxidative nucleotide damage: consequences and prevention, Oncogene 21, 8895-8904.
8. Michaels, M. L., and Miller, J. H. (1992) The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine), J. Bacteriol. 174, 6321-6325.
9. Nakabeppu, Y., Sakumi, K., Sakamoto, K., Tsuchimoto, D., Tsuzuki, T., and Nakatsu, Y. (2006) Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids, Biol. Chem. 387, 373-379.
10. Maki, H., and Sekiguchi, M. (1992) MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis, Nature 355, 273-275.
11. Yanofsky, C., Cox, E. C., and Horn, V. (1966) The unusual mutagenic specificity of an E. coli mutator gene, Proc. Natl. Acad. Sci. U.S.A. 55, 274-281.
12. Kasai, H. (2002) Chemistry-based studies on oxidative DNA damage: formation, repair, and mutagenesis, Free Radical Biol. Med. 33, 450-456.
13. Sakai, A., Nakanishi, M., Yoshiyama, K., and Maki, H. (2006) Impact of reactive oxygen species on spontaneous mutagenesis in Escherichia coli, Genes Cells 11, 767-778.
14. Inoue, M., Kamiya, H., Fujikawa, K., Ootsuyama, Y., Murata-Kamiya, N., Osaki, T., Yasumoto, K., and Kasai, H. (1998) Induction of chromosomal gene mutations in Escherichia coli by direct incorporation of oxidatively damaged nucleotides. New evaluation method for mutagenesis by damaged DNA precursors in vivo, J. Biol. Chem. 273, 11069-11074.
15. Kamiya, H., and Kasai, H. (2000) 2-Hydroxy-dATP is incorporated opposite G by Escherichia coli DNA polymerase III resulting in high mutagenicity, Nucleic Acids Res. 28, 1640-1646.
16. Kamiya, H., Iida, E., Murata-Kamiya, N., Yamamoto, Y., Miki, T., and Harashima, H. (2003) Suppression of spontaneous and hydrogen peroxide-induced mutations by a MutT-type nucleotide pool sanitization enzyme, the Escherichia coli Orf135 protein, Genes Cells 8, 941-950.
17. Kamiya, H., Murata-Kamiya, N., Iida, E., and Harashima, H. (2001) Hydrolysis of oxidized nucleotides by the Escherichia coli Orf135 protein, Biochem. Biophys. Res. Commun. 288, 499-502.
18. Tsuzuki, T., Egashira, A., Igarashi, H., Iwakuma, T., Nakatsuru, Y., Tominaga, Y., Kawate, H., Nakao, K., Nakamura, K., Ide, F., Kura, S., Nakabeppu, Y., Katsuki, M., Ishikawa, T., and Sekiguchi, M. (2001) Spontaneous tumorigenesis in mice defective in the MTH1 gene encoding 8-oxo-dGTPase, Proc. Natl. Acad. Sci. U.S.A. 98, 11456-11461.
19. Fujikawa, K., Kamiya, H., Yakushiji, H., Fujii, Y., Nakabeppu, Y., and Kasai, H. (1999) The oxidized forms of dATP are substrates for the human MutT homologue, the hMTH1 protein, J. Biol. Chem. 274, 18201-18205.
20. Colussi, C., Parlanti, E., Degan, P., Aquilina, G., Barnes, D., Macpherson, P., Karran, P., Crescenzi, M., Dogliotti, E., and Bignami, M. (2002) The mammalian mismatch repair pathway removes DNA 8-oxodGMP incorporated from the oxidized dNTP pool, Curr. Biol. 12, 912-918.
21. Russo, M. T., Blasi, M. F., Chiera, F., Fortini, P., Degan, P., Macpherson, P., Furuichi, M., Nakabeppu, Y., Karran, P., Aquilina, G., and Bignami, M. (2004) The oxidized deoxynucleoside triphosphate pool is a significant contributor to genetic instability in mismatch repair-deficient cells, Mol. Cell Biol. 24, 465-474.
22. Nohmi, T., Kim, S. R., and Yamada, M. (2005) Modulation of oxidative mutagenesis and carcinogenesis by polymorphic forms of human DNA repair enzymes, Mutat. Res. 591, 60-73.
23. Einolf, H. J., and Guengerich, F. P. (2001) Fidelity of nucleotide insertion at 8-oxo-7,8-dihydroguanine by mammalian DNA polymerase δ. Steady-state and pre-steady-state kinetic analysis, J. Biol. Chem. 276, 3764-3771.
24. Einolf, H. J., Schnetz-Boutaud, N., and Guengerich, F. P. (1998) Steady-state and pre-steady-state kinetic analysis of 8-oxo-7,8-dihydroguanosine triphosphate incorporation and extension by replicative and repair DNA polymerases, Biochemistry 37, 13300-13312.
25. Miller, H., Prasad, R., Wilson, S. H., Johnson, F., and Grollman, A. P. (2000) 8-oxodGTP incorporation by DNA polymerase β is modified by active-site residue Asn279, Biochemistry 39, 1029-1033.
26. Kamiya, H., and Kasai, H. (1995) Formation of 2-hydroxydeoxyadenosine triphosphate, an oxidatively damaged nucleotide, and its incorporation by DNA polymerases. Steady-state kinetics of the incorporation, J. Biol. Chem. 270, 19446-19450.
27. Ohmori, H., Friedberg, E. C., Fuchs, R. P., Goodman, M. F., Hanaoka, F., Hinkle, D., Kunkel, T. A., Lawrence, C. W., Livneh, Z., Nohmi, T., Prakash, L., Prakash, S., Todo, T., Walker, G. C., Wang, Z., and Woodgate, R. (2001) The Y-family of DNA polymerases, Mol. Cell 8, 7-8.
28. Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K., and Hanaoka, F. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η, Nature 399, 700-704.
29. Johnson, R. E., Prakash, S., and Prakash, L. (1999) Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Polη, Science 283, 1001-1004.
30. Prakash, S., Johnson, R. E., and Prakash, L. (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function, Annu. Rev. Biochem. 74, 317-353.
31. Friedberg, E. C. (2005) Suffering in silence: the tolerance of DNA damage, Nat. Rev. Mol. Cell Biol. 6, 943-953.
32. Nohmi, T. (2006) Environmental Stress and Lesion-Bypass DNA Polymerases, Annu. Rev. Microbiol. 60, 231-253.
33. Shimizu, M., Gruz, P., Kamiya, H., Kim, S. R., Pisani, F. M., Masutani, C., Kanke, Y., Harashima, H., Hanaoka, F., and Nohmi, T. (2003) Erroneous incorporation of oxidized DNA precursors by Y-family DNA polymerases, EMBO Rep. 4, 269-273.
34. Yamada, M., Nunoshiba, T., Shimizu, M., Gruz, P., Kamiya, H., Harashima, H., and Nohmi, T. (2006) Involvement of Y-family DNA polymerases in mutagenesis caused by oxidized nucleotides in Escherichia coli, J. Bacteriol. 188, 4992-4995.
35. Satou, K., Yamada, M., Nohmi, T., Harashima, H., and Kamiya, H. (2005) Mutagenesis induced by oxidized DNA precursors: roles of Y family DNA polymerases in Escherichia coli, Chem. Res. Toxicol. 18, 1271-1278.
36. Kannouche, P., Broughton, B. C., Volker, M., Hanaoka, F., Mullenders, L. H., and Lehmann, A. R. (2001) Domain structure, localization, and function of DNA polymerase η, defective in xeroderma pigmentosum variant cells, Genes Dev. 15, 158-172.
37. Tissier, A., Kannouche, P., Reck, M. P., Lehmann, A. R., Fuchs, R. P., and Cordonnier, A. (2004) Co-localization in replication foci and interaction of human Y-family members, DNA polymerase polη and REV1 protein, DNA Repair (Amsterdam) 3, 1503-1514.
38. McIlwraith, M. J., Vaisman, A., Liu, Y., Fanning, E., Woodgate, R., and West, S. C. (2005) Human DNA polymerase η promotes DNA synthesis from strand invasion intermediates of homologous recombination, Mol. Cell 20, 783-792.
39. Kawamoto, T., Araki, K., Sonoda, E., Yamashita, Y. M., Harada, K., Kikuchi, K., Masutani, C., Hanaoka, F., Nozaki, K., Hashimoto, N., and Takeda, S. (2005) Dual roles for DNA polymerase η in homologous DNA recombination and translesion DNA synthesis, Mol. Cell 20, 793-799.
40. Mayorov, V. I., Rogozin, I. B., Adkison, L. R., and Gearhart, P. J. (2005) DNA polymerase η contributes to strand bias of mutations of A versus T in immunoglobulin genes, J. Immunol. 174, 7781-7786.
41. Masutani, C., Kusumoto, R., Iwai, S., and Hanaoka, F. (2000) Mechanisms of accurate translesion synthesis by human DNA polymerase η, EMBO J. 19, 3100-3109.
42. Tissier, A., McDonald, J. P., Frank, E. G., and Woodgate, R. (2000) polι, a remarkably error-prone human DNA polymerase, Genes Dev. 14, 1642-1650.
43. Cheng, K. C., Cahill, D. S., Kasai, H., Nishimura, S., and Loeb, L. A. (1992) 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G - T and A - C substitutions, J. Biol. Chem. 267, 166-172.
44. Vaisman, A., Frank, E. G., Iwai, S., Ohashi, E., Ohmori, H., Hanaoka, F., and Woodgate, R. (2003) Sequence context-dependent replication of DNA templates containing UV-induced lesions by human DNA polymerase ι, DNA Repair (Amsterdam) 2, 991-1006.
45. Creighton, S., Bloom, L. B., and Goodman, M. F. (1995) Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading, and lesion bypass efficiencies, Methods Enzymol. 262, 232-256.
46. Goodman, M. F., Creighton, S., Bloom, L. B., and Petruska, J. (1993) Biochemical basis of DNA replication fidelity, Crit. Rev. Biochem. Mol. Biol. 28, 83-126.
47. Slupphaug, G., Kavli, B., and Krokan, H. E. (2003) The interacting pathways for prevention and repair of oxidative DNA damage, Mutat. Res. 531, 231-251.
48. Pavlov, Y. I., Minnick, D. T., Izuta, S., and Kunkel, T. A. (1994) DNA replication fidelity with 8-oxodeoxyguanosine triphosphate, Biochemistry 33, 4695-4701.
49. Satou, K., Harashima, H., and Kamiya, H. (2003) Mutagenic effects of 2-hydroxy-dATP on replication in a HeLa extract: induction of substitution and deletion mutations, Nucleic Acids Res. 31, 2570-2575.
50. Lehmann, A. R. (2006) New functions for Y family polymerases, Mol. Cell 24, 493-495.
51. Godoy, V. G., Jarosz, D. F., Walker, F. L., Simmons, L. A., and Walker, G. C. (2006) Y-family DNA polymerases respond to DNA damage-independent inhibition of replication fork progression, EMBO J. 25, 868-879.
52. Nair, D. T., Johnson, R. E., Prakash, S., Prakash, L., and Aggarwal, A. K. (2004) Replication by human DNA polymerase-iota occurs by Hoogsteen base-pairing, Nature 430, 377-380.
53. Wolfle, W. T., Johnson, R. E., Minko, I. G., Lloyd, R. S., Prakash, S., and Prakash, L. (2005) Human DNA polymerase ι promotes replication through a ring-closed minor-groove adduct that adopts a syn conformation in DNA, Mol. Cell Biol. 25, 8748-8754.
54. Kouchakdjian, M., Bodepudi, V., Shibutani, S., Eisenberg, M., Johnson, F., Grollman, A. P., and Patel, D. J. (1991) NMR structural studies of the ionizing radiation adduct 7-hydro-8-oxodeoxyguanosine (8-oxo-7H-dG) opposite deoxyadenosine in a DNA duplex. 8-Oxo-7H-dG(syn).dA(anti) alignment at lesion site, Biochemistry 30, 1403-1412.
55. Haracska, L., Yu, S. L., Johnson, R. E., Prakash, L., and Prakash, S. (2000) Efficient and accurate replication in the presence of 7,8-dihydro-8-oxoguanine by DNA polymerase η, Nat. Genet. 25, 458-461.
56. Carlson, K. D., and Washington, M. T. (2005) Mechanism of efficient and accurate nucleotide incorporation opposite 7,8-dihydro-8-oxoguanine by Saccharomyces cerevisiae DNA polymerase η, Mol. Cell Biol. 25, 2169-2176.