Escherichia coli DNA polymerase III is responsible for the high level of spontaneous mutations in mutT strains

Molecular Microbiology

Volumn 86, Issue 6, 2012, Pages 1364-1375

  Yamada, Masami ^a   Shimizu, Masatomi ^a,b   Katafuchi, Atsushi ^a   Grúz, Petr ^a   Fujii, Shingo ^c   Usui, Yukio ^b   Fuchs, Robert P ^c   Nohmi, Takehiko ^a  

^a NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^b TOKYO HEALTHCARE UNIVERSITY   (Japan)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

8 OXO DEOXYGUANOSINE TRIPHOSPHATE; DEOXYGUANOSINE TRIPHOSPHATE; DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE IV; DNA POLYMERASE V; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE DELETION; GENE MUTATION; MUTT GENE; NONHUMAN; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL;

DEOXYGUANINE NUCLEOTIDES; DNA POLYMERASE III; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTATION; MUTATION RATE; PYROPHOSPHATASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

EID: 84871023589     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12061     Document Type: Article

References (61)

1. Akiyama, M., Maki, H., Sekiguchi, M., and Horiuchi, T. (1989) A specific role of MutT protein: to prevent dG.dA mispairing in DNA replication. Proc Natl Acad Sci USA 86: 3949-3952.
2. Ames, B.N. (1983) Dietary carcinogens and anticarcinogens. Oxygen radicals and degenerative diseases. Science 221: 1256-1264.
3. Ames, B.N., and Gold, L.S. (1991) Endogenous mutagens and the causes of aging and cancer. Mutat Res 250: 3-16.
4. Bailey, S., Wing, R.A., and Steitz, T.A. (2006) The structure of T.aquaticus DNA polymerase III is distinct from eukaryotic replicative DNA polymerases. Cell 126: 893-904.
5. Beese, L.S., Derbyshire, V., and Steitz, T.A. (1993) Structure of DNA polymerase I Klenow fragment bound to duplex DNA. Science 260: 352-355.
6. Bessman, M.J., Frick, D.N., and O'Handley, S.F. (1996) The MutT proteins or 'Nudix' hydrolases, a family of versatile, widely distributed, 'housecleaning' enzymes. J Biol Chem 271: 25059-25062.
7. Bjelland, S., and Seeberg, E. (2003) Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat Res 531: 37-80.
8. Bloom, L.B., Chen, X., Fygenson, D.K., Turner, J., O'Donnell, M., and Goodman, M.F. (1997) Fidelity of Escherichia coli DNA polymerase III holoenzyme. The effects of b, g complex processivity proteins and e proofreading exonuclease on nucleotide misincorporation efficiencies. J Biol Chem 272: 27919-27930.
9. Burnouf, D.Y., Olieric, V., Wagner, J., Fujii, S., Reinbolt, J., Fuchs, R.P., and Dumas, P. (2004) Structural and biochemical analysis of sliding clamp/ligand interactions suggest a competition between replicative and translesion DNA polymerases. J Mol Biol 335: 1187-1197.
10. Cai, J.P., Kakuma, T., Tsuzuki, T., and Sekiguchi, M. (1995) cDNA and genomic sequences for rat 8-oxo-dGTPase that prevents occurrence of spontaneous mutations due to oxidation of guanine nucleotides. Carcinogenesis 16: 2343-2350.
11. Cai, J.P., Ishibashi, T., Takagi, Y., Hayakawa, H., and Sekiguchi, M. (2003) Mouse MTH2 protein which prevents mutations caused by 8-oxoguanine nucleotides. Biochem Biophys Res Commun 305: 1073-1077.
12. Creighton, S., and Goodman, M.F. (1995) Gel kinetic analysis of DNA polymerase fidelity in the presence of proofreading using bacteriophage T4 DNA polymerase. J Biol Chem 270: 4759-4774.
13. Doublie, S., Tabor, S., Long, A.M., Richardson, C.C., and Ellenberger, T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution. Nature 391: 251-258.
14. Echols, H. (1981) SOS functions, cancer and inducible evolution. Cell 25: 1-2.
15. Egashira, A., Yamauchi, K., Yoshiyama, K., Kawate, H., Katsuki, M., Sekiguchi, M., etal. (2002) Mutational specificity of mice defective in the MTH1 and/or the MSH2 genes. DNA Repair (Amst) 1: 881-893.
16. Einolf, H.J., and Guengerich, F.P. (2001) Fidelity of nucleotide insertion at 8-oxo-7, 8-dihydroguanine by mammalian DNA polymerase d. Steady-state and pre-steady-state kinetic analysis. J Biol Chem 276: 3764-3771.
17. 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.
18. Filee, J., Forterre, P., Sen-Lin, T., and Laurent, J. (2002) Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J Mol Evol 54: 763-773.
19. Fowler, R.G., Amutan, M.V., and Isbell, R.J. (1992) The interaction of the Escherichia coli mutD and mutT pathways in the prevention of A:T→C:G transversions. Mutat Res 284: 307-319.
20. Fowler, R.G., Erickson, J.A., and Isbell, R.J. (1994) Activity of the Escherichia coli mutT mutator allele in an anaerobic environment. J Bacteriol 176: 7727-7729.
21. Fowler, R.G., White, S.J., Koyama, C., Moore, S.C., Dunn, R.L., and Schaaper, R.M. (2003) Interactions among the Escherichia coli mutT, mutM, and mutY damage prevention pathways. DNA Repair (Amst) 2: 159-173.
22. Friedberg, E.C., Wagner, R., and Radman, M. (2002) Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science 296: 1627-1630.
23. Fujii, S., and Fuchs, R.P. (2004) Defining the position of the switches between replicative and bypass DNA polymerases. EMBO J 23: 4342-4352.
24. Furuichi, M., Yoshida, M.C., Oda, H., Tajiri, T., Nakabeppu, Y., Tsuzuki, T., and Sekiguchi, M. (1994) Genomic structure and chromosome location of the human mutT homologue gene MTH1 encoding 8-oxo-dGTPase for prevention of A:T to C:G transversion. Genomics 24: 485-490.
25. Hasegawa, K., Yoshiyama, K., and Maki, H. (2008) Spontaneous mutagenesis associated with nucleotide excision repair in Escherichia coli. Genes Cells 13: 459-469.
26. Ishibashi, T., Hayakawa, H., and Sekiguchi, M. (2003) A novel mechanism for preventing mutations caused by oxidation of guanine nucleotides. EMBO Rep 4: 479-483.
27. Ito, J., and Braithwaite, D.K. (1991) Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res 19: 4045-4057.
28. 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.
29. Janion, C., Sikora, A., Nowosielska, A., and Grzesiuk, E. (2003) E.coli BW535, a triple mutant for the DNA repair genes xth, nth, and nfo, chronically induces the SOS response. Environ Mol Mutagen 41: 237-242.
30. Kakuma, T., Nishida, J., Tsuzuki, T., and Sekiguchi, M. (1995) Mouse MTH1 protein with 8-oxo-7, 8-dihydro-2′-deoxyguanosine 5′-triphosphatase activity that prevents transversion mutation. cDNA cloning and tissue distribution. J Biol Chem 270: 25942-25948.
31. 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.
32. Kasai, H. (2002) Chemistry-based studies on oxidative DNA damage: formation, repair, and mutagenesis. Free Radic Biol Med 33: 450-456.
33. Katafuchi, A., and Nohmi, T. (2010) DNA polymerases involved in the incorporation of oxidized nucleotides into DNA: their efficiency and template base preference. Mutat Res 703: 24-31.
34. Kohara, Y., Akiyama, K., and Isono, K. (1987) The physical map of the whole E.coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell 50: 495-508.
35. Lamers, M.H., Georgescu, R.E., Lee, S.G., O'Donnell, M., and Kuriyan, J. (2006) Crystal structure of the catalytic a subunit of E.coli replicative DNA polymerase III. Cell 126: 881-892.
36. Lopez de Saro, F.J., Georgescu, R.E., Goodman, M.F., and O'Donnell, M. (2003) Competitive processivity-clamp usage by DNA polymerases during DNA replication and repair. EMBO J 22: 6408-6418.
37. McHenry, C.S. (1988) DNA polymerase III holoenzyme of Escherichia coli. Annu Rev Biochem 57: 519-550.
38. McHenry, C.S. (2011) DNA replicases from a bacterial perspective. Annu Rev Biochem 80: 403-436.
39. Maga, G., Villani, G., Crespan, E., Wimmer, U., Ferrari, E., Bertocci, B., and Hubscher, U. (2007) 8-oxo-guanine bypass by human DNA polymerases in the presence of auxiliary proteins. Nature 447: 606-608.
40. Maki, H., and Sekiguchi, M. (1992) MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355: 273-275.
41. 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.
42. Miller, H., Prasad, R., Wilson, S.H., Johnson, F., and Grollman, A.P. (2000) 8-oxodGTP incorporation by DNA polymerase b is modified by active-site residue Asn279. Biochemistry 39: 1029-1033.
43. Mo, J.Y., Maki, H., and Sekiguchi, M. (1992) Hydrolytic elimination of a mutagenic nucleotide, 8-oxodGTP, by human 18-kilodalton protein: sanitization of nucleotide pool. Proc Natl Acad Sci USA 89: 11021-11025.
44. 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.
45. Nohmi, T. (2006) Environmental stress and lesion-bypass DNA polymerases. Annu Rev Microbiol 60: 231-253.
46. 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.
47. Nunoshiba, T., Obata, F., Boss, A.C., Oikawa, S., Mori, T., Kawanishi, S., and Yamamoto, K. (1999) Role of iron and superoxide for generation of hydroxyl radical, oxidative DNA lesions, and mutagenesis in Escherichia coli. J Biol Chem 274: 34832-34837.
48. - superoxide dismutases and Fur, a repressor for iron-uptake systems. DNA Repair (Amst) 1: 411-418.
49. 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.
50. Sakumi, K., Furuichi, M., Tsuzuki, T., Kakuma, T., Kawabata, S., Maki, H., and Sekiguchi, M. (1993) Cloning and expression of cDNA for a human enzyme that hydrolyzes 8-oxo-dGTP, a mutagenic substrate for DNA synthesis. J Biol Chem 268: 23524-23530.
51. Salem, A.M., Nakano, T., Takuwa, M., Matoba, N., Tsuboi, T., Terato, H., etal. (2009) Genetic analysis of repair and damage tolerance mechanisms for DNA-protein cross-links in Escherichia coli. J Bacteriol 191: 5657-5668.
52. Sekiguchi, M., and Tsuzuki, T. (2002) Oxidative nucleotide damage: consequences and prevention. Oncogene 21: 8895-8904.
53. Setoyama, D., Ito, R., Takagi, Y., and Sekiguchi, M. (2011) Molecular actions of Escherichia coli MutT for control of spontaneous mutagenesis. Mutat Res 707: 9-14.
54. Shevell, D.E., Abou-Zamzam, A.M., Demple, B., and Walker, G.C. (1988) Construction of an Escherichia coli K-12 ada deletion by gene replacement in a recD strain reveals a second methyltransferase that repairs alkylated DNA. J Bacteriol 170: 3294-3296.
55. Shimizu, M., Gruz, P., Kamiya, H., Masutani, C., Xu, Y., Usui, Y., etal. (2007) Efficient and erroneous incorporation of oxidized DNA precursors by human DNA polymerase η. Biochemistry 46: 5515-5522.
56. Tajiri, T., Maki, H., and Sekiguchi, M. (1995) Functional cooperation of MutT, MutM and MutY proteins in preventing mutations caused by spontaneous oxidation of guanine nucleotide in Escherichia coli. Mutat Res 336: 257-267.
57. Treffers, H.P., Spinelli, V., and Belser, N.O. (1954) A factor (or mutator gene) influencing mutation rates in Escherichia coli. Proc Natl Acad Sci USA 40: 1064-1071.
58. Tsuzuki, T., Egashira, A., Igarashi, H., Iwakuma, T., Nakatsuru, Y., Tominaga, Y., etal. (2001) Spontaneous tumorigenesis in mice defective in the MTH1 gene encoding 8-oxo-dGTPase. Proc Natl Acad Sci USA 98: 11456-11461.
59. Wagner, J., and Nohmi, T. (2000) Escherichia coli DNA polymerase IV mutator activity: genetic requirements and mutational specificity. J Bacteriol 182: 4587-4595.
60. 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.
61. Yanofsky, C., Cox, E.C., and Horn, V. (1966) The unusual mutagenic specificity of an E.coli mutator gene. Proc Natl Acad Sci USA 55: 274-281.