Oxidative damage to nucleotide: Consequences and preventive mechanisms

Oxidative Stress, Disease and Cancer

Volumn , Issue , 2006, Pages 221-252

  Nakatsu, Yoshimichi ^a   Sekiguchi, Mutsuo ^b  

^a KYUSHU UNIVERSITY   (Japan)

^b FUKUOKA DENTAL COLLEGE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84967436535     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1142/9781860948046_0006     Document Type: Chapter

References (93)

1. Ames BN, Gold LS. Endogenous mutagens and the causes of aging and cancer. Mutat. Res. 250: 3-16 (1991).
2. Henle ES, Linn S. Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J. Biol. Chem. 272: 19095-19098 (1997).
3. Gajewski E, Rao G, Nackerdien Z, Dizdaroglu M. Modification of DNA bases in mammalian chromatin by radiation-generated free radicals. Biochemistry 29: 7876-7882 (1990).
4. Demple B, Harrison L. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63: 915-948 (1994).
5. Kasai H, Nishimura S. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res. 12: 2137-2145 (1984).
6. Fraga CG, Shigenaga MK, Park JW, Degan P, Ames BN. Oxidative damage to DNA during aging: 8-hydroxy-2′-deoxyguanosine in rat organ DNA and urine. Proc. Natl. Acad. Sci. USA 87: 4533-4537 (1990).
7. Evans J, Maccabee M, Hatahet Z, Courcelle J, Bockrath R, Ide H, Wallace S. Thymine ring saturation and fragmentation products: lesion bypass, misinsertion and implications for mutagenesis. Mutat. Res. 299: 147-156 (1993).
8. Brooks PJ, Wise DS, Berry DA, Kosmoski JV, Smerdon MJ, Somers RL, Mackie H, Spoonde AY, Ackerman EJ, Coleman K, Tarone RE, Robbins JH. The oxidative DNA lesion 8,5′-(S)-cyclo-2′-deoxyadenosineis repaired by the nucleotide excision repair pathway and blocks gene expression in mammalian cells. J. Biol. Chem. 275: 22355-22362 (2000).
9. Kuraoka I, Bender C, Romieu A, Cadet J, Wood RD, Lindahl T. Removal of oxygen free-radical-induced 5′,8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc. Natl. Acad. Sci. USA 97: 3832-3837 (2000).
10. Shibutani S, Takeshita M, Grollman AP. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349: 431-434 (1991).
11. Smith KC. Spontaneous mutagenesis: experimental, genetic and other factors. Mutat. Res. 277: 139-162 (1992).
12. Cabrera M, Nghiem Y, Miller JH. mutM, a secondmutator locus in Escherichia coli that generates G.C→T. A transversions. J. Bacteriol. 170: 5405-5407 (1988).
13. Chung MH, Kasai H, Jones DS, Inoue H, Ishikawa H, Ohtsuka E, Nishimura S. An endonuclease activity of Escherichia coli that specifically removes 8- hydroxyguanine residues from DNA. Mutat. Res. 254: 1-12 (1991).
14. Michaels ML, Pham L, Cruz C, Miller JH. Mut M, a protein that prevents G.C→T. A transversions, is formamidopyrimidine-DNA glycosylase. Nucleic Acids Res. 19: 3629-3632 (1991).
15. Bessho T, Tano K, Kasai H, Nishimura S. Deficiency of 8-hydroxyguanine DNA endonuclease activity and accumulation of the 8-hydroxyguanine in mutatormutant (mutM) of Escherichia coli. Biochem. Biophys. Res. Commun. 188: 372-378 (1992).
16. Au KG, Cabrera M, Miller JH, Modrich P. Escherichia coli mutY gene product is required for specific A-G→CG mismatch correction. Proc. Natl. Acad. Sci. USA 85: 9163-9166 (1988).
17. Nghiem Y, Cabrera M, Cupples CG, Miller JH. The mutY gene: a mutator locus in Escherichia coli that generates G.C→T. A transversions. Proc. Natl. Acad. Sci. USA 85: 2709-2713 (1988).
18. Au KG, Clark S, Miller JH, Modrich P. Escherichia coli mutY gene encodes an adenine glycosylase active on G-A mispairs. Proc. Natl. Acad. Sci. USA 86: 8877-8881 (1989).
19. Michaels ML, Tchou J, Grollman AP, Miller JH. A repair system for 8-oxo-7,8-dihydrodeoxyguanine. Biochemistry 31: 10964-10968 (1992).
20. Tchou J, Grollman AP. Repair of DNA containing the oxidatively-damaged base, 8-oxoguanine. Mutat. Res. 299: 277-287 (1993).
21. Slupska MM, Baikalov C, Luther WM, Chiang JH, Wei YF, Miller JH. Cloning and sequencing a human homolog (hMYH) of the Escherichia coli mutY gene whose function is required for the repair of oxidative DNA damage. J. Bacteriol. 178: 3885-3892 (1996).
22. Hirano S, Tominaga Y, Ichinoe A, Ushijima Y, Tsuchimoto D, Honda-Ohnishi Y, Ohtsubo T, Sakumi K, Nakabeppu Y. Mutator phenotype of MUTYH-nullmouse embryonic stem cells. J. Biol. Chem. 278: 38121-38124 (2003).
23. Klungland A, Rosewell I, Hollenbach S, Larsen E, Daly G, Epe B, Seeberg E, Lindahl T, Barnes DE. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. USA 96: 13300-13305 (1999).
24. Minowa O, Arai T, Hirano M, Monden Y, Nakai S, Fukuda M, Itoh M, Takano H, Hippou Y, Aburatani H, Masumura K, Nohmi T, Nishimura S, Noda T. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc. Natl. Acad. Sci. USA 97: 4156-4161 (2000).
25. Sakumi K, Tominaga Y, Furuichi M, Xu P, Tsuzuki T, Sekiguchi M, Nakabeppu Y. Ogg1 knockout-associated lung tumorigenesis and its suppression by Mth1 gene disruption. Cancer Res. 63: 902-905 (2003).
26. Maki H, Sekiguchi M. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355: 273-275 (1992).
27. Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G→T and A→C substitutions. J. Biol. Chem. 267: 166-172 (1992).
28. Mo JY, Maki H, Sekiguchi M. Mutational specificity of the dnaE173 mutator associated with a defect in the catalytic subunit of DNA polymerase III of Escherichia coli. J. Mol. Biol. 222: 925-936 (1991).
29. Schaaper RM, Danforth BN, Glickman BW. Mechanisms of spontaneous mutagenesis: an analysis of the spectrum of spontaneous mutation in the Escherichia coli lacI gene. J. Mol. Biol. 189: 273-284 (1986).
30. Mo JY, Maki H, Sekiguchi M. Hydrolytic elimination of a mutagenic nucleotide, 8-oxod GTP, by human 18-kilodalton protein: sanitization of nucleotide pool. Proc. Natl. Acad. Sci. USA 89: 11021-11025 (1992).
31. Sakumi K, Furuichi M, Tsuzuki T, Kakuma T, Kawabata S, Maki H, Sekiguchi M. Cloning and expression of cDNA for a human enzyme that hydrolyzes 8-oxo-d GTP, a mutagenic substrate for DNA synthesis. J. Biol. Chem. 268: 23524-23530 (1993).
32. Furuichi M, Yoshida MC, Oda H, Tajiri T, Nakabeppu Y, Tsuzuki T, Sekiguchi M. 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 (1994).
33. 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, Sekiguchi M. Spontaneous tumorigenesis in mice defective in the MTH1 gene encoding 8-oxo-dGTPase. Proc. Natl. Acad. Sci. USA 98: 11456-11461 (2001).
34. Yanofsky C, Cox EC, Horn V. The unusual mutagenic specificity of an E. coli mutator gene. Proc. Natl. Acad. Sci. USA 55: 274-281 (1966).
35. Akiyama M, Maki H, Sekiguchi M. Horiuchi T. A specific role of MutT protein: to prevent dG.dA mispairing in DNA replication. Proc. Natl. Acad. Sci. USA 86: 3949-3952 (1989).
36. Tajiri T, Maki H, Sekiguchi M. Functional cooperation of Mut T, MutM and MutY proteins in preventing mutations caused by spontaneous oxidation of guanine nucleotide in Escherichia coli. Mutat. Res. 336: 257-267 (1995).
37. Ishibashi T, Hayakawa H, Sekiguchi M. A novel mechanism for preventing mutations caused by oxidation of guanine nucleotides. EMBO Rep. 4: 479-483 (2003).
38. Dizdaroglu M, Jaruga P, Birincioglu M, Rodriguez H. Free radical-induced damage to DNA: mechanisms and measurement. Free Radic. Biol. Med. 32: 1102-1115 (2002).
39. Purmal AA, Kow YW, Wallace SS. 5-Hydroxypyrimidine deoxynucleoside triphosphates are more efficiently incorporated into DNA by exonuclease-free Klenow fragment than 8-oxopurine deoxynucleoside triphosphates. Nucleic Acids Res. 22: 3930-3935 (1994).
40. Einolf HJ, Schnetz-Boutaud N, Guengerich FP. Steady-state and pre-steadystate kinetic analysis of 8-oxo-7,8-dihydroguanosine triphosphate incorporation and extension by replicative and repair DNA polymerases. Biochemistry 37: 13300-13312 (1998).
41. Kamiya H, Kasai H. 2-Hydroxy-dATP is incorporated opposite G by Escherichia coli DNA polymerase III resulting in high mutagenicity. Nucleic Acids Res. 28: 1640-1646 (2000).
42. Pavlov YI, Minnick DT, Izuta S, Kunkel TA. DNA replication fidelity with 8-oxodeoxyguanosine triphosphate. Biochemistry 33: 4695-4701 (1994).
43. Inoue M, Kamiya H, Fujikawa K, Ootsuyama Y, Murata-Kamiya N, Osaki T, Yasumoto K, Kasai H. Induction of chromosomal gene mutations in Escherichia coli by direct incorporation of oxidatively damaged nucleotides. New evaluationmethod for mutagenesis by damaged DNA precursors in vivo. J. Biol. Chem. 273: 11069-11074 (1998).
44. Kamiya H, Kasai H. 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 (1995).
45. Fujikawa K, Kamiya H, Kasai H. The mutations induced by oxidatively damaged nucleotides, 5-formyl-dUTP and 5-hydroxy-d CTP, in Escherichia coli. Nucleic Acids Res. 26: 4582-4587 (1998).
46. Purmal AA, Bond JP, Lyons BA, Kow YW, Wallace SS. Uracil glycol deoxynucleoside triphosphate is a better substrate for DNA polymerase I Klenow fragment than thymine glycol deoxynucleoside triphosphate. Biochemistry 37: 330-338 (1998).
47. Kamiya H, Maki H, Kasai H. Two DNA polymerases of Escherichia coli display distinct misinsertion specificities for 2-hydroxy-dATP during DNA synthesis. Biochemistry 39: 9508-9513 (2000).
48. Kamiya H, Murata-Kamiya N, Karino N, Ueno Y, Matsuda A, Kasai H. Induction of T→G and T→A transversions by 5-formyluracil in mammalian cells. Mutat. Res. 513: 213-222 (2002).
49. Treffers HP, Spinelli V, Belser NO. A factor (or mutator gene) influencing mutation rates in E. coli. Proc. Natl. Acad. Sci. USA 40: 1064-1071 (1954).
50. Cox EC, Yanofsky C. Altered base ratios in the DNA of an Escherichia coli mutator strain. Proc. Natl. Acad. Sci. USA 58: 1895-1902 (1967).
51. Akiyama M, Horiuchi T, Sekiguchi M. Molecular cloning and nucleotide sequence of the mutT mutator of Escherichia coli that causes A:T to C:G transversion. Mol. Gen. Genet. 206: 9-16 (1987).
52. Bhatnagar SK, Bessman MJ. Studies on the mutator gene, mutT of Escherichia coli. Molecular cloning of the gene, purification of the gene product, and identification of a novel nucleoside triphosphatase. J. Biol. Chem. 263: 8953-8957 (1988).
53. Michaels ML, Cruz C, Grollman AP, Miller JH. Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc. Natl. Acad. Sci. USA 89: 7022-7025 (1992).
54. Taddei F, Hayakawa H, Bouton M, Cirinesi A, Matic I, Sekiguchi M, Radman M. Counteraction by MutT protein of transcriptional errors caused by oxidative damage. Science 278: 128-130 (1997).
55. Hayakawa H, Kuwano M, Sekiguchi M. Specific binding of 8-oxoguaninecontaining RNA to polynucleotide phosphorylase protein. Biochemistry 40: 9977-9982 (2001).
56. Cai JP, Kakuma T, Tsuzuki T, Sekiguchi M. 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 (1995).
57. Kakuma T, Nishida J, Tsuzuki T, Sekiguchi M. Mouse MTH1 protein with 8-oxo-7,8-dihydro-2′-deoxyguanosine5′-triphosphatase activity that prevents transversion mutation, cDNA cloning and tissue distribution. J. Biol. Chem. 270: 25942-25948 (1995).
58. Colussi C, Parlanti E, Degan P, Aquilina G, Barnes D, Macpherson P, Karran P, Crescenzi M, Dogliotti E, Bignami M. The mammalian mismatch repair pathway removes DNA 8-oxodGMP incorporated from the oxidized dNTP pool. Curr. Biol. 12: 912-918 (2002).
59. Yoshimura D, Sakumi K, Ohno M, Sakai Y, Furuichi M, Iwai S, Nakabeppu Y. An oxidized purine nucleoside triphosphatase, MTH1, suppresses cell death caused by oxidative stress. J. Biol. Chem. 278: 37965-37973 (2003).
60. Russo MT, Blasi MF, Chiera F, Fortini P, Degan P, Macpherson P, Furuichi M, Nakabeppu Y, Karran P, Aquilina G, Bignami M. The oxidized deoxynucleoside triphosphate pool is a significant contributor to genetic instability in mismatch repair-deficient cells. Mol. Cell Biol. 24: 465-474 (2004).
61. Kamath AV, Yanofsky C. Sequence and characterization of mutT from Proteus vulgaris. Gene 134: 99-102 (1993).
62. Bullions LC, Mejean V, Claverys JP, Bessman MJ. Purification of the MutX protein of Streptococcus pneumoniae, a homologue of Escherichia coli MutT. Identification of a novel catalytic domain for nucleoside triphosphate pyrophosphohydrolase activity. J. Biol. Chem. 269: 12339-12344 (1994).
63. Bessman MJ, Frick DN, O’Handley SF. The MutT proteins or “Nudix” hydrolases, a family of versatile, widely distributed, “housecleaning” enzymes. J. Biol. Chem. 271: 25059-25062 (1996).
64. O’Handley SF, Frick DN, Bullions LC, Mildvan AS, Bessman MJ. Escherichia coli orf17 codes for a nucleoside triphosphate pyrophosphohydrolasemember of the MutT family of proteins. Cloning, purification, and characterization of the enzyme. J. Biol. Chem. 271: 24649-24654 (1996).
65. O’Handley SF, Frick DN, Dunn CA, Bessman MJ. Orf186 represents a new member of the Nudix hydrolases, active on adenosine(5′)triphospho(5′)adenosine, ADP-ribose, and NADH. J. Biol. Chem. 273: 3192-3197 (1998).
66. Sheikh S, O’Handley SF, Dunn CA, Bessman MJ. Identification and characterization of the Nudix hydrolase from the Archaeon, Methanococcus jannaschii, as a highly specific ADP-ribose pyrophosphatase. J. Biol. Chem. 273: 20924-20928 (1998).
67. Safrany ST, Caffrey JJ, Yang X, Bembenek ME, Moyer MB, Burkhart WA, Shears SB. Anovel context for the ‘MutT’ module, a guardian of cell integrity, in a diphosphoinositol polyphosphate phosphohydrolase. EMBO J. 17: 6599-6607 (1998).
68. Fujii Y, Shimokawa H, Sekiguchi M, Nakabeppu Y. Functional significance of the conserved residues for the 23-residue module among MTH1 and MutT family proteins. J. Biol. Chem. 274: 38251-38259 (1999).
69. Abeygunawardana C, Weber DJ, Frick DN, Bessman MJ, Mildvan AS. Sequence-specific assignments of the backbone 1H, 13C, and 15N resonances of the MutT enzyme by heteronuclear multidimensional NMR. Biochemistry 32: 13071-13080 (1993).
70. Weber DJ, Abeygunawardana C, Bessman MJ, Mildvan AS. Secondary structure of the MutT enzyme as determined by NMR. Biochemistry 32: 13081-13088 (1993).
71. Abeygunawardana C, Weber DJ, Gittis AG, Frick DN, Lin J, Miller AF, Bessman MJ, Mildvan AS. Solution structure of the MutT enzyme, a nucleoside triphosphate pyrophosphohydrolase. Biochemistry 34: 14997-15005 (1995).
72. Frick DN, Weber DJ, Abeygunawardana C, Gittis AG, Bessman MJ, Mildvan AS. NMR studies of the conformations and location of nucleotides bound to the Escherichia coli MutT enzyme. Biochemistry 34: 5577-5586 (1995).
73. Mishima M, Sakai Y, Itoh N, Kamiya H, Furuichi M, Takahashi M, Yamagata Y, Iwai S, Nakabeppu Y, Shirakawa M. Structure of human MTH1, a Nudix family hydrolase that selectively degrades oxidized purine nucleoside triphosphates. J. Biol. Chem. 279: 33806-33815 (2004).
74. Sakai Y, Furuichi M, Takahashi M, Mishima M, Iwai S, Shirakawa M, Nakabeppu Y. A molecular basis for the selective recognition of 2-hydroxydATP and 8-oxo-dGTP by human MTH1. J. Biol. Chem. 277: 8579-8587 (2002).
75. 2+ complex and mechanismof its pyrophosphohydrolase action. Biochemistry 36: 1199-1211 (1997).
76. Fujikawa K, Kamiya H, Yakushiji H, Fujii Y, Nakabeppu Y, Kasai H. The oxidized forms of dATP are substrates for the human MutT homologue, the hMTH1 protein. J. Biol. Chem. 274: 18201-18205 (1999).
77. Fujikawa K, Kamiya H, Yakushiji H, Nakabeppu Y, Kasai H. Human MTH1 protein hydrolyzes the oxidized ribonucleotide, 2-hydroxy-ATP. Nucleic Acids Res. 29: 449-454 (2001).
78. Igarashi H, Tsuzuki T, Kakuma T, Tominaga Y, Sekiguchi M. Organization and expression of the mouse MTH1 gene for preventing transversionmutation. J. Biol. Chem. 272: 3766-3772 (1997).
79. Egashira A, Yamauchi K, Yoshiyama K, Kawate H, Katsuki M, Sekiguchi M, Sugimachi K, Maki H, Tsuzuki T. Mutational specificity of mice defective in the MTH1 and/or the MSH2 genes. DNA Repair (Amst.) 1: 881-893 (2002).
80. Hayashi H, Tominaga Y, Hirano S, McKenna AE, Nakabeppu Y, Matsumoto Y. Replication-associated repair of adenine: 8-oxoguanine mispairs by MYH. Curr. Biol. 12: 335-339 (2002).
81. Kang D, Nishida J, Iyama A, Nakabeppu Y, Furuichi M, Fujiwara T, Sekiguchi M, Takeshige K. Intracellular localization of 8-oxo-dGTPase in human cells, with special reference to the role of the enzyme in mitochondria. J. Biol. Chem. 270: 14659-14665 (1995).
82. Bestwick RK, Moffett GL, Mathews CK. Selective expansion of mitochondrial nucleoside triphosphate pools in antimetabolite-treated HeLa cells. J. Biol. Chem. 257: 9300-9304 (1982).
83. Hayakawa H, Taketomi A, Sakumi K, Kuwano M, Sekiguchi M. Generation and elimination of 8-oxo-7,8-dihydro-2′-deoxyguanosine 5′-triphosphate, a mutagenic substrate for DNA synthesis, in human cells. Biochemistry 34: 89-95 (1995).
84. Cai JP, Ishibashi T, Takagi Y, Hayakawa H, Sekiguchi M. Mouse MTH2 protein which preventsmutations caused by 8-oxoguanine nucleotides. Biochem. Biophys. Res. Commun. 305: 1073-1077 (2003).
85. Shimokawa H, Fujii Y, Furuichi M, Sekiguchi M, Nakabeppu Y. Functional significance of conserved residues in the phosphohydrolase module of Escherichia coli MutT protein. Nucleic Acids Res. 28: 3240-3249 (2000).
86. Yang H, Slupska MM, Wei YF, Tai JH, Luther WM, Xia YR, Shih DM, Chiang JH, Baikalov C, Fitz-Gibbon S, Phan IT, Conrad A, Miller JH. Cloning and characterization of a new member of the Nudix hydrolases from human and mouse. J. Biol. Chem. 275: 8844-8853 (2000).
87. Ito R, Hayakawa H, Sekiguchi M, Ishibashi T. Multiple enzyme activities of Escherichia coli MutT protein for sanitization of DNA and RNA precursor pools. Biochemistry 44: 6670-6674 (2005).
88. Thelander L, Reichard P. Reduction of ribonucleotides. Annu. Rev. Biochem. 48: 133-158 (1979).
89. Hayakawa H, Hofer A, Thelander L, Kitajima S, Cai Y, Oshiro S, Yakushiji H, Nakabeppu Y, Kuwano M, Sekiguchi M. Metabolic fate of oxidized guanine ribonucleotides in mammalian cells. Biochemistry 38: 3610-3614 (1999).
90. Kornberg A, Baker TA. DNA Replication, 2nd edn. WH Freeman and Company, New York, 1992, pp. 53-100.
91. Bialkowski K, Kasprzak KS. A novel assay of 8-oxo-2′-deoxyguanosine-5′-triphosphate pyrophosphohydrolase (8-oxo-dGTPase) activity in cultured cells and its use for evaluation of cadmium(II) inhibition of this activity. Nucleic Acids Res. 26: 3194-3201 (1998).
92. Hayakawa H, Uchiumi T, Fukuda T, Ashizuka M, Kohno K, Kuwano M, Sekiguchi M. Binding capacity of human YB-1 protein for RNA containing 8-oxoguanine. Biochemistry 41: 12739-12744 (2002).
93. Ishibashi T, Hayakawa H, Ito R, Miyazawa M, Yamagata Y, Sekiguchi M. Mammalian enzymes for preventing transcriptional errors caused by oxidative damage. Nucleic Acids Res. 33: 3779-3784 (2005).