Effects of base excision repair proteins on mutagenesis by 8-oxo-7,8-dihydroguanine (8-hydroxyguanine) paired with cytosine and adenine

DNA Repair

Volumn 9, Issue 5, 2010, Pages 542-550

  Suzuki, Tetsuya ^a   Harashima, Hideyoshi ^a   Kamiya, Hiroyuki ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

8 Hydroxyguanine; 8 Oxo 7,8 dihydroguanine; Base excision repair; DNA glycosylase

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; 8 HYDROXYGUANINE; ADENINE; CYTOSINE; DNA GLYCOSYLASE MUTY; DNA GLYCOSYLASE NEIL1; DNA GLYCOSYLASE NTH1; DNA GLYCOSYLASE OGG1; DNA GLYCOSYLTRANSFERASE; PLASMID DNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL LINE; CONTROLLED STUDY; EXCISION REPAIR; GENE FUNCTION; GENE MUTATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MUTAGENESIS; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; PROTEIN FUNCTION;

ADENINE; BASE SEQUENCE; CELL LINE; CYTOSINE; DEOXYGUANINE NUCLEOTIDES; DNA; DNA GLYCOSYLASES; DNA REPAIR; GENE KNOCKDOWN TECHNIQUES; GUANINE; HUMANS; MUTAGENESIS; MUTATION; PLASMIDS; RNA, SMALL INTERFERING;

EID: 77952108570     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2010.02.004     Document Type: Article

References (72)

1. Farr S.B., and Kogoma T. Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol. Rev. 55 (1991) 561-585
2. Halliwell B., and Aruoma O.I. DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems. FEBS Lett. 281 (1991) 9-19
3. Ames B.N., Shigenaga M.K., and Hagen T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 7915-7922
4. Kasai H. Analysis of a form of oxidative DNA damage, 8-hydroxy-2′-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutat. Res. 387 (1997) 147-163
5. Kamiya H. 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 (2003) 517-531
6. Shibutani S., Takeshita M., and Grollman A.P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349 (1991) 431-434
7. Wood M.L., Dizdaroglu M., Gajewski E., and Essigmann J.M. Mechanistic studies of ionizing radiation and oxidative mutagenesis: genetic effects of a single 8-hydroxyguanine (7-hydro-8-oxoguanine) residue inserted at a unique site in a viral genome. Biochemistry 29 (1990) 7024-7032
8. Cheng K.C., Cahill D.S., Kasai H., Nishimura S., and Loeb L.A. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G → T and A → C substitutions. J. Biol. Chem. 267 (1992) 166-172
9. Moriya M., and Grollman A.P. Mutations in the mutY gene of Escherichia coli enhance the frequency of targeted G:C → T:A transversions induced by a single 8-oxoguanine residue in single-stranded DNA. Mol. Gen. Genet. 239 (1993) 72-76
10. Wagner J., Kamiya H., and Fuchs R.P. Leading versus lagging strand mutagenesis induced by 7,8-dihydro-8-oxo-2′-deoxyguanosine in Escherichia coli. J. Mol. Biol. 265 (1997) 302-309
11. Kamiya H., Miura K., Ishikawa H., Inoue H., Nishimura S., and Ohtsuka E. c-Ha-ras containing 8-hydroxyguanine at codon 12 induces point mutations at the modified and adjacent positions. Cancer Res. 52 (1992) 3483-3485
12. Moriya M. Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-oxoguanine in DNA induces targeted G.C → T.A transversions in simian kidney cells. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 1122-1126
13. Kamiya H., Murata-Kamiya N., Koizume S., Inoue H., Nishimura S., and Ohtsuka E. 8-Hydroxyguanine (7,8-dihydro-8-oxoguanine) in hot spots of the c-Ha-ras gene: effects of sequence contexts on mutation spectra. Carcinogenesis 16 (1995) 883-889
14. Le Page F., Margot A., Grollman A.P., Sarasin A., and Gentil A. Mutagenicity of a unique 8-oxoguanine in a human Ha-ras sequence in mammalian cells. Carcinogenesis 16 (1995) 2779-2784
15. Tan X., Grollman A.P., and Shibutani S. Comparison of the mutagenic properties of 8-oxo-7,8-dihydro-2′-deoxyadenosine and 8-oxo-7,8-dihydro-2′-deoxyguanosine DNA lesions in mammalian cells. Carcinogenesis 20 (1999) 2287-2292
16. Maki H., and Sekiguchi M. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355 (1992) 273-275
17. Kamiya H., and Kasai H. 2-Hydroxy-dATP is incorporated opposite G by Escherichia coli DNA polymerase III resulting in high mutagenicity. Nucleic Acids Res. 28 (2000) 1640-1646
18. Inoue M., Kamiya H., Fujikawa K., Ootsuyama Y., Murata-Kamiya N., Osaki T., Yasumoto K., and Kasai H. 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 (1998) 11069-11074
19. Bjoras M., Luna L., Johnsen B., Hoff E., Haug T., Rognes T., and Seeberg E. Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites. EMBO J. 16 (1997) 6314-6322
20. Aburatani H., Hippo Y., Ishida T., Takashima R., Matsuba C., Kodama T., Takao M., Yasui A., Yamamoto K., and Asano M. Cloning and characterization of mammalian 8-hydroxyguanine-specific DNA glycosylase/apurinic, apyrimidinic lyase, a functional mutM homologue. Cancer Res. 57 (1997) 2151-2156
21. Rosenquist T.A., Zharkov D.O., and Grollman A.P. Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 7429-7434
22. Radicella J.P., Dherin C., Desmaze C., Fox M.S., and Boiteux S. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 8010-8015
23. Roldán-Arjona T., Wei Y.-F., Carter K.C., Klungland A., Anselmino C., Wang R.P., Augustus M., and Lindahl T. Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 8016-8020
24. Lu R., Nash H.M., and Verdine G.L. A mammalian DNA repair enzyme that excises oxidatively damaged guanines maps to a locus frequently lost in lung cancer. Curr. Biol. 7 (1997) 397-407
25. Arai K., Morishita K., Shinmura K., Kohno T., Kim S.R., Nohmi T., Taniwaki M., Ohwada S., and Yokota J. Cloning of a human homolog of the yeast OGG1 gene that is involved in the repair of oxidative DNA damage. Oncogene 14 (1997) 2857-2861
26. Takao M., Zhang Q.M., Yonei S., and Yasui A. Differential subcellular localization of human MutY homolog (hMYH) and the functional activity of adenine:8-oxoguanine DNA glycosylase. Nucleic Acids Res. 27 (1999) 3638-3644
27. Slupska M.M., Luther W.M., Chiang J.H., Yang H., and Miller J.H. Functional expression of hMYH, a human homolog of the Escherichia coli MutY protein. J. Bacteriol. 181 (1999) 6210-6213
28. McGoldrick J.P., Yeh Y.C., Solomon M., Essigmann J.M., and Lu A.L. Characterization of a mammalian homolog of the Escherichia coli MutY mismatch repair protein. Mol. Cell. Biol. 15 (1995) 989-996
29. Ohtsubo T., Nishioka K., Imaiso Y., Iwai S., Shimokawa H., Oda H., Fujiwara T., and Nakabeppu Y. Identification of human MutY homolog (hMYH) as a repair enzyme for 2-hydroxyadenine in DNA and detection of multiple forms of hMYH located in nuclei and mitochondria. Nucleic Acids Res. 28 (2000) 1355-1364
30. Hollenbach S., Dhénaut A., Eckert I., Radicella J.P., and Epe B. Overexpression of Ogg1 in mammalian cells: effects on induced and spontaneous oxidative DNA damage and mutagenesis. Carcinogenesis 20 (1999) 1863-1868
31. Yamane A., Shinmura K., Sunaga N., Saitoh T., Yamaguchi S., Shinmura Y., Yoshimura K., Murakami H., Nojima Y., Kohno T., and Yokota J. Suppressive activities of OGG1 and MYH proteins against G:C to T:A mutations caused by 8-hydroxyguanine but not by benzo[a]pyrene diol epoxide in human cells in vivo. Carcinogenesis 24 (2003) 1031-1037
32. Ikeda S., Biswas T., Roy R., Izumi T., Boldogh I., Kurosky A., Sarker A.H., Seki S., and Mitra S. Purification and characterization of human NTH1, a homolog of Escherichia coli endonuclease III. Direct identification of Lys-212 as the active nucleophilic residue. J. Biol. Chem. 273 (1998) 21585-21593
33. Hilbert T.P., Chaung W., Boorstein R.J., Cunningham R.P., and Teebor G.W. Cloning and expression of the cDNA encoding the human homologue of the DNA repair enzyme, Escherichia coli endonuclease III. J. Biol. Chem. 272 (1997) 6733-6740
34. Aspinwall R., Rothwell D.G., Roldan-Arjona T., Anselmino C., Ward C.J., Cheadle J.P., Sampson J.R., Lindahl T., Harris P.C., and Hickson I.D. Cloning and characterization of a functional human homolog of Escherichia coli endonuclease III. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 109-114
35. Dizdaroglu M., Karahalil B., Sentürker S., Buckley T.J., and Roldán-Arjona T. Excision of products of oxidative DNA base damage by human NTH1 protein. Biochemistry 38 (1999) 243-246
36. Hazra T.K., Kow Y.W., Hatahet Z., Imhoff B., Boldogh I., Mokkapati S.K., Mitra S., and Izumi T. Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J. Biol. Chem. 277 (2002) 30417-30420
37. Takao M., Kanno S., Kobayashi K., Zhang Q.M., Yonei S., van der Horst G.T., and Yasui A. A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue. J. Biol. Chem. 277 (2002) 42205-42213
38. Rosenquist T.A., Zaika E., Fernandes A.S., Zharkov D.O., Miller H., and Grollman A.P. The novel DNA glycosylase, NEIL1, protects mammalian cells from radiation-mediated cell death. DNA Repair 2 (2003) 581-1581
39. Katafuchi A., Nakano T., Masaoka A., Terato H., Iwai S., Hanaoka F., and Ide H. Differential specificity of human and Escherichia coli endonuclease III and VIII homologues for oxidative base lesions. J. Biol. Chem. 279 (2004) 14464-14471
40. Matsumoto Y., Zhang Q.M., Takao M., Yasui A., and Yonei S. Escherichia coli Nth and human hNTH1 DNA glycosylases are involved in removal of 8-oxoguanine from 8-oxoguanine/guanine mispairs in DNA. Nucleic Acids Res. 29 (2001) 1975-1981
41. Hazra T.K., Izumi T., Boldogh I., Imhoff B., Kow Y.W., Jaruga P., Dizdaroglu M., and Mitra S. Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3523-3528
42. Bandaru V., Sunkara S., Wallace S.S., and Bond J.P. A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII. DNA Repair 1 (2002) 517-529
43. Morland I., Rolseth V., Luna L., Rognes T., Bjørås M., and Seeberg E. Human DNA glycosylases of the bacterial Fpg/MutM superfamily: an alternative pathway for the repair of 8-oxoguanine and other oxidation products in DNA. Nucleic Acids Res. 30 (2002) 4926-4936
44. Dou H., Mitra S., and Hazra T.K. Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J. Biol. Chem. 278 (2003) 49679-54984
45. Suzuki T., Yamamoto K., Harashima H., and Kamiya H. Base excision repair enzyme endonuclease III suppresses mutagenesis caused by 8-hydroxy-dGTP. DNA Repair 7 (2008) 88-94
46. Kamiya H., and Kasai H. Substitution and deletion mutations induced by 2-hydroxyadenine in Escherichia coli: effects of sequence contexts in leading and lagging strands. Nucleic Acids Res. 25 (1997) 304-310
47. Obata F., Nunoshiba T., Hashimoto-Gotoh T., and Yamamoto K. An improved system for selection of forward mutations in an Escherichia coli supF gene carried by plasmids. J. Radiat. Res. 39 (1998) 263-270
48. Satou K., Hori M., Kawai K., Kasai H., Harashima H., and Kamiya H. Involvement of specialized DNA polymerases in mutagenesis by 8-hydroxy-dGTP in human cells. DNA Repair 8 (2008) 637-642
49. Tornaletti S., Maeda L.S., Kolodner R.D., and Hanawalt P.C. Effect of 8-oxoguanine on transcription elongation by T7 RNA polymerase and mammalian RNA polymerase II. DNA Repair 3 (2004) 483-494
50. Stary A., and Sarasin A. Simian virus 40 (SV40) large T antigen-dependent amplification of an Epstein-Barr virus-SV40 hybrid shuttle vector integrated into the human HeLa cell genome. J. Gen. Virol. 73 (1992) 1679-1685
51. Satou K., Kawai K., Kasai H., Harashima H., and Kamiya H. Mutagenic effects of 8-hydroxy-dGTP in live mammalian cells. Free Radic. Biol. Med. 42 (2007) 1552-1560
52. Oyama M., Wakasugi M., Hama T., Hashidume H., Iwakami Y., Imai R., Hoshino S., Morioka H., Ishigaki Y., Nikaido O., and Matsunaga T. Human NTH1 physically interacts with p53 and proliferating cell nuclear antigen. Biochem. Biophys. Res. Commun. 321 (2004) 183-191
53. Marenstein D.R., Ocampo M.T., Chan M.K., Altamirano A., Basu A.K., Boorstein R.J., Cunningham R.P., and Teebor G.W. Stimulation of human endonuclease III by Y box-binding protein 1 (DNA-binding protein B). Interaction between a base excision repair enzyme and a transcription factor. J. Biol. Chem. 276 (2001) 21242-21249
54. Marenstein D.R., Chan M.K., Altamirano A., Basu A.K., Boorstein R.J., Cunningham R.P., and Teebor G.W. Substrate specificity of human endonuclease III (hNTH1). Effect of human APE1 on hNTH1 activity. J. Biol. Chem. 278 (2003) 9005-9012
55. Dou H., Theriot C.A., Das A., Hegde M.L., Matsumoto Y., Boldogh I., Hazra T.K., Bhakat K.K., and Mitra S. Interaction of the human DNA glycosylase NEIL1 with proliferating cell nuclear antigen. The potential for replication-associated repair of oxidized bases in mammalian genomes. J. Biol. Chem. 283 (2008) 3130-3140
56. Mokkapati S.K., Wiederhold L., Hazra T.K., and Mitra S. Stimulation of DNA glycosylase activity of OGG1 by NEIL1: functional collaboration between two human DNA glycosylases. Biochemistry 43 (2004) 11596-11604
57. Chan M.K., Ocampo-Hafalla M.T., Vartanian V., Jaruga P., Kirkali G., Koenig K.L., Brown S., Lloyd R.S., Dizdaroglu M., and Teebor G.W. Targeted deletion of the genes encoding NTH1 and NEIL1 DNA N-glycosylases reveals the existence of novel carcinogenic oxidative damage to DNA. DNA Repair 8 (2009) 786-794
58. Tajiri T., Maki H., and Sekiguchi M. Functional cooperation of MutT, MutM and MutY proteins in preventing mutations caused by spontaneous oxidation of guanine nucleotide in Escherichia coli. Mutat. Res. 336 (1995) 257-267
59. M. Hori, K. Satou, H. Harashima, H. Kamiya, Suppression of mutagenesis by 8-hydroxy-2'-deoxyguanosine 5'-triphosphate (7,8-dihydro-8-oxo-2'-deoxyguanosine 5'-triphosphate) by human MTH1, MTH2, and NUDT5, Free Radic. Biol. Med. (2010) in press, doi:10.1016/j.freeradbiomed.2010.02.002.
60. Ichikawa J., Tsuchimoto D., Oka S., Ohno M., Furuichi M., Sakumi K., and Nakabeppu Y. Oxidation of mitochondrial deoxynucleotide pools by exposure to sodium nitroprusside induces cell death. DNA Repair 7 (2008) 418-430
61. Oka S., Ohno M., Tsuchimoto D., Sakumi K., Furuichi M., and Nakabeppu Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. EMBO J. 27 (2008) 421-432
62. Lee D.H., and Pfeifer G.P. Translesion synthesis of 7,8-dihydro-8-oxo-2′-deoxyguanosine by DNA polymerase eta in vivo. Mutat. Res. 641 (2008) 19-26
63. Maga G., Crespan E., Wimmer U., van Loon B., Amoroso A., Mondello C., Belgiovine C., Ferrari E., Locatelli G., Villani G., and Hübscher U. Replication protein A and proliferating cell nuclear antigen coordinate DNA polymerase selection in 8-oxo-guanine repair. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 20689-20694
64. Le Page F., Guy A., Cadet J., Sarasin A., and Gentil A. Repair and mutagenic potency of 8-oxoG:A and 8-oxoG:C base pairs in mammalian cells. Nucleic Acids Res. 26 (1998) 1276-1281
65. Sakumi K., Tominaga Y., Furuichi M., Xu P., Tsuzuki T., Sekiguchi M., and Nakabeppu Y. Ogg1 knockout-associated lung tumorigenesis and its suppression by Mth1 gene disruption. Cancer Res. 63 (2003) 902-905
66. Osterod M., Hollenbach S., Hengstler J.G., Barnes D.E., Lindahl T., and Epe B. Age-related tissue-specific accumulation of oxidative DNA base damage in 7,8-dihydro-8-oxoguanine-DNA glycosylase (Ogg1) deficient mice. Carcinogenesis 22 (2001) 1459-1463
67. 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., and Noda T. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 4156-4161
68. Klungland A., Rosewell I., Hollenbach S., Larsen E., Daly G., Epe B., Seeberg E., Lindahl T., and Barnes D.E. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13300-13305
69. Sakamoto K., Tominaga Y., Yamauchi K., Nakatsu Y., Sakumi K., Yoshiyama K., Egashira A., Kura S., Yao T., Tsuneyoshi M., Maki H., Nakabeppu Y., and Tsuzuki T. MUTYH-null mice are susceptible to spontaneous and oxidative stress induced intestinal tumorigenesis. Cancer Res. 67 (2007) 6599-6604
70. Takao M., Kanno S., Shiromoto T., Hasegawa R., Ide H., Ikeda S., Sarker A.H., Seki S., Xing J.Z., Le X.C., Weinfeld M., Kobayashi K., Miyazaki J., Muijtjens M., Hoeijmakers J.H., van der Horst G., and Yasui A. Novel nuclear and mitochondrial glycosylases revealed by disruption of the mouse Nth1 gene encoding an endonuclease III homolog for repair of thymine glycols. EMBO J. 21 (2002) 3486-3493
71. Ocampo M.T., Chaung W., Marenstein D.R., Chan M.K., Altamirano A., Basu A.K., Boorstein R.J., Cunningham R.P., and Teebor G.W. Targeted deletion of mNth1 reveals a novel DNA repair enzyme activity. Mol. Cell. Biol. 22 (2002) 6111-6121
72. Sweasy J.B., Lang T., and DiMaio D. Is base excision repair a tumor suppressor mechanism?. Cell Cycle 5 (2006) 250-259