The role of base excision repair genes OGG1, APN1 and APN2 in benzo[a]pyrene-7,8-dione induced p53 mutagenesis

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 750, Issue 1-2, 2013, Pages 121-128

  Abedin, Zahidur ^a   Louis Juste, Melissa ^a   Stangl, Melissa ^a   Field, Jeffrey ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

APN1; APN2; Base excision repair; Lung cancer; OGG1; PAH metabolism

Indexed keywords

BENZO[A]PYRENE 7,8 DIONE; BENZO[A]PYRENE DERIVATIVE; COMPLEMENTARY DNA; PROTEIN P53; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

APN1 GENE; APN2 GENE; ARTICLE; DNA DAMAGE; EXCISION REPAIR; GENE; GENE FREQUENCY; GENE LOSS; LUNG CARCINOGENESIS; MUTAGENESIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OGG1 GENE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REPORTER GENE; YEAST;

BENZO(A)PYRENE; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; DNA REPAIR ENZYMES; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; ENDODEOXYRIBONUCLEASES; GENES, P53; MUTAGENESIS; MUTAGENS; SACCHAROMYCES CEREVISIAE PROTEINS;

NICOTIANA TABACUM;

EID: 84871715963     PISSN: 13835718     EISSN: 18793592     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2012.10.003     Document Type: Article

References (67)

1. Jemal A., Thun M.J., Ries L.A.G., Howe H.L., Weir H.K., Center M.M., Ward E., Wu X.-C., Eheman C., Anderson R., Ajani U.A., Kohler B., Edwards B.K. Annual Report to the nation on the status of cancer, 1975-2005, featuring trends in lung cancer, tobacco use, and tobacco control. J. Natl. Cancer Inst. 2008, 100:1672-1694.
2. Hecht S.S. Tobacco smoke carcinogens and lung cancer. J. Natl. Cancer Inst. 1999, 91:1194-1210.
3. Loeb L.A., Harris C.C. Advances in chemical carcinogenesis: a historical review and prospective. Cancer Res. 2008, 68:6863-6872.
4. Cavalieri E.L., Rogan E.G. Central role of radical cations in metabolic activation of polycyclic aromatic hydrocarbons. Xenobiotica 1995, 25:677-688.
5. Chakravarti D., Pelling J.C., Cavalieri E.L., Rogan E.G. Relating aromatic hydrocarbon-induced DNA adducts and c-H-ras mutations in mouse skin papillomas: the role of apurinic sites. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:10422-10426.
6. Gelboin H.V. Benzo[a]pyrene metabolism activation and carcinogenesis: role and regulation of mixed function oxidases and related enzymes. Physiol. Rev. 1980, 60:1107-1166.
7. Conney A.H. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons. G. H. A. Clowes Memorial Lecture. Cancer Res. 1982, 42:4875-4917.
8. Penning T.M., Burczynski M.E., Hung C.-F., McCoull K.D., Palackal N.T., Tsuruda L.S. Dihydrodiol dehydrogenases and polycyclic aromatic hydrocarbon activation: generation of reactive and redox active o-quinones. Chem. Res. Toxicol. 1999, 12:1-18.
9. Jennette K.W., Jeffery A.M., Blobstein S.H., Beland F.A., Harvey R.G., Weinstein I.B. Nucleoside adducts from the in vitro reaction of benzo[a]pyrene-7, 8-dihydrodiol-9,10-oxide or benzo[a]pyrene-4,5-oxide with nucleic acids. Biochemistry 1977, 16:932-938.
10. Koreeda M., Moore P.D., Wislocki P.G., Levin W., Conney A.H., Yagi H., Jerina D.M. Binding of benzo[a]pyrene-7,8-diol-9, 10-epoxides to DNA, RNA and protein of mouse skin occurs with high stereoselectivity. Science 1978, 199:778-781.
11. McCoull K.D., Rindgen D., Blair I.A., Penning T.M. Synthesis and characterization of polycyclic aromatic hydrocarbon o-quinone depurinating N7-guanine adducts. Chem. Res. Toxicol. 1999, 12:237-246.
12. Shou M., Harvey R.G., Penning T.M. Reactivity of benzo[a]pyrene-7 8-dione with DNA. Evidence for the formation of deoxyguanosine adducts. Carcinogenesis 1993, 14:475-482.
13. Yu D., Berlin J.A., Penning T.M., Field J. Reactive oxygen species generated by PAH o-quinones cause change-in-function mutations in p53. Chem. Res. Toxicol. 2002, 15:832-842.
14. Park J.H., Gelhaus S., Vedantam S., Oliva A.L., Batra A., Blair I.A., Troxel A.B., Field J., Penning T.M. The pattern of p53 mutations caused by PAH o-quinones is driven by 8-oxo-dGuo formation while the spectrum of mutations is determined by biological selection for dominance. Chem. Res. Toxicol. 2008, 21:1039-1049.
15. Park J.H., Troxel A.B., Harvey R.G., Penning T.M. Polycyclic aromatic hydrocarbon (PAH) o-quinones produced by the aldo-keto-reductases (AKRs) generate abasic sites, oxidized pyrimidines, and 8-oxo-dGuo via reactive oxygen species. Chem. Res. Toxicol. 2006, 19:719-728.
16. Lu D., Harvey R.G., Blair I.A., Penning T.M. Quantitation of benzo[a]pyrene metabolic profiles in human bronchoalveolar (H358) cells by stable isotope dilution liquid chromatography-atmospheric pressure chemical ionization mass spectrometry. Chem. Res. Toxicol. 2011, 24:1905-1914.
17. Denissenko M.F., Pao A., Tang M.-S., Pfeifer G.P. Preferential formation of benzo[a]pyrene adducts at lung cancer mutation hotspots in P53. Science 1996, 274:430-432.
18. Ames B.N., Shigenaga M.K., Hagen T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:7915-7922.
19. Loft S., Vistisen K., Ewertz M., Tjonneland A., Overvad K., Poulsen H.E. Oxidative DNA damage estimated by 8-hydroxydeoxyguanosine excretion in humans: influence of smoking, gender and body mass index. Carcinogenesis 1992, 13:2241-2247.
20. Prieme H., Loft S., Klarlund M., Gronbaek K., Tonnesen P., Poulsen H.E. Effect of smoking cessation on oxidative DNA modification estimated by 8-oxo-7,8-dihydro-2'-deoxyguanosine excretion. Carcinogenesis 1998, 19:347-351.
21. Park J.H., Mangal D., Tacka K.A., Quinn A.M., Harvey R.G., Blair I.A., Penning T.M. Evidence for the aldo-keto reductase pathway of polycyclic aromatic trans-dihydrodiol activation in human lung A549 cells. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:6846-6851.
22. Birtwistle J., Hayden R.E., Khanim F.L., Green R.M., Pearce C., Davies N.J., Wake N., Schrewe H., Ride J.P., Chipman J.K., Bunce C.M. The aldo-keto reductase AKR1C3 contributes to 7, 12-dimethylbenz(a)anthracene-3,4-dihydrodiol mediated oxidative DNA damage in myeloid cells: implications for leukemogenesis. Mutat. Res./Fund. Mol. Mech. Mutagen. 2009, 662:67-74.
23. Thorne D., Wilson J., Kumaravel T.S., Massey E.D., McEwan M. Measurement of oxidative DNA damage induced by mainstream cigarette smoke in cultured NCI-H292 human pulmonary carcinoma cells. Mutat. Res./Gen. Toxicol. Environ. Mutagen. 2009, 673:3-8.
24. Abedin Z., Sen S., Field J. Aldo-keto reductases protect lung adenocarcinoma cells from the acute toxicity of B[a]P-7, 8-trans-dihydrodiol. Chem. Res. Toxicol. 2012, 25:113-121.
25. Jiang H., Gelhaus S.L., Mangal D., Harvey R.G., Blair I.A., Penning T.M. Metabolism of benzo[a]pyrene in human bronchoalveolar H358 cells using liquid chromatography-mass spectrometry. Chem. Res. Toxicol. 2007, 20:1331-1341.
26. Shen Y.M., Troxel A.B., Vedantam S., Penning T.M., Field J. Comparison of p53 mutations induced by PAH o-quinones with those caused by anti-benzo[a]pyrene diol epoxide in vitro: role of reactive oxygen and biological selection. Chem. Res. Toxicol. 2006, 19:1441-1450.
27. Hollstein M., Sidransky D., Vogelstein B., Harris C.C. p53 mutations in human cancers. Science 1991, 253:49-53.
28. Hainaut P., Pfeifer G.P. Patterns of p53 G-->T transversions in lung cancers reflect the primary mutagenic signature of DNA-damage by tobacco smoke. Carcinogenesis 2001, 22:367-374.
29. Sen S., Bhojnagarwala P., Francey L., Lu D., Penning T.M., Field J. p53 mutagenesis by benzo[a]pyrene derived radical cations. Chem. Res. Toxicol. 2012, 25:2117-2126.
30. Beroud C., Soussi T. p53 gene mutation: software and database. Nucleic Acids Res. 1998, 26:200-204.
31. Toyooka S., Tsuda T., Gazdar A.F. The TP53 gene, tobacco exposure, and lung cancer. Hum. Mutat. 2003, 21:229-239.
32. Boiteux S., Radicella J.P. The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis. Arch. Biochem. Biophys. 2000, 377:1-8.
33. Shinmura K., Yokota J. The OGG1 gene encodes a repair enzyme for oxidatively damaged DNA and is involved in human carcinogenesis. Antioxid. Redox Signal. 2001, 3:597-609.
34. Lu R., Nash H.M., Verdine G.L. A mammalian DNA repair enzyme that excises oxidatively damaged guanines maps to a locus frequently lost in lung cancer. Curr. Biol. 1997, 7:397-407.
35. Nishimura S. 8-hydroxyguanine: from its discovery in 1983 to the present status. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2006, 82:127-141.
36. Ho R., Rachek L.I., Xu Y., Kelley M.R., LeDoux S.P., Wilson G.L. Yeast apurinic/apyrimidinic endonuclease Apn1 protects mammalian neuronal cell line from oxidative stress. J. Neurochem. 2007, 102:13-24.
37. Evans A.R., Limp-Foster M., Kelley M.R. Going APE over ref-1. Mutat. Res. 2000, 461:83-108.
38. Wilson D.M., Barsky D. The major human abasic endonuclease: formation, consequences and repair of abasic lesions in DNA. Mutat. Res. 2001, 485:283-307.
39. Hill J.W., Hazra T.K., Izumi T., Mitra S. Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res. 2001, 29:430-438.
40. Saitoh T., Shinmura K., Yamaguchi S., Tani M., Seki S., Murakami H., Nojima Y., Yokota J. Enhancement of OGG1 protein AP lyase activity by increase of APEX protein. Mutat. Res. 2001, 486:31-40.
41. Flaman J.M., Frebourg T., Moreau V., Charbonnier F., Martin C., Chappuis P., Sappino A.P., Limacher J.M., Bron L., Benhattar J., Tada M., Van Meir E.G., Estreicher A., Iggo R.D. A simple p53 functional asay for screening cell lines, blood, and tumors. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:3963-3967.
42. Guide to yeast genetics and molecular biology, Methods in Enzymology 1991, Academic Press, New York. C. Guthrie, G.R. Fink (Eds.).
43. Le Page F., Klungland A., Barnes D.E., Sarasin A., Boiteux S. Transcription coupled repair of 8-oxoguanine in murine cells: the ogg1 protein is required for repair in nontranscribed sequences but not in transcribed sequences. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8397-8402.
44. Brachmann R.K., Vidal M., Boeke J.D. Dominant-negative p53 mutations selected in yeast hit cancer hot spots. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:4091-4095.
45. Rodin S.N., Rodin A.S. Human lung cancer and p53: the interplay between mutagenesis and selection. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:12244-12249.
46. Yoon J.H., Lee C.S., Pfeifer G.P. Simulated sunlight and benzo[a]pyrene diol epoxide induced mutagenesis in the human p53 gene evaluated by the yeast functional assay: lack of correspondence to tumor mutation spectra. Carcinogenesis 2003, 24:113-119.
47. Thomas D., Scot A.D., Barbey R., Padula M., Boiteux S. Inactivation of OGG1 increases the incidence of G. C-->T. A transversions in Saccharomyces cerevisiae: evidence for endogenous oxidative damage to DNA in eukaryotic cells. Mol. Gen. Genet. 1997, 254:171-178.
48. Melo R.G., Leitao A.C., Padula M. Role of OGG1 and NTG2 in the repair of oxidative DNA damage and mutagenesis induced by hydrogen peroxide in Saccharomyces cerevisiae: relationships with transition metals iron and copper. Yeast 2004, 21:991-1003.
49. Karahalil B., Girard P.M., Boiteux S., Dizdaroglu M. Substrate specificity of the Ogg1 protein of Saccharomyces cerevisiae: excision of guanine lesions produced in DNA by ionizing radiation- or hydrogen peroxide/metal ion-generated free radicals. Nucleic Acids Res. 1998, 26:1228-1233.
50. Hu J., Imam S.Z., Hashiguchi K., de Souza-Pinto N.C., Bohr V.A. Phosphorylation of human oxoguanine DNA glycosylase (alpha-OGG1) modulates its function. Nucleic Acids Res. 2005, 33:3271-3282.
51. Demple B., Harrison L. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 1994, 63:915-948.
52. Girard P.M., Boiteux S. Repair of oxidized DNA bases in the yeast Saccharomyces cerevisiae. Biochimie 1997, 79:559-566.
53. Ishchenko A.A., Yang X., Ramotar D., Saparbaev M. The 3'→5' exonuclease of Apn1 provides an alternative pathway to repair 7, 8-dihydro-8-oxodeoxyguanosine in Saccharomyces cerevisiae. Mol. Cell. Biol. 2005, 25:6380-6390.
54. Mol C.D., Hosfield D.J., Tainer J.A. Abasic site recognition by two apurinic/apyrimidinic endonuclease families in DNA base excision repair: the 3' ends justify the means. Mutat. Res./DNA Repair 2000, 460:211-229.
55. Boiteux S., Guillet M. Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae. DNA Repair 2004, 3:1-12.
56. Swanson R.L., Morey N.J., Doetsch P.W., Jinks-Robertson S. Overlapping specificities of base excision repair, nucleotide excision repair, recombination, and translesion synthesis pathways for DNA base damage in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:2929-2935.
57. Ramotar D., Popoff S.C., Gralla E.B., Demple B. Cellular role of yeast Apn1 apurinic endonuclease/3'-diesterase: repair of oxidative and alkylation DNA damage and control of spontaneous mutation. Mol. Cell. Biol. 1991, 11:4537-4544.
58. Kunz B.A., Henson E.S., Roche H., Ramotar D., Nunoshiba T., Demple B. Specificity of the mutator caused by deletion of the yeast structural gene (APN1) for the major apurinic endonuclease. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:8165-8169.
59. Yamane A., Shinmura K., Sunaga N., Saitoh T., Yamaguchi S., Shinmura Y., Yoshimura K., Murakami H., Nojima Y., Kohno T., 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 2003, 24:1031-1037.
60. Larsen E., Kwon K., Coin F., Egly J.M., Klungland A. Transcription activities at 8-oxoG lesions in DNA. DNA Repair 2004, 3:1457-1468.
61. Tornaletti S., Maeda L.S., Kolodner R.D., Hanawalt P.C. Effect of 8-oxoguanine on transcription elongation by T7 RNA polymerase and mammalian RNA polymerase II. DNA Repair (Amst.) 2004, 3:483-494.
62. Tornaletti S., Maeda L.S., Hanawalt P.C. Transcription arrest at an abasic site in the transcribed strand of template DNA. Chem. Res. Toxicol. 2006, 19:1215-1220.
63. Hanawalt P.C., Spivak G. Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell. Biol. 2008, 9:958-970.
64. Pastoriza-Gallego M., Armier J., Sarasin A. Transcription through 8-oxoguanine in DNA repair-proficient and Csb-/Ogg1- DNA repair-deficient mouse embryonic fibroblasts is dependent upon promoter strength and sequence context. Mutagenesis 2007, 22:343-351.
65. Thorslund T., Sunesen M., Bohr V.A., Stevnsner T. Repair of 8-oxoG is slower in endogenous nuclear genes than in mitochondrial DNA and is without strand bias. DNA Repair 2002, 1:261-273.
66. Bregeon D., Doddridge Z.A., You H.J., Weiss B., Doetsch P.W. Transcriptional mutagenesis induced by uracil and 8-oxoguanine in Escherichia coli. Mol. Cell 2003, 12:959-970.
67. Kim N., Jinks-Robertson S. Abasic sites in the transcribed strand of yeast DNA are removed by transcription-coupled nucleotide excision repair. Mol. Cell. Biol. 2010, 30:3206-3215.