Enhancement of the Mutagenicity of Benzo(a)pyrene Diol Epoxide by A Nonmutagenic Dose of Ultraviolet A Radiation

Cancer Research

Volumn 63, Issue 24, 2003, Pages 8708-8716

  Besaratinia, Ahmad ^a   Pfeifer, Gerd P ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGE LAMBDA PROTEIN CII; BENZO[A]PYRENE 7,8 DIHYDRODIOL 9,10 OXIDE; CARCINOGEN; DIHYDROXYBENZO[A]PYRENE OXIDE; DINUCLEOTIDE; POLYCYCLIC AROMATIC HYDROCARBON; TRANSCRIPTION FACTOR; TRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL; ANIMAL CELL; ARTICLE; BACTERIOPHAGE LAMBDA; BIOSYNTHESIS; CONTROLLED STUDY; CPG ISLAND; CYTOTOXICITY; DNA ADDUCT; DNA SEQUENCE; DRUG EFFECT; EMBRYO; FIBROBLAST; GENE MAPPING; GENE MUTATION; GENETICS; MOUSE; MUTAGEN TESTING; MUTAGENICITY; MUTANT; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RADIATION EXPOSURE; TRANSGENE; ULTRAVIOLET A RADIATION; ULTRAVIOLET RADIATION;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; ANIMALS; CARCINOGENS; DNA ADDUCTS; EMBRYO; FIBROBLASTS; MICE; MUTAGENICITY TESTS; TRANSCRIPTION FACTORS; TRANSGENES; ULTRAVIOLET RAYS; VIRAL PROTEINS;

EID: 0346059599     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Wilcosky, T. C., and Griffith, J. D. Application of biological markers. In: B. S. Hulka, T. C. Wilcosky, and J. D. Griffith (eds.), Biological Markers in Epidemiology, Vol. 1, pp. 16-27. New York: Oxford University Press, 1990.
2. Hulka, B. S. Methodological issues in molecular epidemiology. In: B. S. Hulka, T. Wilcosky, and J. Griffith (eds.), Biological Markers in Epidemiology, pp. 214-226. New York: Oxford University Press, 1990.
3. DeMarini, D. M. Mutation spectra of complex mixtures. Mutat. Res., 411: 11-18, 1998.
4. Dolmans, D. E., Fukumura, D., and Jain, R. K. Photodynamic therapy for cancer. Nat. Rev. Cancer, 3: 380-387, 2003.
5. Harvey, R. G. Environmental occurrence and cancer. In: R. G. Harvey (ed.), Polycyclic Aromatic Hydrocarbons: Chemistry and Carcinogenicity, Ed. 1:, pp. 11-25. New York: Cambridge University Press, 1991.
6. Phillips, D. H. Polycyclic aromatic hydrocarbons in the diet. Mutat. Res., 443: 139-147, 1999.
7. Besaratinia, A., Kleinjans, J. C., and Van Schooten, F. J. Biomonitoring of tobacco smoke carcinogenicity by dosimetry of DNA adducts and genotyping and phenotyping of biotransformational enzymes: a review on polycyclic aromatic hydrocarbons. Biomarkers, 7: 209-229, 2002.
8. Phillips, D. H. Smoking-related DNA and protein adducts in human tissues. Carcinogenesis (Lond.), 23: 1979-2004, 2002.
9. Harvey, R. G. Metabolic activation, DNA binding, and mechanisms of carcinogenesis. In: R. G. Harvey (ed.), Polycyclic Aromatic Hydrocarbons: Chemistry and Carcinogenicity, pp. 50-95. New York: Cambridge University Press, 1991.
10. Hall, M., and Grover, P. L. Polycyclic aromatic hydrocarbons: metabolism, activation and tumour initiation. In: C. S. Cooper and P. L. Grover (eds.), Chemical Carcinogenesis and Mutagenesis I, Vol. 94/1, pp. 327-372. Berlin-Heidelberg: Springer-Verlag, 1990.
11. Besaratinia, A. and Pfeifer, G. P. DNA Damage and Mutagenesis Induced by PAHs. In: A. Luch (ed.), The Carcinogenic Effects of Polycyclic Aromatic Hydrocarbons. World Scientific Publishing Company, Singapore, Singapore, in press, 2003.
12. Denissenko, M. F., Pao, A., Tang, M., and Pfeifer, G. P. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in. P53. Science (Wash. DC), 274: 430-432, 1996.
13. Smith, L. E., Denissenko, M. F., Bennett, W. P., Li, H., Amin, S., Tang, M., and Pfeifer, G. P. Targeting of lung cancer mutational hotspots by polycyclic aromatic hydrocarbons. J. Natl. Cancer Inst., 92: 803-811, 2000.
14. Feng, Z., Hu, W., Chen, J. X., Pao, A., Li, H., Rom, W., Hung, M. C., and Tang, M. S. Preferential DNA damage and poor repair determine ras gene mutational hotspot in human cancer. J. Natl. Cancer Inst., 94: 1527-1536, 2002.
15. de Gruijl, F. R. Skin cancer and solar UV radiation. Eur. J. Cancer, 35: 2003-2009, 1999.
16. Woodhead, A. D., Setlow, R. B., and Tanaka, M. Environmental factors in nonmelanoma and melanoma skin cancer. J. Epidemiol., 9: S102-114, 1999.
17. de Gruijl, F. R. Photocarcinogenesis: UVA vs. UVB radiation. Skin Pharmacol. Appl. Skin Physiol., 15: 316-320, 2002.
18. Cadet, J., Berger, M., Douki, T., Morin, B., Raoul, S., Ravanat, J. L., and Spinelli, S. Effects of UV and visible radiation on DNA-final base damage. Biol. Chem., 378: 1275-1286, 1997.
19. King, G. N., Healy, C. M., Glover, M. T., Kwan, J. T., Williams, D. M., Leigh, I. M., Worthington, H. V., and Thornhill, M. H. Increased prevalence of dysplastic and malignant lip lesions in renal-transplant recipients. N. Engl. J. Med., 332: 1052-1057, 1995.
20. Vander Straten, M., Carrasco, D., Paterson, M. S., McCrary, M. L., Meyer, D. J., and Tyring, S. K. Tobacco use and skin disease. South Med. J., 94: 621-634, 2001.
21. Nikkila, A., Penttinen, S., and Kukkonen, J. V. UV-B-Induced acute toxicity of pyrene to the waterflea Daphnia magna in natural freshwaters. Ecotoxicol. Environ. Saf., 44: 271-279, 1999.
22. Boese, B. L., Ozretich, R. J., Lamberson, J. O., Cole, F. A., Swartz, R. C., and Ferraro, S. P. Phototoxic evaluation of marine sediments collected from a PAH-contaminated site. Arch. Environ. Contam. Toxicol., 38: 274-282, 2000.
23. Laycock, N. L., Schirmer, K., Bols, N. C., and Sivak, J. G. Optical properties of rainbow trout lenses after in vitro exposure to polycyclic aromatic hydrocarbons in the presence or absence of ultraviolet radiation. Exp. Eye Res., 70: 205-214, 2000.
24. Pfeifer, G. P., Chen, H. H., Komura, J., and Riggs, A. D. Chromatin structure analysis by ligation-mediated and terminal transferase-mediated polymerase chain reaction. Methods Enzymol., 304: 548-571, 1999.
25. Besaratinia, A., and Pfeifer, G. P. Weak yet distinct mutagenicity of acrylamide in mammalian cells. J. Natl. Cancer Inst., 95: 855-861, 2003.
26. Jakubczak, J. L., Merlino, G., French, J. E., Muller, W. J., Paul, B., Adhya, S., and Garges, S. Analysis of genetic instability during mammary tumor progression using a novel selection-based assay for in vivo mutations in a bacteriophage lambda transgene target. Proc. Natl. Acad. Sci. USA, 93: 9073-9078, 1996.
27. Herskowitz, I., and Hagen, D. The lysis-lysogeny decision of phage lambda: explicit programming and responsiveness. Annu. Rev. Genet., 14: 399-445, 1980.
28. Adams, W. T., and Skopek, T. R. Statistical test for the comparison of samples from mutational spectra. J. Mol. Biol., 194: 391-396, 1987.
29. Besaratinia, A., Bates, S. E., and Pfeifer, G. P. Mutational signature of the proximate bladder carcinogen N-hydroxy-4-acetylaminobiphenyl: inconsistency with the p53 mutational spectrum in bladder cancer. Cancer Res., 62: 4331-4338, 2002.
30. Harbach, P. R., Zimmer, D. M., Filipunas, A. L., Mattes, W. B., and Aaron, C. S. Spontaneous mutation spectrum at the lambda cII locus in liver, lung, and spleen tissue of Big Blue transgenic mice. Environ. Mol. Mutagen., 33: 132-143, 1999.
31. Davies, R., Gant, T. W., Smith, L. L., and Styles, J. A. Tamoxifen induces G:C→T:A mutations in the cII gene in the liver of lambda/lacI transgenic rats but not at 5′-CpG-3* dinucleotide sequences as found in the lacI transgene. Carcinogenesis (Lond.), 20: 1351-1356, 1999.
32. de Boer, J. G., Erfle, H., Walsh, D., Holcroft, J., Provost, J. S., Rogers, B., Tindall, K. R., and Glickman, B. W. Spectrum of spontaneous mutations in liver tissue of lacI transgenic mice. Environ. Mol. Mutagen., 30: 273-286, 1997.
33. Swiger, R. R., Cosentino, L., Shima, N., Bielas, J. H., Cruz-Munoz, W., and Heddle, J. A. The cII locus in the MutaMouse system. Environ. Mol. Mutagen., 34: 201-207, 1999.
34. Mellon, I., Spivak, G., and Hanawalt, P. C. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell, 51: 241-249, 1987.
35. Hanawalt, P. C. Transcription-coupled repair and human disease. Science (Wash. DC), 266: 1957-1958, 1994.
36. Denissenko, M. F., Pao, A., Pfeifer, G. P., and Tang, M. Slow repair of bulky DNA adducts along the nontranscribed strand of the human p53 gene may explain the strand bias of transversion mutations in cancers. Oncogene, 16: 1241-1247, 1998.
37. Rochette, P. J., Therrien, J. P., Drouin, R., Perdiz, D., Bastien, N., Drobetsky, E. A., and Sage, E. UVA-induced cyclobutane pyrimidine dimers form predominantly at thymine-thymine dipyrimidines and correlate with the mutation spectrum in rodent cells. Nucleic Acids Res., 31: 2786-2794, 2003.
38. Yoon, J. H., Smith, L. E., Feng, Z., Tang, M., Lee, C. S., and Pfeifer, G. P. Methylated CpG dinucleotides are the preferential targets for G-to-T transversion mutations induced by benzo[a]pyrene diol epoxide in mammalian cells: similarities with the p53 mutation spectrum in smoking-associated lung cancers. Cancer Res., 61: 7110-7117, 2001.
39. Kozack, R. E., and Loechler, E. L. Molecular modeling of the conformational complexity of (+)-anti-B[a]PDE-adducted DNA using simulated annealing. Carcinogenesis (Lond.), 18: 1585-1593, 1997.
40. Shukla, R., Liu, T., Geacintov, N. E., and Loechler, E. L. The major N2-dG adduct of (+)-anti-B[a]PDE shows a dramatically different mutagenic specificity (predominantly, G → A) in a 5′-CGT-3′ sequence context. Biochemistry, 36: 10256-10261, 1997.
41. Kozack, R. E., and Loechler, E. L. Molecular modeling of the major adduct of (+)-anti-B[a]PDE (N2-dG) in the eight conformations and the five DNA sequences most relevant to base substitution mutagenesis. Carcinogenesis (Lond.), 20: 85-94, 1999.
42. Kozack, R. E., Shukla, R., and Loechler, E. L. A hypothesis for what conformation of the major adduct of (+)-anti-B[a]PDE (N2-dG) causes G→T versus G→A mutations based upon a correlation between mutagenesis and molecular modeling results. Carcinogenesis (Lond.), 20: 95-102, 1999.
43. Seo, K. Y., Jelinsky, S. A., and Loechler, E. L. Factors that influence the mutagenic patterns of DNA adducts from chemical carcinogens. Mutat. Res., 463: 215-246, 2000.
44. Li, B., Mao, B., Liu, T. M., Xu, J., Dourandin, A., Amin, S., and Geacintov, N. E. Laser pulse-induced photochemical strand cleavage of site-specifically and covalently modified (+)-anti-benzo[a]pyrene diol epoxide-oligonucleotide adducts. Chem. Res. Toxicol., 8: 396-402, 1995.
45. Routledge, M. N., McLuckie, K. I., Jones, G. D., Farmer, P. B., and Martin, E. A. Presence of benzo[a]pyrene diol epoxide adducts in target DNA leads to an increase in UV-induced DNA single strand breaks and supF gene mutations. Carcinogenesis (Lond.), 22: 1231-1238, 2001.
46. Ohashi, E., Bebenek, K., Matsuda, T., Feaver, W. J., Gerlach, V. L., Friedberg, E. C., Ohmori, H., and Kunkel, T. A. Fidelity and processivity of DNA synthesis by DNA polymerase kappa, the product of the human DINB1 gene. J. Biol. Chem., 275: 39678-39684, 2000.
47. Ohashi, E., Ogi, T., Kusumoto, R., Iwai, S., Masutani, C., Hanaoka, F., and Ohmori, H. Error-prone bypass of certain DNA lesions by the human DNA polymerase kappa. Genes Dev., 14: 1589-1594, 2000.
48. Zhang, Y., Yuan, F., Xin, H., Wu, X., Rajpal, D. K., Yang, D., and Wang, Z. Human DNA polymerase kappa synthesizes DNA with extraordinarily low fidelity. Nucleic Acids Res., 28: 4147-4156, 2000.
49. O-Wang, J., Kawamura, K., Tada, Y., Ohmori, H., Kimura, H., Sakiyama, S., and Tagawa, M. DNA polymerase kappa, implicated in spontaneous and DNA damage-induced mutagenesis, is overexpressed in lung cancer. Cancer Res., 61: 5366-5369, 2001.
50. Ogi, T., Mimura, J., Hikida, M., Fujimoto, H., Fujii-Kuriyama, Y., and Ohmori, H. Expression of human and mouse genes encoding polkappa: testis-specific developmental regulation and AhR-dependent inducible transcription. Genes Cells, 6: 943-953, 2001.
51. Suzuki, N., Ohashi, E., Kolbanovskiy, A., Geacintov, N. E., Grollman, A. P., Ohmori, H., and Shibutani, S. Translesion synthesis by human DNA polymerase kappa on a DNA template containing a single stereoisomer of dG-(+)- or dG-(-)-anti-N(2)-BPDE (7, 8-dihydroxy-anti-9, 10-epoxy-7, 8, 9, 10-tetrahydrobenzo[a]pyrene). Biochemistry, 41: 6100-6106, 2002.
52. Ogi, T., Shinkai, Y., Tanaka, K., and Ohmori, H. Polkappa protects mammalian cells against the lethal and mutagenic effects of benzo[a]pyrene. Proc. Natl. Acad. Sci. USA, 99: 15548-15553, 2002.
53. Matsuda, T., Bebenek, K., Masutani, C., Hanaoka, F., and Kunkel, T. A. Low fidelity DNA synthesis by human DNA polymerase-eta. Nature (Lond.), 404: 1011-1013, 2000.
54. Masutani, C., Araki, M., Yamada, A., Kusumoto, R., Nogimori, T., Maekawa, T., Iwai, S., and Hanaoka, F. Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J., 18: 3491-3501, 1999.
55. Johnson, R. E., Washington, M. T., Prakash, S., and Prakash, L. Fidelity of human DNA polymerase eta. J. Biol. Chem., 275: 7447-7450, 2000.
56. Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K., and Hanaoka, F. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature (Lond.), 399: 700-704, 1999.
57. Johnson, R. E., Kondratick, C. M., Prakash, S., and Prakash, L. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science (Wash. DC), 285: 263-265, 1999.
58. Chiapperino, D., Kroth, H., Kramarczuk, I. H., Sayer, J. M., Masutani, C., Hanaoka, F., Jerina, D. M., and Cheh, A. M. Preferential misincorporation of purine nucleotides by human DNA polymerase eta opposite benzo[a]pyrene 7, 8-diol 9, 10-epoxide deoxyguanosine adducts. J. Biol. Chem., 277: 11765-11771, 2002.
59. Zhang, Y., Wu, X., Guo, D., Rechkoblit, O., and Wang, Z. Activities of human DNA polymerase kappa in response to the major benzo[a]pyrene DNA adduct: error-free lesion bypass and extension synthesis from opposite the lesion. DNA Repair (Amst.), 1: 559-569, 2002.
60. Stary, A., Kannouche, P., Lehmann, A. R., and Sarasin, A. Role of DNA polymerase eta in the UV mutation spectrum in human cells. J. Biol. Chem., 278: 18767-18775, 2003.
61. Friedberg, E. C. How nucleotide excision repair protects against cancer. Nat. Rev. Cancer, 1: 22-33, 2001.
62. Batty, D. P., and Wood, R. D. Damage recognition in nucleotide excision repair of DNA. Gene, 241: 193-204, 2000.
63. van Steeg, H., de Vries, A., van Oostrom, C., van Benthem, J., Beems, R. B., and van Kreijl, C. F. DNA repair-deficient Xpa and Xpa/p53+/- knock-out mice: nature of the models. Toxicol. Pathol., 29(Suppl): 109-116, 2001.
64. Geacintov, N. E., Broyde, S., Buterin, T., Naegeli, H., Wu, M., Yan, S., and Patel, D. J. Thermodynamic and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery. Biopolymers, 65: 202-210, 2002.
65. Sarasin, A. The molecular pathways of ultraviolet-induced carcinogenesis. Mutat. Res., 428: 5-10, 1999.
66. Conney, A. H., Chang, R. L., Cui, X. X., Schiltz, M., Yagi, H., Jerina, D. M., and Wei, S. J. Dose-dependent differences in the profile of mutations induced by carcinogenic (R, S, S, R) bay- and fjord-region diol epoxides of polycyclic aromatic hydrocarbons. Adv. Exp. Med. Biol., 500: 697-707, 2001.
67. Shyong, E. Q., Lu, Y., Goldstein, A., Lebwohl, M., and Wei, H. Synergistic enhancement of H2O2 production in human epidermoid carcinoma cells by Benzo[a]pyrene and ultraviolet A radiation. Toxicol. Appl. Pharmacol., 188: 104-109, 2003.
68. You, Y. H., Lee, D. H., Yoon, J. H., Nakajima, S., Yasui, A., and Pfeifer, G. P. Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells. J. Biol. Chem., 276: 44688-44694, 2001.
69. You, Y. H., Li, C., and Pfeifer, G. P. Involvement of 5-methylcytosine in sunlight-induced mutagenesis. J. Mol. Biol., 293: 493-503, 1999.