Genotoxic polycyclic aromatic hydrocarbon ortho-quinones generated by aldo-keto reductases induce CYP1A1 via nuclear translocation of the aryl hydrocarbon receptor

Cancer Research

Volumn 60, Issue 4, 2000, Pages 908-915

  Burczynski, Michael E ^a   Penning, Trevor M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 7,8 DIHYDROXYBENZO[A]PYRENE; AROMATIC HYDROCARBON RECEPTOR; ETHOXYRESORUFIN DEETHYLASE; MEDROXYPROGESTERONE ACETATE; OXIDOREDUCTASE; POLYCYCLIC AROMATIC HYDROCARBON; QUINONE DERIVATIVE; URSODEOXYCHOLIC ACID;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME LOCALIZATION; ENZYME METABOLISM; GENE EXPRESSION; GENE TRANSLOCATION; GENETIC TRANSFECTION; GENOTOXICITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; TRANSCRIPTION INITIATION;

ALCOHOL OXIDOREDUCTASES; BENZO(A)PYRENE; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CYTOCHROME P-450 CYP1A1; ENZYME INDUCTION; HUMANS; QUINONES; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN; TRANS-ACTIVATION (GENETICS); TUMOR CELLS, CULTURED;

EID: 0034652743     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Gelboin, H. V. Benzo[a]pyrene metabolism, activation and carcinogenesis: role and regulation of mixed function oxidases and related enzymes. Physiol. Rev., 60: 1107-1166, 1980.
2. Conney, A. H. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons. G. H. A. Clowes Memorial Lecture. Cancer Res., 42: 4875-4917, 1982.
3. Dipple, A. Polycyclic aromatic hydrocarbon carcinogenesis: Introduction. In: R. G. Harvey (ed.), Polycyclic Aromatic Carcinogenesis, pp. 1-17. ACS Symposium Series, Vol. 283. Washington, D.C., American Chemical Society, 1985.
4. Yang, S. K., McCourt, D. W., Roller, P. P., and Gelboin, H. V. Enzymatic conversion of benzo[a]pyrene leading predominantly to the diol-epoxide r-7,t-8-dihydroxy-t-9,10-oxy-7,8,9,10-tetrahydrobenzo[a]pyrene through a single enantiomer of r-7,t-8-dihydroxy-7,8-dihydrobenzo[a]pyrene. Proc. Natl. Acad. Sci. USA, 73: 2594-2598, 1976.
5. Thakker, D. R., Yagi, H., Lu, A. Y. H., Levin, W., Conney, A. H., and Jerina, D. M. Metabolism of benzo[a]pyrene: conversion of (±)-trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene to highly mutagenic 7,8-diol-9,10-epoxides. Proc. Natl. Acad. Sci. USA, 73: 3381-3385, 1976.
6. Hernandez, O., and Bend, J. R. Metabolism of epoxides. In: W. B. Jakoby (ed.), Metabolic Basis of Detoxication, pp. 207-228, New York: Academic Press, 1982.
7. Marshall, C. J., Vousden, K. H., and Phillips, D. H. Activation of c-Ha-ras-1 proto-oncogene by in vitro chemical modification with a chemical carcinogen, benzo[a]pyrene diol epoxide. Nature. (Lond.) 310: 585-589, 1984.
8. Denissenko, M. F., Pao, A., Tang, M. S., and Pfieifer, G. P. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in p53. Science (Washington DC), 274: 430-432, 1996.
9. Hruszkewicz, A. M., Canella, K. A., Peltonen, K., Lotrappa, L., and Dipple, A. DNA polymerase action on benzo[a]pyrene-DNA adducts. Carcinogenesis (Lond.), 13: 2347-2352, 1992.
10. Vousden, K. H., Bos, J. L., Marshall, C. J., and Phillips, D. H. Mutations activating c-Ha-ras1 protooncogene (HRASI) induced by chemical carcinogenesis and depurination. Proc. Natl. Acad. Sci. USA, 83: 1222-1226, 1986.
11. Smithgall, T. E., Harvey, R. G., and Penning, T. M. Regio-and stereospecificity of homogeneous 3α-hydroxysteroid-dihydrodiol dehydrogenase for trans-dihydrodiol metabolites of polycyclic aromatic hydrocarbons. J. Biol. Chem., 261: 6184-6191. 1986.
12. Burczynski, M. E., Harvey, R. G., and Penning, T. M. Expression and characterization of four recombinant human dihydrodiol dehydrogenase isoforms: oxidation of trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene to the activated o-quinone metabolite benzo[a]pyrene-7,8-dione. Biochemistry, 37: 6781-6790, 1998.
13. Smithgall, T. E., Harvey, R. G., and Penning, T. M. Spectroscopic identification of ortho-quinones as the products of polycyclic aromatic trans-dihydrodiol oxidation catalyzed by dihydrodiol dehydrogenase. J. Biol. Chem., 263: 1814-1820, 1988.
14. Jez, J. M., Flynn, T. G., and Penning, T. M. A new nomenclature system for the aldo-keto reductase superfamily. Biochem. Pharmacol., 54: 639-647, 1997.
15. Penning, T. M., Ohnishi, S. T., Ohnishi, T., and Harvey, R. G. Generation of reactive oxygen species during the enzymatic oxidation of polycyclic aromatic hydrocarbon trans-dihydrodiols catalyzed by dihydrodiol dehydrogenase. Chem. Res. Toxicol., 9: 84-92, 1996.
16. Flowers-Geary, L., Bleczinski, W., Harvey, R. G., and Penning, T. M. Cytotoxicity and mutagenicity of polycyclic aromatic hydrocarbon o-quinones produced by dihydrodiol dehydrogenase. Chem. Biol. Interact., 99: 55-72, 1996.
17. Flowers, L., Bleczinski, W. F., Burczynski, M. E., Harvey, R. G., and Penning, T. M. Disposition and biological activity of benzo[a]pyrene-7,8-dione. A genotoxic metabolite generated by dihydrodiol dehydrogenase. Biochemistry, 35: 13664-13672, 1996.
18. Shou, M., Harvey, R. G., and Penning, T. M. Reactivity of benzo[a]pyrene-7,8-dione with DNA. Evidence for the formation of deoxyguanosine adducts. Carcinogenesis (Lond.), 14: 475-482, 1993.
19. McCoull, K. D., Rindgen, D., Blair, I. A., and Penning, T. M. Synthesis and characterization of depurinating adducts of polycylic aromatic hydrocarbon o-quinones. Chem. Res. Toxicol., 12: 237-246, 1999
20. Flowers, L., Ohnishi, S. T., and Penning, T. M. DNA strand scission by polycyclic aromatic hydrocarbon o-quinones: role of reactive oxygen species, Cu(II)/Cu(I) redox cycling and o-semiquinone anion radicals. Biochemistry, 36: 8640-8648, 1997.
21. Prochaska, H. J., De Long, M. J., and Talalay, P. On the mechanism of induction of cancer protective enzymes: a unifying proposal. Proc. Natl. Acad. Sci. USA, 82: 8232-8236, 1985.
22. Okey, A. B., Riddick, D. S., and Harper, P. A. Molecular biology of the aromatic hydrocarbon (dioxin) receptor. Trends Pharmacol, Sci., 15: 226-232, 1994.
23. Hankinson, O. The aryl hydrocarbon receptor complex. Annu Rev. Pharmacol. Toxicol., 35: 307-340, 1995.
24. Whitlock, J. P., Jr., Okino, S. T., Dong, L., Ko, H. P., Clarke-Katzenberg, R., Ma. Q., and Li, H. Induction of cytochrome P4501A1: a model for analyzing mammalian gene transcription. FASEB J., 10: 809-818, 1996.
25. Talalay, P., De Long, M. J., and Prochaska, H. J. Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis. Proc. Natl. Acad. Sci. USA, 85: 8261-8265, 1988.
26. Rushmore, T. H.; Morton, M. R., and Pickett, C. B. The antioxidant responsive-element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem., 266: 11632-11639, 1991.
27. Venugopal, R., and Jaiswal, A. K. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene, 17: 31-45-3156, 1998.
28. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., Yamamoto, M. and Nabeshima, Y. An Nrf2/small Mat heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun., 236: 313-322, 1997.
29. Hayes, J. D., and Pullford, D. J. The glutathione-S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol., 30: 445-600, 1995.
30. Burezynski, M. E., Lin, H K., and Penning, T. M. Isoform-specific induction of a human aldo-keto reductase by polycyclic aromatic hydrocarbons (PAHs), electrophiles and ovidative stress: implications for the alternative pathway of PAH activation catalyzed by human dihydrodiol dehydrogenase. Cancer Res., 59: 607-614, 1999.
31. Fieser, L. F. β-Napthoquinone and α-napthoquinone. Org. Synth., 2: 430-435, 1943
32. Sukumaran K. B., and Harvey, R. G. Synthesis of the o-quinones and dihydrodiols of polycyclic aromatic hydrocarbons from the corresponding phenols. J. Org. Chem., 45: 4407-4413, 1980.
33. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. Current Protocols in Molecular Biology. New York: Wiley, 1989.
34. Kress, S., and Greenlee, W. F. Cell-specific regulation of human CYPIA1 and CYPIB1 genes. Cancer Res., 57: 1265-1269, 1997.
35. Riddick, D. S., Huang, Y., Harper, P. A., and Okey, A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin versus 3-methylcholanthrene: comparative studies of Ah receptor binding, transformation, and induction of CYPIA1. J. Biol. Chem., 269: 12118-12128, 1994.
36. Postlind, H., Vu, T. P. Tukey, R. H., and Quattrochi, L. C. Response of human CYPI-luciferase plasmids to 2,3,7,8-tetrachlorodibenzo-p-dioxin and polycyclic aromatic hydrocarbons. Toxicol. Appl. Pharmacol., 118: 255-262, 1993.
37. Glusker, J. P. X-ray analyses of polycyclic hydrocarbon metabolite structures. In: R G. Harvey (ed.), Polycyclic Hydrocarbons and Carcinogenesis, pp. 125-185, ACS Symposium Series, Vol. 283. Washington, D.C.: American Chemical Society, 1985.
38. Pollenz, R. S. The aryl hydrocarbon receptor, but not the aryl hydrocarbon receptor nuclear translocator protein, is rapidly depleted in hepatic and nonhepatic culture cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Mol. Pharmacol., 49: 391-398, 1996.
39. Giannone, J. V., Li, W., Probst, M., and Okey, A. Prolonged depletion of AH receptor without alteration of receptor mRNA levels alter treatment of cells in culture with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem. Pharmacol., 55: 489-497, 1998.
40. Wacker, W. K. C., and Vallee, B. L. Nucleic acids and metals. J. Biol. Chem., 211: 3257-3262, 1959
41. Prutz, W. A., Butler, J., and Land, B. J. lnteraction of Cu(I) with nucleic acids. Int. J. Radiat. Biol., 58: 215-234, 1990.
42. Leadon, S. A., Stampfer, M. R., and Bartley, J. Production of oxidative DNA damage during the metabolic activation of benzo[a]pyrene in human mammary epithelial cells correlates with cell killing. Proc. Natl. Acad. Sci. USA, 85: 4345-4368, 1988.
43. Kim, K. B., and Lee, B. M. Oxidative stress to DNA, protein and antioxidant enzymes (superoxide dismutase and catalase) in rats treated with benzo[a]pyrene. Cancer Lett., 113: 205-212, 1997.
44. Cerutti, P.A. Prooxidant states and tumor promotion. Science (Washington DC), 227: 375-381, 1985.
45. Shu, H. P., Paustenbach, D. J., and Murray, F. J. A critical evaluation of the use of mutagenesis, carcinogenesis, and tumor promotion data in a cancer risk assessment of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Regul. Toxicol. Pharmacol., 7: 57-88, 1987.
46. Birnbaum, L. S. The mechanism of dioxin toxicity: relationship to risk assessment. Environ Health. Perspect., 102: 157-167, 1994.
47. Whysner, J., and Williams, G. M. 2,3,7,8-Tetrachlordibenzo-p-dioxin mechanistic data and risk assessment: gene regulation, cytotoxicity, enhanced cellular proliferation, and tumor promotion. Pharmacol. Ther., 71: 193-223, 1996.
48. Tritscher, A. M., Goldstein, J. A., Portier, C. J., McCoy, Z., Clark, G. C., and Lucier, G. W. Dose-response relationships for chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin in a rat tumor promotion model: quantification and immunolocalization of CYPIA1 and CYPIA2 in the liver. Cancer Res., 52: 3436-3442, 1992.