Identification of benzo[a]pyrene-7,8-dione as an authentic metabolite of (±)-trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene in isolated rat hepatocytes

Carcinogenesis

Volumn 16, Issue 11, 1995, Pages 2707-2715

  Flowers geary, Lynn ^a   Harvey, Ronald G ^a,b   Penning, Trevor M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZO[A]PYRENE DERIVATIVE; DIHYDRODIOL DEHYDROGENASE; INDOMETACIN; TRITIUM;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; ISOTOPE LABELING; LIVER CELL; LIVER METABOLISM; MALE; MASS SPECTROMETRY; METABOLITE; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SPECTROSCOPY;

ALCOHOL OXIDOREDUCTASES; ANIMAL; BENZOPYRENES; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIHYDROXYDIHYDROBENZOPYRENES; HAMSTERS; IN VITRO; LIVER; MALE; RATS; RATS, SPRAGUE-DAWLEY; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.;

EID: 0028824573     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/16.11.2707     Document Type: Article

References (35)

1. Jeffrey, A.M., Jennette, K.W., Blobstein, S.H., Weinstein, I.B., Beland, F.A., Harvey, R.G., Kasai, H., Miura, J. and Nakanishi, K. (1976) Benzo[α]pyrene-nucleic acid derivative found in vivo: Structure of a benzo[a]pyrene-tetrahydrodiol epoxide-guanosine adduct. J. Am. Chem. Soc., 98, 5714-5715.
2. Jeffrey, A.M., Weinstein, I.B., Jennette, K.W., Grzeskowiak, K., Nakanishi, K., Harvey, R.G., Autrup, H. and Harris, C. (1977) Structures of benzo[a]pyrene-nucleic acid adducts formed in human and bovine bronchial explants. Nature, 269, 348-350.
3. Koreeda, M., Moore, P.D., Wislocki, P.G., Levin, W., Conney, A.H., Yagi, H. and Jerina, D.M. (1978) Binding of benzo[a]pyiene-7, 8-diol-9, 10-epoxides to DNA, RNA and protein of mouse skin occurs with high stereoselectivity. Science, 199, 778-780.
4. Newbold, R.F. and Brookes, P. (1976) Exceptional mutagenicity of a benzo[a]pyrene diol epoxide in cultured mammalian cells. Nature, 261, 52-54.
5. Kapitulnik J., Wislocki, P.G., Levin, W., Yagi, H., Jerina, D.M. and Conney, A.H. (1978) Tumorigemcity studies with diol epoxides of benzo[a]pyrene which indicate that (±)-tranr-7β, 8α-dihydroxy-9α, 10α- cpoxy-7, 8, 9, 10-tctrahydrabenzo[a] pyrcne is an ultimate carcinogen in newborn mice. Cancer Res., 38, 354-358.
6. Cavalieri, E., Roth, R. and Rogan, E. (1976) Metabolic activation of aromatic hydrocarbons by one-electron oxidation in relation to the mechanism of tumor initiation. In Freudenthal, R.I. and Jones, P.W. (eds), Polynuclear Aromatic Hydrocarbons: Chemistry, Metabolism and Carcinogenesis. Raven Press, New York, vol. 1, pp. 181-190.
7. Cavalieri, E.L. and Rogan, E.G. (1992) The approach to understanding aromatic hydrocarbon carcinogenesis. The central role of radical cations in metabolic activation. Pharmac. Ther., 55, 183-199.
8. Cavalieri, E.L., Higginbotham, S., RamaKnshna, N.V.S., Devanesan, P.D., Todorovic, R., Rogan, E.G. and Salmasi, S. (1991) Comparative dose-response tumongenicity studies of dibenzo[a, l]pyrene versus 7, 12-dimethylbenz[a]anthracene, benzo[a]pyrene and two dibenzo[a, l]pyrene dihydrodiols in mouse skin and rat mammary gland. Carcinogenesis, 12, 1939-1944.
9. Cavalieri, E.L., Rogan, E.G., Higginbotham, S., Cremonesi, P. and Salmasi, S. (1989) Tumor-initiating activity in mouse skin and carcinogenicity in rat mammary gland of dibenzo[a, l]pyrenes: The very potent environmental carcinogen dibenzo[a, l] pyrene. J. Cancer Res. Clin. Oncol., 115, 67-72.
10. Smithgall, T.E., Harvey, R.G. and Penning, T.M. (1986) Regio- and stereospecificity of homogeneous 3a-hydroxysteroid-dihydrodiol dehydrogenase for rranr-dihydrodiol metabolites of polycyclic aromatic hydrocarbons. J. Biol. Chem., 261, 6184-6191.
11. Smithgall, T.E., Harvey, R.G. and Penning, T.M. (1988) Spectroscopic identification of ordioquinones as the products of polycyclic aromatic /rans-dihydrodiol oxidation catalyzed by dihydrodiol dehydrogenase. A potential route of proximate carcinogen metabolism. J. Biol. Chem., 263, 1814-1820.
12. Shou, M., Harvey, R.G. and Penning, T.M. (1992) Contribution of dihydrodiol dehydrogenase to the metabolism of (±)-rrans-7, 8-dihydroxy-7, 8-dihydrobenzo[a]pyrene in fortified rat liver subcellular fractions. Carcinogenesis, 13, 1575-1582.
13. Klein, J., Seidel, A., Frank, H., Oesch, F. and Platt, K.L. (1991) Regiospecific oxidation of polycyclic aromatic dihydrodiols by rat liver dihydrodiol dehydrogenase. Chem.-Biol. Inter., 79, 287-303.
14. Penning, T.M., Ohnishi, S.T., Ohnishi, T. and Harvey, R.G. (1996) Generation of reactive oxygen species during the oxidation of PAH rrans-dihydrodiols catalyzed by dihydrodiol dehydrogenase. Chem. Res. Toxicol., In press.
15. Flowers-Geary, L., Harvey, R G. and Penning, T.M. (1992) Examination of polycyclic aromatic hydrocarbon o-quinones produced by dihydrodiol dehydrogenase as substrates for redox-cycling in rat liver. Biochem. (Life Sci. Adv.), 11, 49-58.
16. Flowers-Geary, L., Harvey, R.G. and Penning, T.M. (1993) Cytotoxicity of polycyclic aromatic hydrocarbon o-quinones in rat and human hepatoma cells. Chem. Res. Toxicol., 6, 252-260.
17. Flowers-Geary, L., Bleczinski, W., Harvey, R.G. and Penning, T.M. (1995) Cytotoxicity and mutagenicity of polycyclic aromatic hydrocarbon o-quinones produced by dihydrodiol dehydrogenase. Chem-Biol. Inter, In press.
18. Flowers-Geary, L. and Penning, T.M. (1994) Benzo[o]pyrene-7, 8-dione as an activated metabolite of (±)-tran.v-7, 8-dihydroxy-7, 8-dihydrobenzo-|a]pyrene. Proc. Am. Assoc. Cancer Res., 35, A793.
19. Shou, M., Harvey, R.G. and Penning, T.M. (1993) Reactivity of benzo[o]pyrene-7, 8-dione with DNA. Evidence for the formation of deoxyguanosine adducts. Carcinogenesis, 14, 475-482.
20. Fu, P.P. and Harvey, R.G. (1977) Synthesis of the diols and diolepoxides of carcinogenic hydrocarbons. Tetrahedron Lett., 24, 2059-2062.
21. Sukumaran, K.B. and Harvey, R.G. (1980) Synthesis of o-quinones and dihydrodiols of polycyclic aromatic hydrocarbons from the corresponding phenols. J. Org. Chem., 45, 4407-4413.
22. Smithgall, T.E. and Penning, T.M. (1985) Sex differences in indomethacin sensitive 3a-hydroxysteroid dehydrogenase of rat liver cytosol. Cancer Res., 45, 4946-4949.
23. Baird, W.M. and Diamond, L. (1976) Effect of 7, 8-benzoflavone on the formation of benzo[a|pyrene-DNA-bound products in hamster embryo cells. Chem.-Biol. Interact., 13, 67-75.
24. Seglen, P.O. (1976) Preparation of isolated rat liver cells. Methods Cell Biol., 13, 29-83.
25. Failla, M L. and Cousins, RJ. (1978) Zinc uptake by isolated rat liver parenchymal cells. Biochim Biophys. Acta, 538, 435-444.
26. Ivins, J.K. and Penning, T.M. (1987) Radiochemical detection of dihydrodiol dehydrogenase: Distribution of die enzyme in male Sprague-Dawley rat tissues and its sensitivity to inhibition by indomethacin and 6-medroxyprogesterone acetate. Cancer Res., 47, 680-684.
27. Buller, A.L., Sharp, R.B. and Penning, T.M. (1989) Characterization of dihydrodiol dehydrogenase in rat H-4IIe hepatoma cells. Cancer Res., 49, 6976-6980.
28. Penning, T.M., Sharp, R.B. and Smithgall, T.E. (1989) Non-K-region o-quinones as enzyme-generated inactivators of dihydrodiol dehydrogenase. Biochemistry, 28, 4505-4511.
29. Murty, V.S and Penning, T.M. (1992) Characterization of mercapturic acid and glutathionyl conjugates of benzo[a]pyrene-7, 8-dione by twodimensional NMR. Bioconj. Chem., 3, 218-224.
30. Jones, C.A, Moore, B.P., Cohen, G.M., Fry, J.R. and Bridges, J.W. (1978)Studies on the metabolism and excretion of benzo[a]pyrene in isolated adult rat hepatocytes. Biochem. Pharmacol., 27, 693-702.
31. Burke, M.D., Vadi, H., Jemstrom, B. and Orrenius, S. (1977) Metabolism of benzo[ajpyrene with isolated hepatocytes and the formation and degradation of DNA-binding derivatives J. Biol. Chem., 252, 6424-6431.
32. Lorentzen, RJ., Caspary, W.J., Lesko, S.A. and Ts’o, P.O.P. (1975) The autooxidation of 6-hydroxybenzo[a]pyrene and 6-oxobenzo[a]pyrene radical, reactive metabolites of benzo[a]pyrene. Biochemistry, 14, 3970-3977.
33. Gelboin, H.V. (1980) Benzofajpyrene metabolism, activation, and carcinogenesis: Role and regulation of mixed-function oxidases and related enzymes. Physiol. Rev., 60, 1107-1166
34. Selkirk, J.K., Croy, R.G., Whitlock, J.P. and Gelboin, H.V. (1975) In vitro metabolism of benzo[a]pyrene by human liver microsomes and lymphocytes. Cancer Res., 35, 3651-3655.
35. Yang, S.K., McCourt, D.W., Roller, P.P. and Gelboin, H.V. (1976) Enzymatic conversion of benzo[a]pyrene leading predominantly to the diol-epoxide r-7, t-8-dihydroxy-f-9, 10-oxy-7, 8, 9, 10-tetrahydrobenzo[a]pyrene through a single enantiomer of r-7,(-8-dihydroxy-7, 8-dihydrobcnzo[a]pyrcnc. Proc. Natl Acad. Sci USA, 73, 2594-2598.