Synthesis and characterization of polycyclic aromatic hydrocarbon o- quinone depurinating N7-guanine adducts

Chemical Research in Toxicology

Volumn 12, Issue 3, 1999, Pages 237-246

  McCoull, Kirsten D ^a   Rindgen, Diane ^a   Blair, Ian A ^a   Penning, Trevor ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 7,8 DIHYDROXYBENZO[A]PYRENE; CATECHOL DERIVATIVE; DEOXYGUANOSINE; DIHYDRODIOL DEHYDROGENASE; DNA; GLYCOSIDE; GUANINE DERIVATIVE; NAPHTHALENE DERIVATIVE; PHENANTHRENE DERIVATIVE; POLYCYCLIC AROMATIC HYDROCARBON; QUINONE DERIVATIVE;

APURINIC SITE; ARTICLE; CELL TRANSFORMATION; CHEMICAL CARCINOGENESIS; CHEMICAL MUTAGENESIS; DNA ADDUCT; MASS SPECTROMETRY; NUCLEIC ACID BASE SUBSTITUTION; POLLUTANT; PROTON NUCLEAR MAGNETIC RESONANCE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SYNTHESIS; ULTRAVIOLET SPECTROSCOPY;

ANIMALS; BENZOPYRENES; CATTLE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DEOXYGUANOSINE; DNA ADDUCTS; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; NAPHTHALENES; PHENANTHRENES; SPECTROPHOTOMETRY, ULTRAVIOLET;

DION;

EID: 0033024560     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx980182z     Document Type: Article

References (40)

1. Dipple, A. (1985) Polycyclic aromatic hydrocarbon carcinogenesis: an introduction. In Polycyclic Hydrocarbons and Carcinogenesis (Harvey, R. G., Ed.) pp 1-17, ACS Symposium Series 283, American Chemical Society, Washington, DC.
2. Tabin, C. J., Bradley, S. M., Bargmann, C. I., Weinberg, R. A., Papageorge, A. G., Scolnick, E. M., Dhar, R., Lowy, D. R., and Chang, E. H. (1982) Mechanism of activation of a human oncogene. Nature 300, 143-149.
3. Reddy, E. P., Reynolds, R. K., Santos, E., and Barbacid, M. (1982) A point mutation is responsible for the acquisition of transforming properties by the T24 human bladder carcinoma oncogene. Nature 300, 149-152.
4. Hollstein, M., Sidransky, D., Vogelstein, B., and Harris, C. C. (1991) p53 Mutations in human cancers. Science 253, 49-53.
5. Denissenko, M. F., Pao, A., Tang, M., and Pfeifer, G. P. (1996) Preferential formation of benzo[α]pyrene adducts at lung cancer mutational hotspots in p53. Science 274, 430-432.
6. Thakker, D. R., Yagi, H., Lu, A. Y. H., Levin, W., Conney, A. H., and Jerina, D. M. (1976) Metabolism of benzo[α]pyrene: Conversion of (±)-trans-7,8-dihydroxy-7,8-dihydrobenzo[α]pyrene to highly mutagenic 7,8-diol-9,10-epoxides. Proc. Natl. Acad. Sci. U.S.A. 73, 3381-3385.
7. Jeffrey, A. M., Jennette, K. W., Blobstein, S. H., Weinstein, I. B., Beland, F. A., Harvey, R. G., Kasai, H., Miura, I., and Nakanishi, K. (1976) Benzo[α]pyrene-nucleic acid derivative found in vivo: structure of a benzo[α]pyrenetetrahydrodiol epoxide-guanosine adduct. J. Am. Chem. Soc. 98, 5714-5715.
8. Marshall, C. J., Vousden, K. H., and Phillips, D. H. (1984) Activation of c-Ha-ras-1 proto-oncogene by in vitro modification with a chemical carcinogen, benzo[α]pyrene diol-epoxide. Nature 310, 586-589.
9. Shibutani, S., Margulis, L. A., Geacintov, N. E., and Grollman, A. P. (1993) Translesional synthesis on a DNA template containing a single stereoisomer of dG-(+)- or dG-(-)-anti-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10-tetrahydrobenzo[α]pyrene). Biochemistry 32, 7531-7541.
10. Cavalieri, E. L., and Rogan, E. G. (1992) The approach to understanding aromatic hydrocarbon carcinogenesis. The central role of radical cations in metabolic activation. Pharmacol. Ther. 55, 183-199.
11. Devanesan, P. D., RamaKrishna, N. V. S., Todorovic, R., Rogan, E. G., Cavalieri, E. L., Jeong, H., Jankowiak, R., and Small, G. J. (1992) Identification and quantitation of benzo[α]pyrene-DNA adducts formed by rat liver microsomes in vitro. Chem. Res. Toxicol. 5, 302-309.
12. Chakravarti, D., Pelling, J. C., Cavalieri, E. L., and Rogan, E. G. (1995) Relating aromatic hydrocarbon-induced DNA adducts and c-H-ras mutations in mouse skin papillomas. Proc. Natl. Acad. Sci. U.S.A. 92, 10422-10426.
13. Sagher, D., and Strauss, B. (1983) Insertion of nucleotides opposite apurinic/apyrimidinic sites in deoxyribonucleic acid during in vitro synthesis: uniqueness of adenine nucleotides. Biochemistry 22, 4518-4526.
14. Smithgall, T. E., Harvey, R. G., and Penning, T. M. (1986) Regio-and stereospecificity of homogeneous 3α-hydroxysteroid-dihydrodiol dehydrogenase for trans-dihydrodiol metabolites of polycyclic aromatic hydrocarbons. J. Biol. Chem. 261, 6184-6191.
15. Smithgall, T. E., Harvey, R. G., and Penning, T. M. (1988) Spectroscopic identification of ortho-quinones as the products of polycyclic aromatic trans-dihydrodiol oxidation catalyzed by dihydrodiol dehydrogenase. J. Biol. Chem. 263, 1814-1820.
16. Burczynski, M. E., Harvey, R. G., and Penning, T. M. (1998) Expression and characterization of four recombinant human dihydrodiol dehydrogenase isoforms: oxidation of trans-7,8-dihydroxy-7,8-dihydrobenzo[α]pyrene to the activated o-quinone metabolite benzo[α]pyrene-7,8-dione. Biochemistry 37, 6781-6790.
17. Flowers-Geary, L., Harvey, R. G., and Penning, T. M. (1995) Identification of benzo[α]pyrene-7,8-dione as an authentic metabolite of (±)-trans-7,8-dihydroxy-7,8-dihydrobenzo[α]pyrene in isolated rat hepatocytes. Carcinogenesis 16, 2707-2715.
18. Shou, M., Harvey, R. G., and Penning, T. M. (1993) Reactivity of benzo[α]pyrene-7,8-dione with DNA. Evidence for the formation of deoxyguanosine adducts. Carcinogenesis 14, 475-482.
19. Flowers, L., Ohnishi, S. T., and Penning, T. M. (1997) 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.
20. Flowers, L., Bleczinski, W. F., Burczynski, M. E., Harvey, R. G., and Penning, T. M. (1996) Disposition and biological activity of benzo[α]pyrene-7,8-dione. A genotoxic metabolite generated by dihydrodiol dehydrogenase. Biochemistry 35, 13664-13672.
21. Breen, A. P., and Murphy, J. A. (1995) Reactions of oxyl radicals with DNA. Free Radical Biol. Med. 18, 1033-1077.
22. Stack, D. E., Byun, J., Gross, M. L., Rogan, E. G., and Cavalieri, E. L. (1996) Molecular characteristics of catechol estrogen quinones in reactions with deoxyribonucleosides. Chem. Res. Toxicol. 9, 851-859.
23. Cavalieri, E. L., Stack, D. E., Devanesan, P. D., Todorovic, R., Dwivedy, I., Higginbotham, S., Johansson, S. L., Patil, K. D., Gross, M. L., Gooden, J. K., Ramanathan, R., Cerny, R. L., and Rogan, E. G. (1997) Molecular origin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. U.S.A. 94, 10937-10942.
24. Fieser, L. F. (1943) 1,2-Naphthoquinone. Organic Syntheses, Collect. Vol. 2, pp 430-432, Wiley, New York.
25. Platt, K. L., and Oesch, F. (1982) Synthesis of non-K-region ortho-quinones of polycyclic aromatic hydrocarbons from cyclic ketones. Tetrahedron Lett. 23, 163-166.
26. Sukumaran, K. B., and Harvey, R. G. (1980) Synthesis of the o-quinones and dihydrodiols of polycyclic aromatic hydrocarbons from the corresponding phenols. J. Org. Chem. 45, 4407-4413.
27. Zeller, K.-P. (1974) Mass spectra of quinones. In The Chemistry of the Quinonoid Compounds (Patai, S., Ed.) pp 231-256, Wiley, New York.
28. Kim, H. S., Yu, M., Jiang, Q., and LeBreton, P. R. (1993) UV photoelectron and ab initio quantum mechanical characterization of 2′-deoxyguanosine 5′-phosphate: electronic influences on DNA alkylation patterns. J. Am. Chem. Soc. 115, 6169-6183.
29. Murty, V. S., and Penning, T. M. (1992) Characterization of mercapturic acid and glutathionyl conjugates of benzo[α]pyrene-7,8-dione by two-dimensional NMR. Bioconjugate Chem. 3, 218-224.
30. Citti, L., Gervasi, P. G., Turchi, G., Bellucci, G., and Bianchini, R. (1984) The reaction of 3,4-epoxy-1-butene with deoxyguanosine and DNA in vitro: synthesis and characterization of the main adducts. Carcinogenesis 5, 47-52.
31. Zoltewicz, J. A., Clark, D. F., Sharpless, T. W., and Grahe, G. (1970) Kinetics and mechanism of the acid-catalyzed hydrolysis of some purine nucleosides. J. Am. Chem. Soc. 92, 1741-1750.
32. Rogan, E. G., Cavalieri, E. L., Tibbels, S. R., Cremonesi, P., Warner, C. D., Nagel, D. L., Tomer, K. B., Cerny, R. L., and Gross, M. L. (1988) Synthesis and identification of benzo[α]pyrene-guanine nucleoside adducts formed by electrochemical oxidation and by horseradish peroxidase catalyzed reaction of benzo[α]-pyrene with DNA. J. Am. Chem. Soc. 110, 4023-4029.
33. RamaKrishna, N. V. S., Gao, F., Padmavathi, N. S., Cavalieri, E. L., Rogan, E. G., Cerny, R. L., and Gross, M. L. (1992) Model adducts of benzo[α]pyrene and nucleosides formed from its radical cation and diol epoxide. Chem. Res. Toxicol. 5, 293-302.
34. RamaKrishna, N. V. S., Padmavathi, N. S., Cavalieri, E. L., Rogan, E. G., Cerny, R. L., and Gross, M. L. (1993) Synthesis and structure determination of the adducts formed by electrochemical oxidation of the potent carcinogen dibenzo[α,l]pyrene in the presence of nucleosides. Chem. Res. Toxicol. 6, 554-560.
35. Monks, T. J., Hanzlik, R. P., Cohen, G. M., Ross, D., and Graham, D. G. (1992) Quinone chemistry and toxicity. Toxicol. Appl. Pharmacol. 112, 2-16.
36. Murty, V. S., and Penning, T. M. (1992) Polycyclic aromatic hydrocarbon (PAH) ortho-quinone conjugate chemistry: kinetics of thiol addition to PAH ortho-quinones and structures of thio-ether adducts of naphthalene-1,2-dione. Chem.-Biol. Interact. 84, 169-188.
37. Akanni, A., and Abul-Hajj, Y. J. (1997) Estrogen-nucleic acid adducts: reaction of 3,4-estrone-o-quinone radical anion with deoxyribonucleosides. Chem. Res. Toxicol. 10, 760-766.
38. Shen, L., Qiu, S., van Breemen, R. B., Zhang, F., Chen, Y., and Bolton, J. L. (1997) Reaction of the Premarin metabolite 4-hydroxyequilenin semiquinone radical with 2′-deoxyguanosine: formation of unusual cyclic adducts. J. Am. Chem. Soc. 119, 11126-11127.
39. Shen, L., Qiu, S., Chen, Y., Zhang, F., van Breemen, R. B., Nikolic, D., and Bolton, J. L. (1998) Alkylation of 2′-deoxynucleosides and DNA by the Premarin metabolite 4-hydroxyequilenin semiquinone radical. Chem. Res. Toxicol. 11, 94-101.
40. Tsuruda, L., Hou, Y.-T., and Penning, T. (1999) Stable transfection of dihydrodiol dehydrogenase in MCF-7 breast carcinoma cells promotes polycyclic aromatic hydrocarbon o-quinone formation which leads to cell death. Polycyclic Aromat. Compd. (in press).