The greater reactivity of estradiol-3,4-quinone vs estradiol-2,3-quinone with DNA in the formation of depurinating adducts: Implications for tumor-initiating activity

Chemical Research in Toxicology

Volumn 19, Issue 1, 2006, Pages 164-172

  Zahid, Muhammad ^a   Kohli, Ekta ^a   Saeed, Muhammad ^a   Rogan, Eleanor ^a   Cavalieri, Ercole ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLCHOLANTHRENE; ESTRADIOL; ESTRADIOL 2,3 QUINONE; ESTRADIOL 3,4 QUINONE; LACTOPEROXIDASE; MONOPHENOL MONOOXYGENASE; PROSTAGLANDIN SYNTHASE; QUINONE DERIVATIVE; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CANCER RISK; CELL PROLIFERATION; DNA ADDUCT; DNA DETERMINATION; ENZYME ACTIVATION; ENZYME PURIFICATION; HALF LIFE TIME; LIVER MICROSOME; REACTION ANALYSIS;

ADENINE; CARCINOGENS; DEOXYADENOSINES; DNA; DNA ADDUCTS; ESTRADIOL; ESTROGENS, CATECHOL; GUANOSINE; LACTOPEROXIDASE; MONOPHENOL MONOOXYGENASE; MUTAGENS; OXIDATION-REDUCTION; TIME FACTORS;

EID: 31844450313     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx050229y     Document Type: Article

References (42)

1. Liehr, J. G., Fang, W. F., Sirbasku, D. A., and Ari-Ulubelen, A. (1986) Carcinogenicity of catechol estrogens in Syrian hamsters. J. Steroid Biochem. 24, 353-356.
2. Nandi, S. (1978) Role of hormones in mammary neoplasia. Cancer Res. 38, 4046-4049.
3. Li, J. J. (1993) Estrogen carcinogenesis in hamster tissues: Update. Endocr. Rev. 14, 94-95.
4. Lang, R., and Redmann, U. (1979) Nonmutagenicity of some sex hormones in the Ames salmonella/microsome mutagenicity test. Mutat. Res. 67, 361-365.
5. Lang, R., and Reimann, R. (1993) Studies for a genotoxic potential of some endogenous and exogenous sex steroids. I. Communication: Examination for the induction of gene mutations using the Ames Salmonella/microsome test and the HGPRT test in V79 cells. Environ. Mol. Mutagen. 21, 272-304.
6. Drevon, C., Piccoli, C., and Montesano, R. (1981) Mutagenicity assays of estrogenic hormones in mammalian cells. Mutat. Res. 89, 83-90.
7. Furth, J. (1982) Hormones as etiological agents in neoplasia. In Cancer. A Comprehensive Treatise. 1. Etiology: Chemical and Physical Carcinogenesis (Becker, F. F., Ed.) Chapter 4, pp 89-134, Cancer Plenum Press, New York.
8. Li, J. J., and Li, S. A. (1990) Estrogen carcinogenesis in hamster tissues: A critical review. Endocr. Rev. 11, 524-531.
9. Nandi, S., Guzman, R. C., and Yang, J. (1995) Hormones and mammary carcinogenesis in mice, rats and humans: A unifying hypothesis. Proc. Natl Acad. Sci. U.S.A. 92, 3650-3657.
10. Feigelson, H. S., and Henderson, B. E. (1996) Estrogens and breast cancer. Carcinogenesis 17, 2279-2284.
11. Dickson, R. B., and Stancel, G. M. (2000) Estrogen receptor-mediated processes in normal and cancer cells. In JNCI Monograph 27: Estrogens as Endogenous Carcinogens in the Breast and Prostate (Cavalieri, E., and Rogan, E., Eds) pp 135-145, Oxford Press, New York.
12. Hahn, W. C., and Weinberg, R. A. (2002) Rules for making tumor cells. N. Engl. J. Med. 347, 1593-1603.
13. 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. 99, 10937-10942.
14. Cavalieri, E., Frenkel, K., Liehr, J. G., Rogan, E., and Roy, D. (2000) Estrogens as endogenous genotoxic agents: DNA adducts and mutations. In JNCI Monograph 27: Estrogens as Endogenous Carcinogens in the Breast and Prostate (Cavalieri, E., and Rogan, E., Eds.) pp 75-93, Oxford Press, New York.
15. Cavalieri, E., Rogan, E., and Chakravarti, D. (2004) The role of endogenous catechol quinones in the initiation of cancer and neurodegenerative diseases. In Methods in Enzymology, Quinones and Quinone Enzymes, Part B (Sies, H., and Packer, L., Eds) Vol. 382, pp 293-319, Elsevier, Duesseldorf, Germany.
16. Li, K.-M., Todorovic, R., Devanesan, P., Higginbotham, S., Köfeler, H., Ramanathan, R., Gross, M. L., Rogan, E. G., and Cavalieri, E. L. (2004) Metabolism and DNA binding studies of 4-hydroxyestradiol and estradiol-3,4-quinone in vitro and in female ACI rat mammary gland in vivo. Carcinogenesis 25, 289-297.
17. Chakravarti, D., Mailander, P., Li, K.-M., Higginbotham, S., Zhang, H., Gross, M. L., Cavalieri, E., and Rogan, E. (2001) Evidence that a burst of DNA depurination in SENCAR mouse skin induces error-prone repair and forms mutations in the H-ras gene. Oncogene 20, 7945-7953.
18. Chakravarti, D., Mailander, P. C., Higginbotham, S., Cavalieri, E. L., and Rogan, E. G. (2003) The catechol estrogen-3,4-quinone metabolites induce mutations in the mammary gland of ACI rats. Proc. Am. Assoc. Cancer Res. 44, 180.
19. Zhao, Z., Kosinska, W., Khmelnitsky, M., Cavalieri, E. L., Rogan, E. G., Chakravarti, D., Sacks, P., and Guttenplan, J. B. (2005) Mutagenic activity of 4-hydroxyestradiol, but not 2-hydroxyestradiol, in BB2 rat embryonic cells, and the mutational spectrum of 4-hydroxyestradiol. Chem. Res. Toxicol., in press.
20. Li, J. J., and Li, S. A. (1987) Estrogen carcinogenesis in Syrian hamster tissue: Role of metabolism. Fed. Proc. 46, 1858-1863.
21. Newbold, R. R., and Liehr, J. G. (2000) Induction of uterine adenocarcinoma in CD-1 mice by catechol estrogens. Cancer Res. 60, 235-237.
22. Russo, J., Lareef, M. H., Tahin, Q., Hu, Y.-F., Slater, C., Ao, X., and Russo, I. H. (2002) 17β-Estradiol is carcinogenic in human breast epithelial cells. J. Steroid Biochem. Mol. Biol. 80, 149-162.
23. Russo, J., Lareef, M. H., Balogh, G., Guo, S., and Russo, I. H. (2003) Estrogen and its metabolites are carcinogenic agents in human breast epithelial cells. J. Steroid Biochem. Mol. Biol. 87, 1-25.
24. Lareef, M. H., Garber, J., Russo, P. A., Russo, I. H., Heulings, R., and Russo, J. (2005) The estrogen antagonist ICI-182-780 does not inhibit the transformation phenotypes induced by 17-β-estradiol and 4-OH estradiol in human breast epithelial cells. Int. J. Oncol. 26, 423-429.
25. Russo, I. H., Fernandez, S. V., and Russo, J. (2005) Estradiol and its metabolites 4-hydroxyestradiol and 2-hydroxyestradiol induce mutations in human breast epithelial cells. Int. J. Cancer, in press.
26. Stack, D., Byun, J., Gross, M. L., Rogan, E. G., and Cavalieri, E. (1996) Molecular characteristics of catechol estrogen quinones in reactions with deoxyribonucleosides. Chem. Res. Toxicol. 9, 851-859.
27. NIH Guidelines for the Laboratory Use of Chemical Carcinogens (1981) NIH Publication No. 81-2385, U.S. Government Printing Office, Washington, DC.
28. Saeed, M., Zahid, M., Rogan, E., and Cavalieri, E. (2005) Synthesis of the catechols of natural and synthetic estrogens by using 2-iodoxybenzoic acid (IBX) as the oxidizing agent. Steroids 70, 173-178.
29. Wong, A. K. L., Cavalieri, E., and Rogan, E. (1986) Dependence of benzo[a]pyrene metabolic profile on the concentration of cumene hydroperoxide with uninduced and induced rat liver microsomes. Biochem. Pharmacol. 35, 1583-1588.
30. Mancera, O., Rosenkranz, G., and Sondheimer, F. (1953) Steroids. Part XLVI. Synthesis of 11β-hydroxytestosterone and 11-keto testosterone. J. Chem. Soc. Abstract 2189-2191.
31. 32P-Postlabeling analysis of benzo[a]pyrene-DNA adducts formed in vitro and in vivo. Chem. Res. Toxicol. 2, 312-315.
32. Saeed, M., Gunselman, S. J., Higginbotham, S., Rogan, E., and Cavalieri, E. (2005) Formation of the depurinating N3adenine and N7guanine adducts by reaction of DNA with hexestrol-3′-4′-quinone or enzyme-activated 3′-hydroxyhexestrol. Implications for a unifying mechanism of tumor initiation by natural and synthetic estrogens. Steroids 70, 37-45.
33. RamaKrishna, N. V., 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[a,l]pyrene in the presence of nucleosides. Chem. Res. Toxicol. 6, 554-560.
34. Mulder, P. P., Chen, L., Sekhar, B. C., George, M., Gross, M. L., Rogan, E. G., and Cavalieri, E. L. (1996) Synthesis and structure determination of the adducts formed by electrochemical oxidation of 1,2,3,4-tetrahydro-7,12- dimethylbenz[a]anthracene in the presence of deoxyribonucleosides or adenine. Chem. Res. Toxicol. 9, 1264-1277.
35. Hanson, A. A., Rogan, E. G., and Cavalieri, E. L. (1998) Synthesis of adducts formed by iodine oxidation of aromatic hydrocarbons in the presence of deoxyribonucleosides and nucleobases. Chem. Res. Toxicol. 11, 1201-1208.
36. Li, K.-M., Byun, J., Gross, M. L., Zamzow, D., Jankowiak, R., Rogan, E. G., and Cavalieri, E. L. (1999) Synthesis and structure determination of the adducts formed by electrochemical oxidation of dibenzo[a,l]-pyrene in the presence of adenine. Chem. Res. Toxicol. 12, 749-757.
37. Chen, L., Devanesan, P. D., Higginbotham, S., Ariese, F., Jankowiak, R., Small, G. J., Rogan, E. G., and Cavalieri, E. L. (1996) Expanded analysis of benzo[a]pyrene-DNA adducts formed in vitro and in mouse skin: Their significance in tumor initiation. Chem. Res. Toxicol. 9, 897-903.
38. Cavalieri, E. L., Rogan, E. G., Li, K.-M., Todorovic, R., Ariese, F., Jankowiak, R., Grubor, N., and Small, G. J. (2005) Identification and quantification of the depurinating DNA adducts formed in mouse skin treated with dibenzo[a,l]pyrene (DB[a,l]P) or its metabolites and in rat mammary gland treated with DB[a,l]P. Chem. Res. Toxicol. 18, 976-983.
39. Saeed, M., Zahid, M., Gunselman, S. J., Rogan, E., and Cavalieri, E. (2005) Slow loss of deoxyribose from the N7deoxyguanosine adducts of estradiol-3,4-quinone and hexestrol-3′,4′-quinone. Implications for mutagenic activity. Steroids 70, 29-35.
40. Dwivedy, I., Devanesan, P., Cremonesi, P., Rogan, E., and Cavalieri, E. (1992) Synthesis and characterization of estrogen 2,3- and 3,4-quinones. Comparison of DNA adducts formed by the quinones versus horseradish peroxidase-activated catechol estrogens. Chem. Res. Toxicol. 5, 828-833.
41. Liehr, J. G., and Ricci, M. J. (1996) 4-Hydroxylation of estrogens as markers of human mammary tumors. Proc. Natl. Acad. Sci. U.S.A. 93, 3294-3296.
42. Rogan, E. G., Badawi, A. F., Devanesan, P. D., Meza, J. L., Edney, J. A., West, W. W., Higginbotham, S. M., and Cavalieri, E. L. (2003) Relative imbalances in estrogen metabolism and conjugation in breast tissue of women with carcinoma: Potential biomarkers of susceptibility to cancer. Carcinogenesis 24, 697-702.