Cytochrome P450 isoforms catalyze formation of catechol estrogen quinones that react with DNA

Metabolism: Clinical and Experimental

Volumn 56, Issue 7, 2007, Pages 887-894

  Zhang, Yan ^a   Gaikwad, Nilesh W ^a   Olson, Kevin ^a   Zahid, Muhammad ^a   Cavalieri, Ercole L ^a   Rogan, Eleanor G ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYESTRADIOL; 4 HYDROXYESTRADIOL; CATECHOL ESTROGEN; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; CYTOCHROME P450 3A4; CYTOCHROME P450 ISOENZYME; DNA; ESTRADIOL 2,3 QUINONE; ESTRADIOL 3,4 QUINONE; GLUTATHIONE; QUINONE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CONTROLLED STUDY; GENE MUTATION; HORMONE DETERMINATION; LIQUID CHROMATOGRAPHY; OXIDATION; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY;

ARYL HYDROCARBON HYDROXYLASES; CATALYSIS; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 ENZYME SYSTEM; DNA; ESTROGENS, CATECHOL; GLUTATHIONE; QUINONES;

EID: 34250011712     PISSN: 00260495     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.metabol.2007.03.001     Document Type: Article

References (34)

1. Henderson B.E., and Feigelson H.S. Hormonal carcinogenesis. Carcinogenesis 21 (2000) 427-433
2. Lippman M.E., and Dickson R.B. Mechanism of normal and malignant breast epithelial growth regulation. J Steroid Biochem 34 (1989) 107-121
3. Chakravarti D., Mailander P., Li K.-M., et al. Evidence that a burst of DNA depurinating in SENCAR mouse skin induces error-prone repair and forms mutations in the H-ras gene. Oncogene 20 (2001) 7945-7953
4. Cavalieri E.L., Rogan E.G., and Chakravarti D. The role of endogenous catechol quinones in the initiation of cancer and neurodegenerative diseases. In: Sies H., and Packer L. (Eds). Methods in enzymology, quinones and quinone enzymes, part B vol 382 (2004), Elsevier, Duesseldorf (Germany) 293-319
5. Lee A.J., Cai M.X., Thomas P.E., et al. Characterization of the oxidative metabolites of 17β-estradiol and estrone formed by 15 selectively expressed human cytochrome P450 isoforms. Endocrinology 144 (2003) 3382-3398
6. Hanna I.H., Dawling S., Roodi N., et al. Cytochrome P450 1B1 (CYP1B1) pharmacogenetics: association of polymorphism with functional differences in estrogen hydroxylation activity. Cancer Res 60 (2000) 3440-3444
7. Mailander P.C., Meza J.L., Higginbotham S., et al. Induction of A.T to G.C mutations by erroneous repair of depurinated DNA following estrogen treatment of the mammary gland of ACI rats. J Steroid Biochem Mol Biol 101 (2006) 204-215
8. Liehr J.G., Fang W.F., Sirbasku D.A., et al. Carcinogenicity of catechol estrogens in Syrian hamsters. J Steroid Biochem 24 (1986) 353-356
9. Li J.J., and Li S.A. Estrogen carcinogenesis in Syrian hamster tissue: role of metabolism. Fed Proc 46 (1987) 1858-1863
10. Newbold R.R., and Liehr J.G. Induction of uterine adenocarcinoma in CD-1 mice by catechol estrogens. Cancer Res 60 (2000) 235-237
11. Zhao Z., Kosinska W., Khmelnitsky M., et al. Mutagenic activity of 4-hydroxyestradiol, but not 2-hydroxyestradiol, in BB2 rat embryonic cells, and the mutational spectrum of 4-hydoxyestradiol. Chem Res Toxicol 19 (2006) 475-479
12. Lee A.J., Kosh J.W., Conney A.H., et al. Characterization of the NADPH-dependent metabolism of 17β-estradiol to multiple metabolites by human liver microsomes and selectively expressed human cytochrome P450 3A4 and 3A5. Pharm Exp Ther 298 (2001) 420-432
13. Butterworth M., Lau S.S., and Monks T.J. 17β-Estradiol metabolism by hamster hepatic microsomes: comparison of catechol O-methylation with catechol estrogen oxidation and glutathione conjugation. Chem Res Toxicol 9 (1996) 793-799
14. Iverson S.L., Shen L., Anlar N., et al. Bioactivation of estrone and its catechol metabolites to quinoid-glutathione conjugates in rat liver microsomes. Chem Res Toxicol 9 (1996) 492-499
15. Cao K., Devanesan P.D., Ramanathan R., et al. Covalent binding of catechol estrogens to glutathione catalyzed by horseradish peroxidase, lactoperoxidase, or rat liver microsomes. Chem Res Toxicol 11 (1998) 917-924
16. Hachey D.L., Dawling S., Roodi N., et al. Sequential action of phase I and II enzymes cytochrome P450 1B1 and glutathione S-transferase P1 in mammary estrogen metabolism. Cancer Res 63 (2003) 8492-8499
17. Li K.-M., Todorovic R., Devanesan P., et al. 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 (2004) 289-297
18. Dawling S., Roodi N., Mernaugh R.L., et al. Catechol-O-methyltransferase (COMT)-mediated metabolism of catechol estrogens: comparison of wild-type and variant COMT isoforms. Cancer Res 61 (2001) 6716-6722
19. Dwivedy I., Devanesan P., Cremonesi P., et al. 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 (1992) 828-833
20. Zahid M., Kohli E., Saeed M., et al. The greater reactivity of estradiol-3,4-quinone versus estradiol-2,3-quinone with DNA in the formation of depurinating adducts. Implication for tumor-initiating activity. Chem Res Toxicol 19 (2006) 164-172
21. Roy D., Bernhardt A., Strobel H.W., et al. Catalysis of the oxidation of steroid and stilbene estrogens to estrogen quinone metabolites by the beta-naphthoflavone-inducible cytochrome P450 family. Arch Biochem Biophys 296 (1992) 450-456
22. Gonzalez F.J. Cytochrome P450 in humans. In: Schenkman J.B., and Greim H. (Eds). Cytochrome P450 (1992), Springer-Verlag, Berlin 239-257
23. Gonzalez F.J. Human cytochrome P450: problems and prospects. Trends Pharmacol Sci 13 (1992) 346-352
24. Huang Z., Fasco M.J., Figge H.L., et al. Expression of cytochromes P450 in human breast tissue and tumors. Drug Metab Dispos 24 (1996) 899-905
25. Rogan E.G., Badawi A.F., Devanesan P.D., et al. Relative imbalances in estrogen metabolism and conjugation in breast tissue of women with carcinoma: potential biomarkers of susceptibility to cancer. Carcinogenesis 24 (2003) 697-702
26. Spink D.C., Hayes C.L., Young N.R., et al. The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on estrogen metabolism in MCF-7 breast cancer cells: evidence for induction of a novel 17β-estradiol 4-hydroxylase. J Steroid Biochem Mol Biol 51 (1994) 251-258
27. Modugno F., Knoll C., Kanbour-Shakir A., et al. A potential role for the estrogen-metabolizing cytochrome P450 enzymes in human breast carcinogenesis. Breast Cancer Res Treat 82 (2003) 191-197
28. Williams J.A., and Phillips D.H. Mammary expression of xenobiotic metabolizing enzymes and their potential role in breast cancer. Cancer Res 60 (2000) 4667-4677
29. Stack D.E., Byun J., Gross M.L., et al. Molecular characteristics of catechol estrogen quinones in reactions with deoxyribonucleosides. Chem Res Toxicol 9 (1996) 851-859
30. Cao K., Stack D.E., Ramanathan R., et al. Synthesis and structure elucidation of estrogen quinones conjugated with cysteine, N-acetylcysteine, and glutathione. Chem Res Toxicol 11 (1998) 909-916
31. Wang M.Y., and Liehr J.G. Induction by estrogens of lipid peroxidation and lipid peroxide-derived malonaldehyde-DNA adducts in male Syrian hamsters: role of lipid peroxidation in estrogen-induced kidney carcinogenesis. Carcinogenesis 16 (1995) 1941-1945
32. Cavalieri E.L., Kumar S., Todorovic R., et al. Imbalance of estrogen homeostasis in kidney and liver of hamsters treated with estradiol: implication for estrogen-induced initiation of renal tumors. Chem Res Toxicol 14 (2001) 1041-1050
33. Boyland E., and Chasseaud L.F. The role of glutathione and glutathione-S-transferase in mercapturic acid biosynthesis. Adv Enzymol 32 (1996) 173-219
34. Nutter L.M., Zhou B., Sierra E.E., et al. Cellular biochemical determinants modulating the metabolism of estrone-3,4-quinone. Chem Res Toxicol 7 (1994) 609-613