Estrogen metabolism and formation of estrogen-DNA adducts in estradiol-treated MCF-10F cells. The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin induction and catechol-O-methyltransferase inhibition

Journal of Steroid Biochemistry and Molecular Biology

Volumn 105, Issue 1-5, 2007, Pages 150-158

  Lu, Fang ^a   Zahid, Muhammad ^a   Saeed, Muhammad ^a   Cavalieri, Ercole L ^a   Rogan, Eleanor G ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

2,3,7,8 Tetrachlorodibenzo p dioxin (TCDD); Catechol O methyltransferase; Depurinating estrogen DNA adducts; Estrogen metabolism; MCF 10F cells

Indexed keywords

2' FLUORO 3,4 DIHYDROXY 5 NITROBENZOPHENONE; 2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CATECHOL ESTROGEN; CATECHOL ESTROGEN QUINONE; CATECHOL METHYLTRANSFERASE; CATECHOL METHYLTRANSFERASE INHIBITOR; CYTOCHROME P450; DNA; ESTRADIOL; ESTROGEN; ESTRONE; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; DNA ADDUCT; ELECTROCHEMICAL DETECTION; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; ESTROGEN METABOLISM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL;

BENZOPHENONES; BLOTTING, WESTERN; BREAST NEOPLASMS; CATECHOL O-METHYLTRANSFERASE; CELL LINE, TUMOR; DNA ADDUCTS; ESTRADIOL; HUMANS; TETRACHLORODIBENZODIOXIN;

EID: 34547697291     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2006.12.102     Document Type: Article

References (32)

1. Henderson B.E., and Feigelson H.S. Hormonal carcinogenesis. Carcinogenesis 21 (2000) 427-433
2. Cavalieri E., Chakravarti D., Guttenplan J., Hart E., Ingle J., Jankowiak R., Muti P., Rogan E., Russo J., Santen R., and Sutter T. Catechol estrogen quinones as initiators of breast and other human cancers: implications for biomarkers of susceptibility and cancer prevention. BBA Rev. Cancer 1766 (2006) 63-78
3. Zhu B.T., and Conney A.H. Functional role of estrogen metabolism in target cells: review and perspectives. Carcinogenesis 19 (1998) 1-27
4. Spink D.C., Spink B.C., Cao J.Q., DePasquale J.A., Pentecost B.T., Fasco M.J., Li Y., and Sutter T.R. Differential expression of CYP1A1 and CYP1B1 in human breast epithelial cells and breast tumor cells. Carcinogenesis 19 (1998) 291-298
5. Chakravarti D., Mailander P.C., Li K.-M., Higginbotham S., Zhang H.L., Gross M.L., Meza J.L., Cavalieri E.L., and Rogan E.G. 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 (2001) 7945-7953
6. Mailander P.C., Meza J.L., Higginbotham S., and Chakravarti D. 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
7. Zhao Z., Kosinska W., Khmelnitsky M., Cavalieri E.L., Rogan E.G., Chakravarti D., Sacks P.G., and Guttenplan J.B. Mutagenic activity of 4-hydroxyestradiol, but not 2-hydroxyestradiol, in BB rat2 embryonic cells, and the mutational spectrum of 4-hydroxyestradiol. Chem. Res. Toxicol. 19 (2006) 475-479
8. Russo J., Lareef M.H., Tahin O., Hu Y.F., Slater C., Ao X., and Russo I.H. 17Beta-estradiol is carcinogenic in human breast epithelial cells. J. Steroid Biochem. Mol. Biol. 80 (2002) 149-162
9. Russo J., Lareef M.H., Balogh G., Guo S., and Russo I.H. Estrogen and its metabolites are carcinogenic agents in human breast epithelial cells. J. Steroid Biochem. Mol. Biol. 87 (2003) 1-25
10. Lareef M.H., Garber J., Russo P.A., Russo I.H., Heulings R., and Russo J. The estrogen antagonist ICI-182-780 does not inhibit the transformation phenotypes induced by 17-beta-estradiol and 4-OH estradiol in human breast epithelial cells. Int. J. Oncol. 26 (2005) 423-429
11. Mannisto P.T., and Kaakkola S. Catechol-O-methyltransferase (COMT): biochemistry, molecular biology, pharmacology, and clinical efficacy of the new selective COMT inhibitors. Pharmacol. Rev. 51 (1999) 593-628
12. N.W. Gaikwad, E.G. Rogan, E.L. Cavalieri, Evidence for NQO1-catalyzed reduction of estrogen ortho-quinones. Mass spectrometric determination of enzyme-substrate complex, Free Radic. Biol. Med., 2007, in press.
13. Hersey R.M., Williams K.I., and Weisz J. Catechol estrogen formation by brain tissue: characterization of a direct product isolation assay for estrogen-2- and 4-hydroxylase activity and its application to studies of 2- and 4-hydroxyestradiol formation by rabbit hypothalamus. Endocrinology 109 (1981) 1912-1920
14. Cohn C.K., Dunner D.L., and Axelrod J. Reduced catechol-O-methyltransferase activity in red blood cells of women with primary affective disorder. Science 70 (1970) 1323-1324
15. Lavigne J.A., Helzlsouer K.J., Huang H.Y., Strickland P.T., Bell D.A., Selmin O., Watson M.A., Hoffman S., Comstock G.W., and Yager J.D. An association between the allele coding for a low activity variant of catechol-O-methyltransferase and the risk for breast cancer. Cancer Res. 57 (1997) 5493-5497
16. Huang C.S., Chern H.D., Chang K.J., Cheng C.W., Hsu S.M., and Shen C.Y. Breast cancer risk associated with genotype polymorphism of the estrogen metabolizing genes CYP17, CYP1A1, and COMT: a multigenic study on cancer susceptibility. Cancer Res. 59 (1999) 4870-4875
17. Yim D.-S., Park S.K., Yoo K.-Y., Yoon K.-S., Chung H.H., Kang H.J., Ahn S.H., Noh D.Y., Choe K.J., Jang I.J., Shin S.G., Strickland P.T., Hirvonen A., and Kang D. Relationship between the val158met polymorphism of catechol-O-methyl transferase and breast cancer. Pharmacogenetics 11 (2001) 1-8
18. Thompson P.A., Shields P.G., Freudenheim J.L., Stone A., Vena J.E., Marshall J.R., Graham S., Laughlin R., Nemoto T., Kadlubar F.F., and Ambrosone C.B. Genetic polymorphisms in catechole-O-methyltransferase, menopausal status, and breast cancer risk. Cancer Res. 58 (1998) 2107-2110
19. Millikan R., Pittman G.S., Tse C.-K.J., Duell E., Newman B., Savitz D., Moorman P.G., Boissy R.J., and Bell D.A. Catechol-O-methyltransferase and breast cancer risk. Carcinogenesis 19 (1998) 1943-1947
20. Wedren S., Rudqvist T.R., Granath F., Weiderpass E., Ingelman-Sundberg M., Persson I., and Magnusson C. Catechol-O-methyltransferase gene polymorphism and post-menopausal breast cancer risk. Carcinogenesis 24 (2003) 681-687
21. Lachman H.M., Papolos D.F., Saito T., Yu Y.M., Szumlanski C., and Weinshilboum R.M. Human catechol-O-methyltransferase pharmacogenetics: description of a functional polymorphism and its potential application to neuropsychiatric disorders. Pharmacogenetics 6 (1996) 243-250
22. Scanlon P.D., Raymond F.A., and Weinshilboum R.M. Catechol-O-methyltransferase: thermolabile enzyme in erythrocytes of subjects homozygous for allele for low activity. Science 203 (1979) 63-65
23. Garner C.E., Burka L.T., Etheridge A.E., and Matthews H.B. Catechol metabolites of polychlorinated biphenyls inhibit the catechol-O-methyltransferase-mediated metabolism of catechol estrogens. Toxicol. Appl. Pharmacol. 162 (2000) 115-123
24. Chen Z.H., Hurh Y.J., Na H.K., Kim J.H., Chun Y.J., Kim D.H., Kang K.S., Cho M.H., and Surh Y.J. Resveratrol inhibits TCDD-induced expression of CYP1A1 and CYP1B1 and catechol estrogen-mediated oxidative DNA damage in cultured human mammary epithelial cells. Carcinogenesis 25 (2004) 2005-2013
25. Saeed M., Zahid M., Rogan E.G., and Cavalieri E.L. Synthesis of catechols of natural and synthetic estrogens by using 2-iodoxybenzoic acid (IBX) as the oxidizing agent. Steroids 70 (2005) 173-178
26. Stack D.E., Byun J., Gross M.L., Rogan E.G., and Cavalieri E.L. Molecular characteristics of catechol estrogen quinones in reactions with deoxyribonucleosides. Chem. Res. Toxicol. 9 (1996) 851-859
27. Li K.-M., Todorovic R., Devanesan P., Higginbotham S., Kofeler H., Ramanathan R., Gross M.L., Rogan E.G., and Cavalieri E.L. 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
28. Denizot F., and Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89 (1986) 271-277
29. Goodman J.E., Jensen L.T., He P., and Yager J.D. Characterization of human soluble high and low activity catechol-O-methyltransferase catalyzed catechol estrogen methylation. Pharmacogenetics 12 (2002) 517-528
30. Rogan E.G., Badawi A.F., Devanesan P., Meza J.L., Edney J.A., West W.W., Higginbotham S.M., and Cavalieri E.L. 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
31. Vidal J.D., Vandevoort C.A., Marcus C.B., Lazarewicz N.R., and Conley A.J. 2,3,7,8-tetrachlorodibenzo-p-dioxin induces CYP1B1 expression in human luteinized granulosa cells. Arch. Biochem. Biophys. 439 (2005) 53-60
32. Dawling S., Roodi N., Mernaugh R.L., Wang X., and Parl F.F. Catechol-O-methyltransferase (COMT)-mediated metabolism of catechol estrogens: comparison of wild-type and variant COMT isoforms. Cancer Res. 61 (2001) 6716-6722