Increased sensitivity of estrogen receptor alpha overexpressing antral follicles to methoxychlor and its metabolites

Toxicological Sciences

Volumn 120, Issue 2, 2011, Pages 447-459

  Paulose, Tessie ^a   Hernández Ochoa, Isabel ^a   Basavarajappa, Mallikarjuna S ^a   Peretz, Jackye ^a   Flaws, Jodi A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Antral follicles; Estrogen receptor alpha; HPTE; Metabolizing enzymes; Methoxychlor; Mono hydroxy methoxychlor; Nuclear receptors; Ovary; Pesticide

Indexed keywords

ANDROGEN RECEPTOR; AROMATIC HYDROCARBON RECEPTOR; BISHYDROXYMETHOXYCHLOR; CYTOCHROME P450 3A4; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MESSENGER RNA; METHOXYCHLOR; MONOHYDROXYMETHOXYCHLOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; FEMALE; GENOTYPE; LIVER CLEARANCE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FOLLICLE; RECEPTOR BINDING; REPRODUCTIVE TOXICITY; XENOBIOTIC METABOLISM;

MUS;

EID: 79953107917     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr011     Document Type: Article

References (41)

1. Barnett, K. R., Tomic, D., Gupta, R. K., Miller, K. P., Meachum, S., Paulose, T., and Flaws, J. A. (2007). The aryl hydrocarbon receptor affects mouse ovarian follicle growth via mechanisms involving estradiol regulation and responsiveness. Biol. Reprod. 76, 1062-1070.
2. Borgeest, C., Symonds, D., Mayer, L. P., Hoyer, P. B., and Flaws, J. A. (2002). Methoxychlor may cause ovarian follicular atresia and proliferation of the ovarian epithelium in the mouse. Toxicol. Sci. 68, 473-478.
3. Bulger, W. H., Muccitelli, R. M., and Kupfer, D. (1978). Studies on the in vivo and in vitro estrogenic activities of methoxychlor and its metabolites. Role of hepatic mono-oxygenase in methoxychlor activation. Biochem. Pharmacol. 27, 2417-2423.
4. Chang, E. C., Charn, T. H., Park, S. H., Helferich, W. G., Komm, B., Katzenellenbogen, J. A., and Katzenellenbogen, B. S. (2008). Estrogen receptors alpha and beta as determinants of gene expression: Influence of ligand, dose, and chromatin binding. Mol. Endocrinol. 22, 1032-1043.
5. Couse, J. F., Davis, V. L., Hanson, R. B., Jefferson, W. N., McLachlan, J. A., Bullock, B. C., Newbold, R. R., and Korach, K. S. (1997a). Accelerated onset of uterine tumors in transgenic mice with aberrant expression of the estrogen receptor after neonatal exposure to diethylstilbestrol. Mol. Carcinog. 19, 236-242.
6. Couse, J. F., Lindzey, J., Grandien, K., Gustafsson, J. A., and Korach, K. S. (1997b). Tissue distribution and quantitative analysis of estrogen receptor alpha and estrogen receptor beta messenger ribonucleic acid in the wild-type and ER alpha knockout mouse. Endocrinology 138, 4613-4621.
7. Cummings, A. M. (1997). Methoxychlor as a model for environmental estrogens. Crit. Rev. Toxicol. 27, 367-379.
8. Danzo, B. J. (1997). Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ. Health Perspect. 105, 294-301.
9. Gaido, K. W., Leonard, L. S., Maness, S. C., Hall, J. M., McDonnell, D. P., Saville, B., and Safe, S. (1999). Differential interaction of the methoxychlor metabolite 2,2-Bis-(p-hydroxyphenyl)-1,1,1-trichloroethane with estrogen receptors α and β. Endocrinology 140, 5746-5753.
10. Gaido, K. W., Maness, S. C., McDonnell, D. P., Dehal, S. S., Kupfer, D., and Safe, S. (2000). Interaction of methoxychlor and related compounds with estrogen receptor α and β, and androgen receptor: structure-activity studies. Mol. Pharmacol. 58, 852-858.
11. Golovleva, L. A., Polyakova, A. B., Pertsova, R. N., and Finkelshtein, Z. I. (1984). The fate of methoxychlor in soils and transformation by soil microorganisms. J. Environ. Health Sci. B 19, 523-538.
12. Gray, L. E., Jr., Ostby, J. S., Ferrell, J. M., Sigmon, C. R., and Goldman, J. M. (1988). Methoxychlor induces estrogen-like alterations of behavior and the reproductive tract in the female rat and hamster: effects on sex behavior, running wheel activity, and uterine morphology. Tox. Appl. Pharm. 96, 525-540.
13. Gupta, R. K., Miller, K. P., Babus, J. K., and Flaws, J. A. (2006). Methoxychlor inhibits growth and induces atresia of antral follicles through an oxidative stress pathway. Toxicol. Sci. 93, 382-389.
14. Hall, J. M., and McDonnell, D. P. (1999). The estrogen receptor b-isoform (ERb) of the human estrogen receptor modulates ERa transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140, 5566-5578.
15. Hirshfield, A. N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43-101.
16. Hruska, K. S., Tilli, M. T., Ren, S., Cotarla, I., Kwong, T., Li, M., Fondell, J. D., Hewitt, J. A., Koos, R. D., Furth, P. A., et al. (2002). Conditional over-expression of estrogen receptor alpha in a transgenic mouse model. Transgenic Res. 11, 361-372.
17. Hsueh, A. J., Adashi, E. Y., Jones, P. B., and Welsh, T. H., Jr. (1984). Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocr. Rev. 5, 76-127.
18. Kraus, W. L., Weis, K. E., and Katzenellenbogen, B. S. (1995). Inhibitory cross-talk between steroid hormone receptors: differential targeting of estrogen receptor in the repression of its transcriptional activity by agonistand antagonist-occupied progestin receptors. Mol. Cell. Biol. 15, 1847-1857.
19. Krishnan, V., Porter, W., Santostefano, M., Wang, X., and Safe, S. (1995). Molecular mechanism of inhibition of estrogen-induced cathepsin D gene expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in MCF-7 cells. Mol. Cell. Biol. 15, 6710-6719.
20. Kuiper, G., Lemmen, J. G., Carlsson, B., Corton, J. C., Safe, S., Van Der Saag, P. T., Van Der Burg, B., and Gustafsson, J. A. (1998). Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor b. Endocrinology 139, 4252-4263.
21. Lemaire, G., Mnif, W., Mauvais, P., Balaguer, P., and Rahmani, R. (2006). Activation of a and b estrogen receptors by persistent pesticides in reporter cell lines. Life Sci. 79, 1160-1169.
22. Lindberg, M. K., Moverare, S., Skrtic, S., Gao, H., Dahlman-Wright, K., Gustafsson, J. A., and Ohlsson, C. (2003). Estrogen receptor (ER)-beta reduces ER(alpha)-regulated gene transcription supporting a "Ying-Yang" relationship between ER alpha and ER beta in mice. Mol. Endocrinol. 17, 203-208.
23. Matthews, J., and Gustafsson, J. A. (2003). Estrogen signaling: A subtle balance between ER alpha and ER beta. Mol. Interv. 3, 281-292.
24. Miller, K. P., Gupta, R. K., and Flaws, J. A. (2006). Methoxychlor metabolites may cause ovarian toxicity through estrogen-regulated pathwats. Toxicol. Sci. 93, 180-188.
25. Miller, K. P., Gupta, R. K., Greenfeld, C. R., Babus, J. K., and Flaws, J. A. (2005). Methoxychlor directly affects ovarian antral follicle growth and atresia through Bcl-2- and Bax-mediated pathways. Toxicol. Sci. 88, 213-221.
26. Murdoch, F. E., and Gorski, J. (1991). The role of ligand in estrogen receptor regulation of gene expression. Mol. Cell. Endocrinol. 78, C103-C108.
27. Mwinyi, J., Cavaco, I., Pederson, R. S., Persson, A., Burkhardt, S., Mkrtchian, S., and Ingelman-Sundberg, M. (2010). Regulation of CYP2C19 expression by estrogen receptor alpha: implications for estrogen-dependent inhibition of drug metabolism. Mol. Pharmacol 78, 886-894.
28. Newbold, R. R., Jefferson, W. N., and Padilla-Banks, E. (2007). Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod. Toxicol. 24, 253-258.
29. Oropeza-Hernandez, L. F., Lopez-Romero, R., and Albores, A. (2003). Hepatic CYP1A, 2B, 2C, 2E and 3A regulation by methoxychlor in male and female rats. Toxicol. Lett. 144, 93-103.
30. Safe, S., and Wormke, M. (2003). Inhibitory aryl hydrocarbon receptorestrogen receptor alpha cross-talk and mechanisms of action. Chem. Res. Toxicol. 16, 807-816.
31. Sanchez, R., Nguyen, D., Rocha, W., White, J. H., and Mader, S. (2002). Diversity in the mechanism of gene regulation by estrogen receptors. Bioessays 24, 244-254.
32. Scippo, M.-L., Argiris, C., Van de Weerdt, C., Muller, M., Willemsen, P., Martial, J., and Maghuin-Rogister, G. (2004). Recombinant human estrogen, androgen and progesterone receptors for detection of potential endocrine disruptors. Anal. Bioanal. Chem. 378, 664-669.
33. Shockett, P., Difilippantonio, M., Hellman, N., and Schatz, D. G. (1995). A modified tetracycline-regulated system provides autoregulatory, inducible gene expression in cultured cells and transgenic mice. Proc. Natl Acad. Sci. U S A. 92, 6522-6526.
34. Stresser, D. M., and Kupfer, D. (1997). Catalytic characteristics of CYP3A4: requirement for a phenolic function in ortho hydroxylation of estradiol and mono-O-demethylated methoxychlor. Biochemistry 36, 2203-2210.
35. Stresser, D. M., and Kupfer, D. (1998). Human cytochrome P450-catalyzed conversion of the proestrogenic pesticide methoxychlor into an estrogen. Role of CYP2C19 and CYP1A2 in O-demethylation. Drug Metab. Dispos. 26, 868-875.
36. Symonds, D. A., Miller, K. P., Tomic, D., and Flaws, J. A. (2006). Effect of methoxychlor and estradiol on cytochrome p450 enzymes in the mouse ovarian surface epithelium. Toxicol. Sci. 89, 510-514.
37. Tanaka, Y., Sasaki, M., Kaneuchi, M., Fujimoto, S., and Dahiya, R. (2003). Estrogen receptor alpha polymorphisms and renal cell carcinoma - a possible risk. Mol. Cell. Endocrinol. 202, 109-116.
38. Tee, M. K., Rogatsky, I., Tzagaraski-Foster, C., Cvoro, A., An, J., Christy, R. J., Yamamoto, K. R., and Leitman, D. C. (2004). Estradiol and selective estrogen receptor modulators differentially regulate target genes with estrogen receptors alpha and beta. Mol. Biol. Cell. 15, 1262-1272.
39. Tomic, D., Frech, M. S., Babus, J. K., Gupta, R. K., Furth, P. A., and Flaws, J. A. (2006). Methoxychlor induces atresia of antral follicles in ERalpha-overexpressing mice. Toxicol. Sci. 93, 196-204.
40. Tomic, D., Frech, M. S., Babus, J. K., Symonds, D., Furth, P. A., Koos, R. D., and Flaws, J. A. (2007). Effects of ERalpha overexpression on female reproduction in mice. Reprod. Toxicol. 23, 317-325.
41. Waters, K. M., Safe, S., and Gaido, K. W. (2001). Differential gene expression in response to methoxychlor and estradiol through ERα, ERβ, and AR in reproductive tissues of female mice. Toxicol. Sci. 63, 47-56.