Daily treatment with α-naphthoflavone enhances follicular growth and ovulation rate in the rat

The aryl hydrocarbon receptor (AhR) is a ligand-activated transcription factor and the first protein involved in a variety of physiological and toxicological processes, including those of xenobiotic metabolizing enzymes. AhR has been found in the ovary of many species and seems to mediate the ovaria...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autor principal: Barreiro, K.A
Otros Autores: Di Yorio, M.P, Artillo-Guida, R.D, Paz, D.A, Faletti, A.G
Formato: Capítulo de libro
Lenguaje:Inglés
Publicado: 2011
Acceso en línea:Registro en Scopus
DOI
Handle
Registro en la Biblioteca Digital
Aporte de:Registro referencial: Solicitar el recurso aquí
Descripción
Sumario:The aryl hydrocarbon receptor (AhR) is a ligand-activated transcription factor and the first protein involved in a variety of physiological and toxicological processes, including those of xenobiotic metabolizing enzymes. AhR has been found in the ovary of many species and seems to mediate the ovarian toxicity of many environmental contaminants, which are AhR ligands. However, the role of AhR in the ovarian function is unknown. Therefore, the aim of this work was to study the action of α-naphthoflavone (αNF), known to be an AhR antagonist, on both follicular growth and ovulation. Immature Sprague-Dawley rats were daily injected intraperitoneally with αNF (0.1-80. mg/kg) or vehicle for 12. days, and primed with gonadotrophins (eCG/hCG) to induce follicular growth and ovulation. Ovaries were obtained 20. h after hCG administration. By means of immunohistochemistry, we found that the numbers of primordial, primary and antral follicles were increased in rats treated with 80. mg/kg αNF and that there were no differences with other doses. Likewise, the ovarian weight and the ovulation rate, measured by both number of oocytes within oviducts and corpora lutea in ovarian sections, were increased when the rats received either 1 or 10. mg/kg daily. Although further studies are necessary to know the mechanism of action of αNF, it is possible that the different ovarian processes can be differentially responsive to the presence of different levels of αNF, and that the same or different endogenous AhR ligands can be involved in these ovarian processes in a cell type-dependent manner. © 2011 Elsevier Inc.
Bibliografía:Abbott, B.D., Schmid, J.E., Pitt, J.A., Buckalew, A.R., Wood, C.R., Held, G.A., Diliberto, J.J., Adverse reproductive outcomes in the transgenic Ah receptor-deficient mouse (1999) Toxicol. Appl. Pharmacol., 155, pp. 62-70
Ashida, H., Nishiumi, S., Fukuda, I., An update on the dietary ligands of the AhR (2008) Expert Opin. Drug Metab. Toxicol., 4, pp. 1429-1447
Barnett, K.R., Tomic, D., Gupta, R.K., Miller, K.P., Meachum, S., Paulose, T., Flaws, J.A., The aryl hydrocarbon receptor affects mouse ovarian follicle growth via mechanisms involving estradiol regulation and responsiveness (2007) Biol. Reprod., 76, pp. 1062-1070
Beecher, G.R., Overview of dietary flavonoids: nomenclature, occurrence and intake (2003) J. Nutr., 133, pp. 3248S-3254S
Benedict, J.C., Lin, T.M., Loeffler, I.K., Peterson, R.E., Flaws, J.A., Physiological role of the aryl hydrocarbon receptor in mouse ovary development (2000) Toxicol. Sci., 56, pp. 382-388
Benedict, J.C., Miller, K.P., Lin, T.M., Greenfeld, C., Babus, J.K., Peterson, R.E., Flaws, J.A., Aryl hydrocarbon receptor regulates growth, but not atresia, of mouse preantral and antral follicles (2003) Biol. Reprod., 68, pp. 1511-1517
Bussmann, U.A., Baranao, J.L., Regulation of aryl hydrocarbon receptor expression in rat granulosa cells (2006) Biol. Reprod., 75, pp. 360-369
Chaffin, C.L., Trewin, A., Hutz, R.J., Estrous cycle-dependent changes in the expression of aromatic hydrocarbon receptor (AHR) and AHR-nuclear translocator (ARNT) mRNAs in the rat ovary and liver (2000) Chem. Biol. Interact., 124, pp. 205-216
Cheng, G., Weihua, Z., Mäkinen, S., Mäkelä, S., Saji, S., Warner, M., Gustafsson, J.A., Hovatta, O., A role for the androgen receptor in follicular atresia of estrogen receptor beta knockout mouse ovary (2002) Biol. Reprod., 66, pp. 77-84
Davis, B.J., Lennard, D.E., Lee, C.A., Tiano, H.F., Morham, S.G., Wetsel, W.C., Langenbach, R., Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta (1999) Endocrinology, 140, pp. 2685-2695
Davis, B.J., Mccurdy, E.A., Miller, B.D., Lucier, G.W., Tritscher, A.M., Ovarian tumors in rats induced by chronic 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin treatment (2000) Cancer Res., 60, pp. 5414-5419
Faletti, A., Viggiano, J.M., Gimeno, M.A., Beta-endorphin inhibits prostaglandin synthesis in rat ovaries and blocks induced ovulation (1995) Prostaglandins, 49, pp. 93-103
Fukuda, I., Mukai, R., Kawase, M., Yoshida, K., Ashida, H., Interaction between the aryl hydrocarbon receptor and its antagonists, flavonoids (2007) Biochem. Biophys. Res. Commun., 359, pp. 822-827
Gao, X., Son, D.S., Terranova, P.F., Rozman, K.K., Toxic equivalency factors of polychlorinated dibenzo-p-dioxins in an ovulation model: validation of the toxic equivalency concept for one aspect of endocrine disruption (1999) Toxicol. Appl. Pharmacol., 157, pp. 107-116
Gao, X., Terranova, P.F., Rozman, K.K., Effects of polychlorinated dibenzofurans, biphenyls, and their mixture with dibenzo-p-dioxins on ovulation in the gonadotrophin-primed immature rat: support for the toxic equivalency concept (2000) Toxicol. Appl. Pharmacol., 163, pp. 115-124
Gasiewicz, T.A., Rucci, G., Alpha-naphthoflavone acts as an antagonist of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin by forming an inactive complex with the Ah receptor (1991) Mol. Pharmacol., 40, pp. 607-612
Gasiewicz, T.A., Kende, A.S., Rucci, G., Whitney, B., Willey, J.J., Analysis of structural requirements for Ah receptor antagonist activity: ellipticines, flavones, and related compounds (1996) Biochem. Pharmacol., 52, pp. 1787-1803
Gaytán, M., Bellido, C., Morales, C., Sánchez-Criado, J.E., Gaytán, F., Effects of selective inhibition of cyclooxygenase and lipooxygenase pathways in follicle rupture and ovulation in the rat (2006) Reproduction, 132, pp. 571-577
Hahn, M.E., Aryl hydrocarbon receptors: diversity and evolution (2002) Chem. Biol. Interact., 141, pp. 131-160
Harper, P.A., Riddick, D.S., Okey, A.B., Regulating the regulator: factors that control levels and activity of the aryl hydrocarbon receptor (2006) Biochem. Pharmacol., 72, pp. 267-279
Henry, E.C., Gasiewicz, T.A., Agonist but not antagonist ligands induce conformational change in the mouse aryl hydrocarbon receptor as detected by partial proteolysis (2003) Mol. Pharmacol., 63, pp. 392-400
Hernandez-Ochoa, I., Barnett-Ringgold, K.R., Dehlinger, S.L., Gupta, R.K., Leslie, T.C., Roby, K.F., Flaws, J.A., The ability of the aryl hydrocarbon receptor to regulate ovarian follicle growth and estradiol biosynthesis in mice depends on stage of sexual maturity (2010) Biol. Reprod., 83, pp. 698-706
Hombach-Klonisch, S., Pocar, P., Kietz, S., Klonisch, T., Molecular actions of polyhalogenated arylhydrocarbons (PAHs) in female reproduction (2005) Curr. Med. Chem., 12, pp. 599-616
Hu, Y.C., Wang, P.H., Yeh, S., Wang, R.S., Xie, C., Xu, Q., Zhou, X., Chang, C., Subfertility and defective folliculogenesis in female mice lacking androgen receptor (2004) Proc. Natl Acad. Sci. USA, 101, pp. 11209-11214
Johnson, J., Canning, J., Kaneko, T., Pru, J.K., Tilly, J.L., Germline stem cells and follicular renewal in the postnatal mammalian ovary (2004) Nature, 428, pp. 145-150
Johnson, J., Bagley, J., Skaznik-Wikiel, M., Lee, H.J., Adams, G.B., Niikura, Y., Tschudy, K.S., Tilly, J.L., Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood (2005) Cell, 122, pp. 303-315
Lu, Y.F., Santostefano, M., Cunningham, B.D., Threadgill, M.D., Safe, S., Substituted flavones as aryl hydrocarbon (Ah) receptor agonists and antagonists (1996) Biochem. Pharmacol., 51, pp. 1077-1087
Mandal, P.K., Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology (2005) J. Comp. Physiol. B, 175, pp. 221-230
Matikainen, T., Perez, G.I., Jurisicova, A., Pru, J.K., Schlezinger, J.J., Ryu, H.Y., Laine, J., Tilly, J.L., Aromatic hydrocarbon receptor-driven Bax gene expression is required for premature ovarian failure caused by biohazardous environmental chemicals (2001) Nat. Genet., 28, pp. 355-360
Matikainen, T.M., Moriyama, T., Morita, Y., Perez, G.I., Korsmeyer, S.J., Sherr, D.H., Tilly, J.L., Ligand activation of the aromatic hydrocarbon receptor transcription factor drives Bax-dependent apoptosis in developing fetal ovarian germ cells (2002) Endocrinology, 143, pp. 615-620
Mattison, D.R., Thorgeirsson, S.S., Ovarian aryl hydrocarbon hydroxylase activity and primordial oocyte toxicity of polycyclic aromatic hydrocarbons in mice (1979) Cancer Res., 39, pp. 3471-3475
Mimura, J., Fujii-Kuriyama, Y., Functional role of AhR in the expression of toxic effects by TCDD (2003) Biochim. Biophys. Acta, 1619, pp. 263-268
Mizuyachi, K., Son, D.S., Rozman, K.K., Terranova, P.F., Alteration in ovarian gene expression in response to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin: reduction of cyclooxygenase-2 in the blockage of ovulation (2002) Reprod. Toxicol., 16, pp. 299-307
Muskhelishvili, L., Wingard, S.K., Latendresse, J.R., Proliferating cell nuclear antigen-a marker for ovarian follicle counts (2005) Toxicol. Pathol., 33, pp. 365-368
Myers, M., Britt, K.L., Wreford, N.G., Ebling, F.J., Kerr, J.B., Methods for quantifying follicular numbers within the mouse ovary (2004) Reproduction, 127, pp. 569-580
Pocar, P., Fischer, B., Klonisch, T., Hombach-Klonisch, S., Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction (2005) Reproduction, 129, pp. 379-389
Reese, J., Zhao, X., Ma, W.G., Brown, N., Maziasz, T.J., Dey, S.K., Comparative analysis of pharmacologic and/or genetic disruption of cyclooxygenase-1 and cyclooxygenase-2 function in female reproduction in mice (2001) Endocrinology, 142, pp. 3198-3206
Reiners, J.J., Clift, R., Mathieu, P., Suppression of cell cycle progression by flavonoids: dependence on the aryl hydrocarbon receptor (1999) Carcinogenesis, 20, pp. 1561-1566
Robles, R., Morita, Y., Mann, K.K., Perez, G.I., Yang, S., Matikainen, T., Sherr, D.H., Tilly, J.L., The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse (2000) Endocrinology, 141, pp. 450-453
Scalbert, A., Williamson, G., Dietary intake and bioavailability of polyphenols (2000) J. Nutr., 130, pp. 2073S-2085S
Shimada, T., Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons (2006) Drug Metab. Pharmacokinet., 21, pp. 257-276
Sirois, J., Sayasith, K., Brown, K.A., Stock, A.E., Bouchard, N., Doré, M., Cyclooxygenase-2 and its role in ovulation: a 2004 account (2004) Hum. Reprod. Update, 10, pp. 373-385
Son, D.S., Ushinohama, K., Gao, X., Taylor, C.C., Roby, K.F., Rozman, K.K., Terranova, P.F., 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin (TCDD) blocks ovulation by a direct action on the ovary without alteration of ovarian steroidogenesis: lack of a direct effect on ovarian granulosa and thecal-interstitial cell steroidogenesis in vitro (1999) Reprod. Toxicol., 13, pp. 521-530
Thompson, K.E., Bourguet, S.M., Christian, P.J., Benedict, J.C., Sipes, I.G., Flaws, J.A., Hoyer, P.B., Differences between rats and mice in the involvement of the aryl hydrocarbon receptor in 4-vinylcyclohexene diepoxide-induced ovarian follicle loss (2005) Toxicol. Appl. Pharmacol., 203, pp. 114-123
Tilly, J.L., Johnson, J., Recent arguments against germ cell renewal in the adult human ovary: is an absence of marker gene expression really acceptable evidence of an absence of oogenesis? (2007) Cell Cycle, 6, pp. 879-883
Zhang, S., Qin, C., Safe, S.H., Flavonoids as aryl hydrocarbon receptor agonists/antagonists: effects of structure and cell context (2003) Environ. Health Perspect., 111, pp. 1877-1882
ISSN:0041008X
DOI:10.1016/j.taap.2011.01.007