Mechanisms of Interaction of Endocrine-Disrupting Chemicals with Glutamate-Evoked Secretion of Gonadotropin-Releasing Hormone

Rasier, Gregory; Parent, Anne-Simone; Gerard, Arlette; Denooz, Raphael; Lebrethon, Marie-Christine; Charlier, Corinne; Bourguignon, Jean-Pierre

doi:10.1093/toxsci/kfm285

Article (Scientific journals)

Mechanisms of Interaction of Endocrine-Disrupting Chemicals with Glutamate-Evoked Secretion of Gonadotropin-Releasing Hormone

Rasier, Gregory; Parent, Anne-Simone; Gerard, Arlette et al.

2008 • In Toxicological Sciences, 102 (1), p. 33-41

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/69894

DOI
10.1093/toxsci/kfm285

PubMed
18032409

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Abstract :

[en] In previous studies, we detected a dichlorodiphenyltrichloroethane (DDT) derivative in the serum of children with sexual precocity after migration from developing countries. Recently, we reported that DDT stimulated pulsatile gonadotropin-releasing hormone (GnRH) secretion and sexual maturation in the female rat. The aim of this study was to delineate the mechanisms of interaction of endocrine-disrupting chemicals including DDT with GnRH secretion evoked by glutamate in vitro. Using hypothalamic explants obtained from 15-day-old female rats, estradiol (E2) and DDT caused a concentration-related increase in glutamate-evoked GnRH release while p,p'-dichlorodiphenyldichloroethene and methoxychlor had no effect. The effective DDT concentrations in vitro were consistent with the serum concentrations measured in vivo 5 days after exposure of immature rats to 10 mg/kg/day of o,p'-DDT. Bisphenol A induced some stimulatory effect, whereas no change was observed with 4-nonylphenol. The o,p'-DDT effects in vitro were prevented partially by a selective antagonist of the alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) subtype of glutamate receptors. A complete prevention of o,p'-DDT effects was caused by an estrogen receptor (ER) antagonist as well as an aryl hydrocarbon receptor (AHR) antagonist and inhibitors of protein kinases A and C and mitogen-activated kinases. While an intermittent incubation with E2 caused no change in amplification of the glutamate-evoked GnRH release for 4 h, continuous incubation with E2 or o,p'-DDT caused an increase of this amplification after 3.5 h of incubation. In summary, DDT amplifies the glutamate-evoked GnRH secretion in vitro through rapid and slow effects involving ER, AHR, and AMPA receptor mediation.

Disciplines :

Environmental sciences & ecology
Anatomy (cytology, histology, embryology...) & physiology

Author, co-author :

Rasier, Gregory ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie

Parent, Anne-Simone ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie

Gerard, Arlette ; Centre Hospitalier Universitaire de Liège - CHU > Pédiatrie

Denooz, Raphael ; Centre Hospitalier Universitaire de Liège - CHU > Toxicologie clinique

Lebrethon, Marie-Christine ; Centre Hospitalier Universitaire de Liège - CHU > Pédiatrie

Charlier, Corinne ; Université de Liège - ULiège > Département de pharmacie > Chimie toxicologique

Bourguignon, Jean-Pierre ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie - IFRES

Language :

English

Title :

Mechanisms of Interaction of Endocrine-Disrupting Chemicals with Glutamate-Evoked Secretion of Gonadotropin-Releasing Hormone

Publication date :

March 2008

Journal title :

Toxicological Sciences

ISSN :

1096-6080

eISSN :

1096-0929

Publisher :

Oxford University Press, United Kingdom

Volume :

102

Issue :

Pages :

33-41

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

DG RDT - Commission Européenne. Direction Générale de la Recherche et de l'Innovation
BSGPE - Belgian Study Group for Pediatric Endocrinology
Fonds Léon Fredericq

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since 23 August 2010

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Bibliography

Abraham, I. M., Todman, M. G., Korach, K. S., and Herbison, A. E. (2004). Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signalling in mouse brain. Endocrinology 145, 3055-3061.
Adachi, S., Yamada, S., Takatsu, Y., Matsui, H., Kinoshita, M., Takase, K., Sugiura, H., Ohtaki, T., Matsumoto, H., Uenoyama, Y., et al. (2007). Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J. Reprod. Dev. 53, 367-378.
Bourgaignon, J. P., Gérard, A., and Franchimont, P. (1989a). Direct activation of gonadotropin-releasing hormone secretion through different receptors to neuroexcitatory amino acids. Neuroendocrinology 49 402-408.
Bourguignon, J. P., Gérard, A., Mathieu, J., Simons, J., and Franchimont, P. (1989b). Pulsatile release of gonadotropin-releasing hormone from hypothalamic explants is restrained by blockade of N-methyl-D-aspartate receptors. Endocrinology 125, 1090-1096.
Buck-Louis, G. M., Gray, L. E., Jr, Michele Marcus, M., Ojeda, S., Pescovitz, O. A., Feldman Witchel, S., Sippell, W., Abbott, D. A., Soto, A., Tyl, R. W., et al. (2008). Environmental factors and puberty timing. Expert panel research needs. Pediatrics (in press).
Charlier, C., and Plomteux, G. (2002). Determination of organochlorine pesticides residues in the blood of healthy individuals. Clin. Chem. Lab. Med. 40, 361-364.
Clark, E. J., Norris, D. O., and Jones, R. E. (1998). Interactions of gonadal steroids and pesticides (DDT and DDE) on gonadal duct in larval tiger salamanders Ambystoma tigrinum. Gen. Comp. Endocrinol. 109, 94-105.
de Roux, N., Genin, E., Carel, J. C., Matsuda, F., Chaussain, J. L., and Milgrom, E. (2003). Hypogonadotropic hypogonadism due to loss of function of the kiss-1-derived peptide receptor GPR54. Proc. Natl. Acad. Sci. U.S.A. 100, 10972-10976.
Desaulniers, D., Cooke, G. M., Leingartner, K., Soumano, K., Cole, J., Yang, J., Wade, M., and Yagminas, A. (2005). Effects of postnatal exposure to a mixture of polychlorinated biphenyls, pp'-dichlorodiphenyltrichloroethane, and p,p'-dichlorodiphenyldichloroethene in prepubertal and adult female Sprague-Dawley rats. Int. J. Toxicol. 24, 111-127.
Diano, S., Naftolin, F., and Horvath, T. L. (1997). Gonadal steroids target AMPA glutamate receptor-containing neurons in the rat hypothalamus, septum and amygdala: A morphological and biochemical study. Endocrinology 138, 778-789.
Diel, P., Olff, S., Schmidt, S., and Michna, H. (2002). Effects of the environmental estrogens bisphenol A, o,p'-DDT, p-tert-octylphenol, and coumestrol on apoptosis induction, cell proliferation, and the expression of estrogen sensitive molecular parameters in the human breast cancer cell line MCF-7. J. Steroid Biochem. Mol. Biol. 80, 61-70.
Dluzen, D. E., and Ramirez, V. D. (1981). Presence and localization of immunoreactive luteinizing hormone-releasing hormone within the olfactory bulbs of adult male and female rats. Peptides 2, 493-496.
Donoso, A. O., Lopez, F. J., and Negro-Vilar, A. (1990). Glutamate-receptors of the non-N-methyl-D-aspartic acid type mediate the increase in luteinizing hormone-releasing hormone release by excitatory amino acids in vitro. Endocrinology 126, 414-420.
Gellert, R. J., Heinrichs, W. L., and Swerdloff, R. S. (1972). DDT homologues: Estrogen-like effects on the vagina, uterus, and pituitary of the rat. Endocrinology 91, 1095-1100.
Gu, Q., Korach, K. S., and Moss, R. L. (1999). Rapid action of 17β-estradiol on. kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors. Endocrinology 140, 660-666.
Harper, P. A., Riddick, D. S., and Okey, A. B. (2006). Regulating the regulator: Factors that control levels and activity of the aryl hydrocarbon receptor. Biochem. Pharmacol. 72, 267-279.
Heinrichs, W. L., Gellert, R. J., Bakke, J. L., and Lawrence, N. L. (1971). DDT administered to neonatal rats induces persistent estrus syndrome. Science 173, 642-643.
Herbison, A. E. (1998). Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr. Rev. 19, 302-330.
Herbison, A. E., and Pape, J. R. (2001). New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front. Neuroendocrinol. 22, 292-308.
Herman-Giddens, M. E., Slora, E. J., Wasserman, R. C., Bourdony, C. J., Bhapkar, M. V., Koch, G. G., and Hasemeier, C. M. (1997). Secondary sexual characteristics and menses in young girls seen in office practice: A study from the paediatric research in office settings network. Pediatrics 99, 505-512.
Improta-Brears, T., Whorton, A. R., Codazzi, F., York, J. D., Meyer, T., and McDonnell, D. P. (1999). Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium. Proc. Natl. Acad. Sci. U.S.A. 96, 4686-4691.
Kelce, W. R., Stone, C. R., Laws, S. C., Gray, L. E., Kemppainen. J. A, and Wilson, E. M. (1995). Persistent DDT metabolite pp'-DDE is a potent androgen receptor antagonist. Nature 375, 581-585.
Krstevska-Konstantinova, M., Charlier, C., Craen, M., Du Caju, M., Heinrichs, C., de Beaufort C, Plomteux, G.; and Bourguignon, J. P. (2001). Sexual precocity after immigration from developing countries to Belgium: Evidence of previous exposure to organochlorine pesticides. Hum. Reprod. 16, 1020-1026.
Kuehl-Kovarik, M. C., Pouliot, W. A., Halterman, G. L., Handa, R. J., Dudek, F. E., and Partin, K. M. (2002). Episodic bursting activity and response to excitatory amino acids in acutely dissociated gonadotropin-releasing hormone neurons genetically targeted with green fluorescent protein. J. Neurosci. 22, 2313-2322.
Kwon, A., Stedman, D. B., Elswick, B. A., Cattley, R. C., and Welsch, F. (2000). Pubertal development and reproductive functions of Crl: CDBR Sprague-Dawley rats exposed to bisphenol A during prenatal and postnatal development. Toxicol. Sci. 55, 399-406.
Lagrange, A. H., Wagner, E. J., Ronnekleiv, O. K., and Kelly, M. J. (1999). Rapid effects of estrogen to modulate G protein-coupled receptors via activation of protein kinase A and protein kinase C pathways. Steroids 64, 64-75.
Lee, P. A., Guo, S. S., and Kulin, H. E. (2001). Age of puberty: Data from the United States of America. APMIS 109, 81-88.
Matagne, V., Lebrethon, M. C., Gérard, A., and Bourguignon, J. P. (2005). Kainate/estrogen receptors and intracelular signalling pathways involved in estradiol rapid effects on gonadotropin-releasing hormone secretion in vitro. Endocrinology 146, 2313-2323.
Matagne, V., Rasier, G., Lebrethon, M. C., Gérard, A., and Bourguignon, J. P. (2004). Estradiol stimulation of pulsatile gonadotropin-releasing hormone secretion in vitro: Correlation with pennatal exposure to sex steroids and induction of sexual precocity in vivo. Endocrinology 145, 2775-2783.
Miller, K. P., Gupta, R. K., and Flaws, J. A. (2006). Methoxychlor metabolites may cause ovarian toxicity through estrogen-regulated pathways. Toxicol. Sci. 93, 180-188.
Mussi, P., Ciana, P., Raviscioni, M., Villa, R., Regondi, S., Agradi, E., Maggi, A., and Di Lorenzo, D. (2005). Activation of brain estrogen receptors in mice lactating from mothers exposed to DDT. Brain Res. Bull. 65, 241-247.
Ohtake, F., Takeyama, K. I., Matsumoto, T., Kitagawa, H., Yamamoto, Y., Nohara, K., Tohyarna, C., Krust, A., Mimura, J., Chambon, P., et al (2003). Modulation of estrogen receptor signalling by association with the activated dioxin receptor. Nature 423, 545-550.
Ojeda, S. R., and Urbanski, H. F. (1994). Puberty in the Rat. In In the Physiology of Reproduction. (E. Knobil and J. D. Neil, Eds.), Vol. 2, pp. 363-409. Raven Press Ltd, New York.
Papanicolaou, G. N., and Traut, H. F. (1941). The diagnostic value of vaginal smears in carcinoma of the uterus. Arch. Pathol. Lab. Med. 121, 211-224.
Parent, A. S., Lebrethon, M. C., Gérard, A., and Bourguignon, J. P. (2005). Factors accounting for perinatal occurrence of pulsatile gonadotropin-releasing hormone secretion in vitro. Biol. Reprod. 72, 143-149.
Parent, A. S., Teilmann, G., Juul, A., Skakkebaek, N. E., Toppari, J., and Bourguignon, J. P. (2003). The timing of normal puberty and the age limits of sexual precocity: Variations around the world, secular trends, and changes after migration: Endocr. Rev. 24, 668-693.
Rasier, G., Parent, A. S., Géard, A., Lebrethon, M. C., and Bourguignon, J. P. (2007). Early maturation of gonadotropin-releasing hormone secretion and sexual precocity after exposure of infant female rats to estradiol or dichlorodiphenyltrichloroethane. Biol. Reprod. 77, 734-742.
Rasier, G., Toppari, J., Parent, A. S., and Bourguignon, J. P. (2006). Female sexual maturation and reproduction after prepubertal exposure to estrogens and endocrine disrupting chemicals: A review of rodent and human data. Mol. Cell. Endocrinol. 254-255, 187-201.
Rubin, B. S., Lenkowski, J. R., Schaeberle, C. M., Vandenberg, L. N., Ronsheim, P. M., and Soto, A. (2006). Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A Endocrinology 147, 3681-3691.
Seminara, S. B., and Kaiser, U. B. (2005). New gatekeepers of reproduction GPR54 and its cognate ligand, kiss-1. Endocrinology 146, 1686-1698.
Teilmann, G., Pedersen, C. B., Skakkebæk, N. E., and Jensen, T. K. (2006). Increased risk of precocious puberty in internationally adopted children in Denmark. Pediatrics 118, 391-399.
Toad, B. J., Schwarz, J. M., Mong, J. A., and McCarthy, M. M. (2007). Glutamate AMPA/kainate receptors, not GABA(A) receptors, mediate estradiol-induced sex differences in the hypothalamus. Dev. Neurobiol. 67, 304-315.
Tomiyama, N., Watanabe, M., Takeda, M., Harada, T., and Kobayashi, H. (2003). A comparative study on the reliability of toxicokinetic parameters for predicting hepatotoxicity of DDT in rats receiving a single or repeated administration. J. Toxicol. Sci. 28, 403-413.
Tsurugizawa, T., Mukai, H., Tanabe, N., Murakami, G. Hojo, Y., Kominami, S., Mitsushashi, K., Komatsuzaki, Y., Morrison, J. H., Janssen, W. G. M., et al. (2005). Estrogen induces rapid decrease in dendritic thorns of CA3 pyramidal neurons in adult male rat hippocampus. Biochem. Biophys. Res. Commun. 337, 1345-1352.
Urbanski, H. F., Kohama, S. G., and Garyfallou, V. T. (1996). Mechanisms mediating the response of gonadotropin-releasing hormone neurons to excitatory amino adds. Rev. Reprod. 1, 173-181.