Pubertal timing after neonatal diethylstilbestrol exposure in female rats: Neuroendocrine vs peripheral effects and additive role of prenatal food restriction.
Pubertal timing after neonatal diethylstilbestrol exposure in female rats, Neuroendocrine vs peripheral effects and additive role of prenatal food restriction.pdf
[en] We studied the effects of neonatal exposure to diethylstilbestrol (DES) on pubertal timing in female rats. We examined associated neuroendocrine changes and effects of prenatal food restriction. Age at vaginal opening was advanced after exposure to 10mug/kg/d of DES and delayed after 1mug/kg/d (subcutaneous injections). Using this lower dose, pulsatile GnRH secretion was slower at 25 days of age. Both doses reduced KiSS1 mRNA levels at 15 days of age. Using functional Kisspeptin promoter assay, 1 or 10muM DES reduced or increased KISS1 transcription, respectively. Leptin stimulatory effect on GnRH secretion in vitro (15 days of age) was reduced after prenatal food restriction and neonatal DES exposure (higher dose), both effects being cumulative. Thus, alterations in pubertal timing by DES neonatally are not unequivocally toward precocity, the level of exposure being critical. We provide evidence of neuroendocrine disruption and interaction with prenatal food availability.
Franssen, Delphine ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Ioannou, Yiannis S.
Alvarez-Real, Alexandra
Gerard, Arlette
Mueller, Johanna K.
Heger, Sabine
Bourguignon, Jean-Pierre ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Parent, Anne-Simone ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Language :
English
Title :
Pubertal timing after neonatal diethylstilbestrol exposure in female rats: Neuroendocrine vs peripheral effects and additive role of prenatal food restriction.
Publication date :
April 2014
Journal title :
Reproductive Toxicology
ISSN :
0890-6238
eISSN :
1873-1708
Publisher :
Elsevier, Netherlands
Issue :
44
Pages :
63-72
Peer reviewed :
Peer Reviewed verified by ORBi
Commentary :
Copyright (c) 2013 Elsevier Inc. All rights reserved. Epub ahead of print
Gorski R.A. Influence of age on the response to paranatal administration of a low dose of androgen. Endocrinology 1968, 82:1001-1004.
Bourguignon J.P., Rasier G., Lebrethon M.C., Gerard A., Naveau E., Parent A.S. Neuroendocrine disruption of pubertal timing and interactions between homeostasis of reproduction and energy balance. Mol Cell Endocrinol 2010, 324:110-120.
Viglietti-Panzica C., Montoncello B., Mura E., Pessatti M., Panzica G. Organizational effects of diethylstilbestrol on brain vasotocin and sexual behavior in male quail. Brain Res Bull 2005, 65:225-233.
Rothschild T.C., Calhoon R.E., Boylan E.S. Effects of diethylstilbestrol exposure in utero on the genital tracts of female ACI rats. Exp Mol Pathol 1988, 48:59-76.
Levy J.R., Faber K.A., Ayyash L., Hughes C.L. The effect of prenatal exposure to the phytoestrogen genistein on sexual differentiation in rats. Proc Soc Exp Biol Med 1995, 208:60-66.
Ashby J., Tinwell H., Lefevre P.A., Odum J., Paton D., Millward S.W., et al. Normal sexual development of rats exposed to butyl benzyl phthalate from conception to weaning. Regul Toxicol Phaarmacol 1997, 26:102-118.
Kwon S., Stedman D.B., Elswick B.A., Cattley R.C., Welsch F. Pubertal development and reproductive functions of Crl:CD BR Sprague-Dawley rats exposed to bisphenol A during prenatal and postnatal development. Toxicol Sci 2000, 55:399-406.
Odum J., Lefevre P.A., Tinwell H., Van Miller J.P., Joiner R.L., Chapin R.E., et al. Comparison of the developmental and reproductive toxicity of diethylstilbestrol administered to rats in utero, lactationally, preweaning, or postweaning. Toxicol Sci 2002, 68:147-163.
Honma S., Suzuki A., Buchanan D.L., Katsu Y., Watanabe H., Iguchi T. Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod Toxicol 2002, 16:117-122.
Kubo K., Arai O., Omura M., Watanabe R., Ogata R., Aou S. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci Res 2003, 45:345-356.
Willoughby K.N., Sarkar A.J., Boyadjieva N.I., Sarkar D.K. Neonatally administered tert-octylphenol affects onset of puberty and reproductive development in female rats. Endocrine 2005, 26:161-168.
Herbst A.L., Ulfelder H., Poskanzer D.C. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 1971, 284:878-881.
Newbold R.R., Jefferson W.N., Grissom S.F., Padilla-Banks E., Snyder R.J., Lobenhofer E.K. Developmental exposure to diethylstilbestrol alters uterine gene expression that may be associated with uterine neoplasia later in life. Mol Carcinog 2007, 46:783-796.
Newbold R.R., Padilla-Banks E., Snyder R.J., Jefferson W.N. Developmental exposure to estrogenic compounds and obesity. Birth Defects Res A: Clin Mol Teratol 2005, 73:478-480.
Nikaido Y., Yoshizawa K., Danbara N., Tsujita-Kyutoku M., Yuri T., Uehara N., et al. Effects of maternal xenoestrogen exposure on development of the reproductive tract and mammary gland in female CD-1 mouse offspring. Reprod Toxicol 2004, 18:803-811.
Gluckman P.D., Hanson M.A. Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med 2004, 9:419-425.
Sloboda D.M., Howie G.J., Pleasants A., Gluckman P.D., Vickers M.H. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS ONE 2009, 4:e6744.
Ibanez L., Jaramillo A., Enriquez G., Miro E., Lopez-Bermejo A., Dunger D., et al. Polycystic ovaries after precocious pubarche: relation to prenatal growth. Hum Reprod 2007, 22:395-400.
Ibanez L., Ong K., Dunger D.B., de Zegher F. Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. J Clin Endocrinol Metab 2006, 91:2153-2158.
Barker D.J. The developmental origins of adult disease. J Am Coll Nutr 2004, 23:588S-595S.
Matagne V., Rasier G., Lebrethon M.C., Gerard A., Bourguignon J.P. Estradiol stimulation of pulsatile gonadotropin-releasing hormone secretion in vitro: correlation with perinatal exposure to sex steroids and induction of sexual precocity in vivo. Endocrinology 2004, 145:2775-2783.
Pinilla L., Aguilar E., Dieguez C., Millar R.P., Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev 2012, 92:1235-1316.
Iwasa T., Matsuzaki T., Murakami M., Fujisawa S., Kinouchi R., Gereltsetseg G., et al. Effects of intrauterine undernutrition on hypothalamic Kiss1 expression and the timing of puberty in female rats. J Physiol 2010, 588:821-829.
Navarro V.M., Sanchez-Garrido M.A., Castellano J.M., Roa J., Garcia-Galiano D., Pineda R., et al. Persistent impairment of hypothalamic KiSS-1 system after exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology 2009, 150:2359-2367.
Newbold R.R., Padilla-Banks E., Jefferson W.N., Heindel J.J. Effects of endocrine disruptors on obesity. Int J Androl 2008, 31:201-208.
Lebrethon M.C., Aganina A., Fournier M., Gerard A., Parent A.S., Bourguignon J.P. Effects of in vivo and in vitro administration of ghrelin, leptin and neuropeptide mediators on pulsatile gonadotrophin-releasing hormone secretion from male rat hypothalamus before and after puberty. J Neuroendocrinol 2007, 19:181-188.
Lebrethon M.C., Vandersmissen E., Gerard A., Parent A.S., Junien J.L., Bourguignon J.P. In vitro stimulation of the prepubertal rat gonadotropin-releasing hormone pulse generator by leptin and neuropeptide Y through distinct mechanisms. Endocrinology 2000, 141:1464-1469.
Bouret S.G., Draper S.J., Simerly R.B. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 2004, 304:108-110.
Vickers M.H., Breier B.H., Cutfield W.S., Hofman P.L., Gluckman P.D. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 2000, 279:E83-E87.
Yura S., Itoh H., Sagawa N., Yamamoto H., Masuzaki H., Nakao K., et al. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab 2005, 1:371-378.
Goldman J.M., Murr A.S., Cooper R.L. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res B: Dev Reprod Toxicol 2007, 80:84-97.
Li Y., Kumazawa T., Ishiguro T., Kawakami Y., Nishitani H., Tagawa Y., et al. Hypothyroidism caused by phenobarbital affects patterns of estrous cyclicity in rats. Congenit Anom (Kyoto) 2011, 51:55-61.
Bourguignon J.P., Gerard A., Mathieu J., Mathieu A., Franchimont P. Maturation of the hypothalamic control of pulsatile gonadotropin-releasing hormone secretion at onset of puberty. I: Increased activation of N-methyl-d-aspartate receptors. Endocrinology 1990, 127:873-881.
Bourguignon J.P., Franchimont P. Puberty-related increase in episodic LHRH release from rat hypothalamus in vitro. Endocrinology 1984, 114:1941-1943.
Bourguignon J.P., Gerard A., Franchimont P. Direct activation of gonadotropin-releasing hormone secretion through different receptors to neuroexcitatory amino acids. Neuroendocrinology 1989, 49:402-408.
Bourguignon J.P., Gerard A., Mathieu J., Simons J., Franchimont P. Pulsatile release of gonadotropin-releasing hormone from hypothalamic explants is restrained by blockade of N-methyl-d,l-aspartate receptors. Endocrinology 1989, 125:1090-1096.
Dluzen D.E., Ramirez V.D. Presence and localization of immunoreactive luteinizing hormone-releasing hormone (LHRH) within the olfactory bulbs of adult male and female rats. Peptides 1981, 2:493-496.
Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25:402-408.
Mueller J.K., Dietzel A., Lomniczi A., Loche A., Tefs K., Kiess W., et al. Transcriptional regulation of the human KiSS1 gene. Mol Cell Endocrinol 2011, 342:8-19.
Mellon P.L., Windle J.J., Goldsmith P.C., Padula C.A., Roberts J.L., Weiner R.I. Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 1990, 5:1-10.
Bourguignon J.P., Gerard A., Alvarez Gonzalez M.L., Franchimont P. Neuroendocrine mechanism of onset of puberty. Sequential reduction in activity of inhibitory and facilitatory N-methyl-d-aspartate receptors. J Clin Invest 1992, 90:1736-1744.
Newbold R.R., Jefferson W.N., Padilla-Banks E., Haseman J. Developmental exposure to diethylstilbestrol (DES) alters uterine response to estrogens in prepubescent mice: low versus high dose effects. Reprod Toxicol 2004, 18:399-406.
Rasier G., Parent A.S., Gerard A., Lebrethon M.C., Bourguignon J.P. Early maturation of gonadotropin-releasing hormone secretion and sexual precocity after exposure of infant female rats to estradiol or dichlorodiphenyltrichloroethane. Biol Reprod 2007, 77:734-742.
Rasier G., Parent A.S., Gerard A., Denooz R., Lebrethon M.C., Charlier C., et al. Mechanisms of interaction of endocrine-disrupting chemicals with glutamate-evoked secretion of gonadotropin-releasing hormone. Toxicol Sci 2008, 102:33-41.
Fernandez M., Bianchi M., Lux-Lantos V., Libertun C. Neonatal exposure to bisphenol a alters reproductive parameters and gonadotropin releasing hormone signaling in female rats. Environ Health Perspect 2009, 117:757-762.
Adewale H.B., Jefferson W.N., Newbold R.R., Patisaul H.B. Neonatal bisphenol-a exposure alters rat reproductive development and ovarian morphology without impairing activation of gonadotropin-releasing hormone neurons. Biol Reprod 2009, 81:690-699.
Seminara S.B. Mechanisms of disease: the first kiss-a crucial role for kisspeptin-1 and its receptor, G-protein-coupled receptor 54, in puberty and reproduction. Nat Clin Pract Endocrinol Metab 2006, 2:328-334.
Roth C.L., Mastronardi C., Lomniczi A., Wright H., Cabrera R., Mungenast A.E., et al. Expression of a tumor-related gene network increases in the mammalian hypothalamus at the time of female puberty. Endocrinology 2007, 148:5147-5161.
Patisaul H.B., Todd K.L., Mickens J.A., Adewale H.B. Impact of neonatal exposure to the ERalpha agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology 2009, 30:350-357.
Bateman H.L., Patisaul H.B. Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus. Neurotoxicology 2008, 29:988-997.
Takumi K., Iijima N., Ozawa H. Developmental changes in the expression of kisspeptin mRNA in rat hypothalamus. J Mol Neurosci 2011, 43:138-145.
Newbold R.R., Padilla-Banks E., Jefferson W.N. Environmental estrogens and obesity. Mol Cell Endocrinol 2009, 304:84-89.
Rubin B.S., Murray M.K., Damassa D.A., King J.C., Soto A.M. Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. Environ Health Perspect 2001, 109:675-680.
Palou M., Konieczna J., Torrens J.M., Sanchez J., Priego T., Fernandes M.L., et al. Impaired insulin and leptin sensitivity in the offspring of moderate caloric-restricted dams during gestation is early programmed. J Nutr Biochem 2012, 23:1627-1639.
Bautista C.J., Boeck L., Larrea F., Nathanielsz P.W., Zambrano E. Effects of a maternal low protein isocaloric diet on milk leptin and progeny serum leptin concentration and appetitive behavior in the first 21 days of neonatal life in the rat. Pediatr Res 2008, 63:358-363.
