Delayed neuroendocrine sexual maturation in female rats after a very low dose of Bisphenol A through altered GABAergic neurotransmission and opposing effects of a high dose.

Franssen, Delphine; GERARD, Arlette; HENNUY, Benoit; Donneau, Anne-Françoise; Bourguignon, Jean-Pierre; Parent, Anne-Simone

doi:10.1210/en.2015-1937

Article (Scientific journals)

Delayed neuroendocrine sexual maturation in female rats after a very low dose of Bisphenol A through altered GABAergic neurotransmission and opposing effects of a high dose.

Franssen, Delphine; GERARD, Arlette; HENNUY, Benoit et al.

2016 • In Endocrinology

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/195530

DOI
10.1210/en.2015-1937

PubMed
26950200

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Franssen 2016 Endocrinology.pdf

Publisher postprint (1.24 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Abstract :

[en] Rat sexual maturation is preceded by a reduction of the interpulse interval (IPI) of gonadotropinreleasing hormone (GnRH) neurosecretion. This work aims at studying disruption of that neuroendocrine event in females after early exposure to a very low dose of Bisphenol A (BPA), a ubiquitous endocrine disrupting chemical. Female rats were exposed to vehicle or BPA 25 ng/kg.day, 25 g/kg.day, or 5 mg/kg.day from postnatal day (PND) 1 to 5 or 15. Exposure to 25 ng/kg.day of BPA for 5 or 15 days was followed by a delay in developmental reduction of GnRH IPI studied ex vivo on PND 20. After 15 days of exposure to that low dose of BPA, vaginal opening tended to be delayed. In contrast, exposure to BPA 5 mg/kg.day for 15 days resulted in a premature reduction inGnRHIPI and a trend toward early vaginal opening. RNAseq analysis on PND20 indicated that exposure to BPA resulted in opposing dose effectsonthemRNAexpression of hypothalamic genes involved inGABAA neurotransmission. The study of GnRH secretion in vitro in the presence of GABAA receptor agonist/antagonist confirmed an increased or a reduced GABAergic tone after in vivo exposure to the very low or the high dose of BPA, respectively. Overall, we show for the first time that neonatal exposure to BPA leads to opposing dose-dependent effects on the neuroendocrine control of puberty in the female rat. A very low and environmentally relevant dose of BPA delays neuroendocrine maturation related to puberty through increased inhibitory GABAergic neurotransmission.

Disciplines :

Endocrinology, metabolism & nutrition

Author, co-author :

Franssen, Delphine ; Université de Liège > Département des sciences cliniques > Pédiatrie

GERARD, Arlette ; Centre Hospitalier Universitaire de Liège - CHU > Service de pédiatrie

HENNUY, Benoit ; Centre Hospitalier Universitaire de Liège - CHU > Centre d'oncologie

Donneau, Anne-Françoise ; Université de Liège > Département des sciences de la santé publique > Biostatistique

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

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

Language :

English

Title :

Delayed neuroendocrine sexual maturation in female rats after a very low dose of Bisphenol A through altered GABAergic neurotransmission and opposing effects of a high dose.

Publication date :

2016

Journal title :

Endocrinology

ISSN :

0013-7227

eISSN :

1945-7170

Publisher :

Endocrine Society, Chevy Chase, United States - Maryland

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 12 April 2016

Statistics

Number of views

260 (36 by ULiège)

Number of downloads

293 (17 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007; 24(2):139-77.
Parent AS, Franssen D, Fudvoye J, Gérard A, Bourguignon JP. Developmental variations in environmental influences incluDing endocrine disruptors on pubertal timing and neuroendocrine control: revision of human observations and mechanistic insight from rodents. Front Neuroendocrinol. 2015;38:12-36.
Nagao T, Yoshimura S, Saito Y, Nakagomi M, Usumi K, Ono H. Reproductive effects in male and female rats of neonatal exposure to genistein. Reprod Toxicol. 2001;15(4):399-411.
Adewale HB, Jefferson WN, Newbold RR, Patisaul HB. Neonatal bisphenol-a exposure alters rat reproductive development and ovarian morphology without impairing activation of gonadotropin-releasing hormone neurons. Biol Reprod. 2009;81(4):690-699.
Yu B, Chen QF, Liu ZP, et al. Estrogen receptor and expressions in hypothalamus-pituitary-ovary axis in rats exposed lactationally to soy isoflavones and bisphenol A. Biomed Env Sci. 2010;23(5): 357-362.
Losa-Ward SM, Todd KL, McCaffrey KA, Tsutsui K, Patisaul HB. Disrupted organization of RFamide pathways in the hypothalamus is associated with advanced puberty in female rats neonatally exposed to bisphenol A. Biol Reprod. 2012;87(2):28.
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. Env Heal Perspect. 2009;117(5):757-762.
Nah WH, Park MJ, Gye MC. Effects of early prepubertal exposure to bisphenol A on the onset of puberty, ovarian weights, and estrous cycle in female mice. Clin Exp Reprod Med. 2011;38(2):75-81.
Navarro VM, Sánchez-Garrido MA, Castellano JM, et al. Persistent impairment of hypothalamic KiSS-1 system after exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology. 2009;150(5):2359-2367.
Geens T, Aerts D, Berthot C, et al. A review of dietary and nondietary exposure to bisphenol-A. Food Chem Toxicol. 2012;50(10): 3725-3740.
Ferguson KK, Peterson KE, Lee JM, et al. Prenatal and peripubertal phthalates and bisphenol A in relation to sex hormones and puberty in boys. Reprod Toxicol. 2014;47:70-76.
Frederiksen H, Aksglaede L, Sorensen K, et al. BisphenolAand other phenols in urine from Danish children and adolescents analyzed by isotope diluted TurboFlow-LC-MS/MS. Int J Hyg Environ Health. 2013;216(6):710-720.
Lee SH, Kang SM, Choi MH, et al. Changes in steroid metabolism among girls with precocious puberty may not be associated with urinary levels of bisphenol A. Reprod Toxicol. 2014;44:1-6.
Durmaz E, Aç? A, Erkekolu P, Akçurin S, Gümüel BK, Bircan I. Urinary bisphenol a levels in girls with idiopathic central precocious puberty. J Clin Res Pediatr Endocrinol. 2014;6(1):16-21.
McGuinn LA, Ghazarian AA, Joseph Su L, Ellison GL. Urinary bisphenol A and age at menarche among adolescent girls: evidence from NHANES 2003-2010. Environ Res. 2015;136:381-386.
Bourguignon JP, Franchimont P. Puberty-related increase in episodic LHRH release from rat hypothalamus in vitro. Endocrinology. 1984;114(5):1941-1943.
Rasier G, Parent AS, Gérard A, Lebrethon MC, Bourguignon JP. Early maturation of gonadotropin-releasing hormone secretion and sexual precocity after exposure of infant female rats to estradiol or dichlorodiphenyltrichloroethane. Biol Reprod. 2007;77(4):734-742.
Franssen D, Ioannou YS, Alvarez-real A, et al. Pubertal timing after neonatal diethylstilbestrol exposure in female rats: neuroendocrine vs peripheral effects and additive role of prenatal food restriction. Reprod Toxicol. 2014;44:63-72.
Rasier G, Toppari J, Parent A-S, Bourguignon J-P. Female sexual maturation and reproduction after prepubertal exposure to estrogens and endocrine disrupting chemicals: a review of rodent and human data. Mol Cell Endocrinol. 2006;254-255:187-201.
Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev. 2003;24(5):668-693.
Matagne V, Rasier G, Lebrethon MC, Gérard A, Bourguignon JP. 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(6):2775-2783.
Keen KL, Burich AJ, Mitsushima D, Kasuya E, Terasawa E. Effects of pulsatile infusion of the GABA(A) receptor blocker bicuculline on the onset of puberty in female rhesus monkeys. Endocrinology. 1999;140(11):5257-5266.
Terasawa E. Role ofGABAin the mechanism of the onset of puberty in non-human primates. Int Rev Neurobiol. 2005;71:113-129.
Bourguignon JP, Gerard A, Purnelle G, et al. Duality of glutamatergic and GABAergic control of pulsatile GnRH secretion by rat hypothalamic explants: II. Reduced NR2C-and GABAA-receptormediated inhibition at initiation of sexual maturation. J Neuroendocrol. 1997;9(3):193-199.
Bourguignon JP, Gerard A, Purnelle G, et al. Duality of glutamatergic and GABAergic control of pulsatile GnRH secretion by rat hypothalamic explants: I. Effects of antisense oligodeoxynucleotides using explants incluDing or excluDing the preoptic area. J Neuroendocrol. 1997;9(3):183-191.
Goldman JM, Murr AS, Cooper RL. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res B Dev Reprod Toxicol. 2007;80(2):84-97.
Bourguignon JP, Gérard A, Franchimont P. Direct activation of gonadotropin-releasing hormone secretion through different receptors to neuroexcitatory amino acids. Neuroendocrinology. 1989; 49(4):402-408.
Bourguignon JP, 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(2):1090-1096.
Dluzen DE, Ramirez VD. Presence and localization of immunoreactive luteinizing hormone-releasing hormone (LHRH) within the olfactory bulbs of adult male and female rats. Peptides. 1981;2(4): 493-496.
Parent AS, Rasier G, Matagne V, et al. Oxytocin facilitates female sexual maturation through a glia-to-neuron signaling pathway. Endocrinology. 2008;149(3):1358-1365.
Trapnell C, Roberts A, Goff L, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7(3):562-578.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(C(T)) method. Methods. 2001;25(4):402-408.
Hagen CP, Sørensen K, Aksglaede L, et al. Pubertal onset in girls is strongly influenced by genetic variation affecting FSH action. Sci Rep. 2014;4:6412.
Cardoso N, Pandolfi M, Lavalle J, et al. Probable aminobutyric acid involvement in bisphenol A effect at the hypothalamic level in adult male rats. J Physiol Biochem. 2011;67(4):559-567.
Facciolo RM, Alò R, Madeo M, Canonaco M, Dessì-Fulgheri F. Early cerebral activities of the environmental estrogen bisphenol A appear to act via the somatostatin receptor subtype sst(2). Environ Health Perspect. 2002;110(suppl 3):397-402.
Cabaton NJ, Canlet C, Wadia PR, et al. Effects of low doses of bisphenol A on the metabolome of perinatally exposed CD-1 mice. Environ Health Perspect. 2013;121(5):586-593.
Ogi H, Itoh K, Ikegaya H, Fushiki S. Alterations of neurotransmitter norepinephrine and aminobutyric acid correlate with murine behavioral perturbations related to bisphenol A exposure. Brain Dev. 2015;37(8):739-746.
Zhou R, Bai Y, Yang R, et al. Abnormal synaptic plasticity in basolateral amygdala may account for hyperactivity and attentiondeficit in male rat exposed perinatally to low-dose bisphenol-A. Neuropharmacology. 2011;60(5):789-798.
Zhou R, Chen F, Chang F, Bai Y, Chen L. Persistent overexpression of DNA methyltransferase 1 attenuating GABAergic inhibition in basolateral amygdala accounts for anxiety in rat offspring exposed perinatally to low-dose bisphenol A. J Psychiatr Res. 2013;47(10): 1535-1544.
YeoM,Berglund K,HannaM,et al. BisphenolAdelays the perinatal chloride shift in cortical neurons by epigenetic effects on the Kcc2 promoter. Proc Natl Acad Sci USA. 2013;110(11):4315-4320.
Choi IS, Cho JH, Park EJ, et al. Multiple effects of bisphenol A, an endocrine disrupter, on GABA(A) receptors in acutely dissociated rat CA3 pyramidal neurons. Neurosci Res. 2007;59(1):8-17.
Bhattarai JP, Park SA, Park JB, et al. Tonic extrasynaptic GABA(A) receptor currents control gonadotropin-releasing hormone neuron excitability in the mouse. Endocrinology. 2011;152(4):1551-1561.
Li Y, Zhang W, Liu J, et al. Prepubertal bisphenol A exposure interferes with ovarian follicle development and its relevant gene expression. Reprod Toxicol. 2014;44:33-40.
Gámez JM, Penalba R, Cardoso N, et al. Exposure to a low dose of bisphenol A impairs pituitary-ovarian axis in prepubertal rats: effects on early folliculogenesis. Environ Toxicol Pharmacol. 2015; 39(1):9-15.
de Almeida OM, Gardino PF, Loureiro dos Santos NE, et al. Opposite roles of GABA and excitatory amino acids on the control of GAD expression in cultured retina cells. Brain Res. 2002;925(1): 89-99.
Bernstein EM, Quick MW. Regulation of aminobutyric acid (GABA) transporters by extracellular GABA. J Biol Chem. 1999; 274(2):889-895.
Watanabe M, Sakuma Y, Kato M. GABAA receptors mediate excitation in adult rat GnRH neurons. Biol Reprod. 2009;81(2):327-332.
Moenter SM, DeFazio RA. Endogenous aminobutyric acid can excite gonadotropin-releasing hormone neurons. Endocrinology. 2005;146(12):5374-5379.
Kusano K, Fueshko S, Gainer H, Wray S. Electrical and synaptic properties of embryonic luteinizing hormone-releasing hormone neurons in explant cultures. Proc Natl Acad Sci USA. 1995;92(9): 3918-3922.
de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA. 2003;100(19):10972-10976.
Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349(17):1614-1627.
Patisaul HB, Todd KL, Mickens JA, Adewale HB. Impact of neonatal exposure to the ER agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats. Neurotoxicology. 2009;30(3):350-357.
Bourguignon JP, Franssen D, Gerard A, et al. Early neuroendocrine disruption in hypothalamus and hippocampus: developmental effects incluDing female sexual maturation and implications for endocrine disrupting chemical screening. J Neuroendocrol. 2013; 25(11):1079-1087.
Bourguignon JP, Gerard A, Mathieu J, Mathieu A, Franchimont P. Maturation of the hypothalamic control of pulsatile gonadotropinreleasing hormone secretion at onset of puberty. I. Increased activation of N-methyl-D-aspartate receptors. Endocrinology. 1990; 127(2):873-881.
Taylor JA, Welshons WV, Vom Saal FS. No effect of route of exposure (oral; subcutaneous injection) on plasma bisphenol A throughout 24h after administration in neonatal female mice. Reprod Toxicol. 2008;25(2):169-176.
Ben-Ari Y. The GABA excitatory/inhibitory developmental sequence: a personal journey. Neuroscience. 2014;279:187-219.
Harley KG, Gunier RB, Kogut K, et al. Prenatal and early childhood bisphenol A concentrations and behavior in school-aged children. Environ Res. 2013;126:43-50.
Roen EL, Wang Y, Calafat AM, et al. Bisphenol A exposure and behavioral problems among inner city children at 7-9 years of age. Environ Res. 2015;142:739-745.
Kardas F, Bayram AK, Demirci E, et al. Increased serum phthalates (MEHP, DEHP) and bisphenol A concentrations in children with autism spectrum disorder: the role of endocrine disruptors in autism ttiopathogenesis. J Child Neurol. 2015;19:142-143.
Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009;30(4):293-342.
European Food Safety Authority. Scientific Opinion on the risks to public health related to the presence of bisphenol A (BPA) in foodstuffs. EFSA J. 2015;13(1):3978.