Early neuroendocrine disruption in hypothalamus and hippocampus: developmental effects including female sexual maturation and implications for endocrine disrupting chemicals screening
Bourguignon, Jean-Pierre ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Franssen, Delphine ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
GERARD, Arlette ; Centre Hospitalier Universitaire de Liège - CHU > Pédiatrie
Pinson, Anneline ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Naveau, Elise ; Université de Liège - ULiège > GIGA - Membres
Parent, Anne-Simone ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Language :
English
Title :
Early neuroendocrine disruption in hypothalamus and hippocampus: developmental effects including female sexual maturation and implications for endocrine disrupting chemicals screening
Herbst AL, Ulfelder H, Poskanzer DC. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 1971; 284: 878-881.
Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986; 1: 1077-1081.
Barker DJ, Osmond C, Forsen TJ, Kajantie E, Eriksson JG. Trajectories of growth among children who have coronary events as adults. N Engl J Med 2005; 353: 1802-1809.
Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 2009; 30: 293-342.
Skakkebaek NE, Rajpert-De Meyts E, Main KM. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 2001; 16: 972-978.
Newbold RR, Padilla-Banks E, Snyder RJ, Phillips TM, Jefferson WN. Developmental exposure to endocrine disruptors and the obesity epidemic. Reprod Toxicol 2007; 23: 290-296.
Wei J, Lin Y, Li Y, Ying C, Chen J, Song L, Zhou Z, Lv Z, Xia W, Chen X, Xu S. Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology 2011; 152: 3049-3061.
Rudel RA, Gray JM, Engel CL, Rawsthorne TW, Dodson RE, Ackerman JM, Rizzo J, Nudelman JL, Brody JG. Food packaging and bisphenol A and bis(2-ethyhexyl) phthalate exposure: findings from a dietary intervention. Environ Health Perspect 2011; 119: 914-920.
Yang X, Doerge DR, Fisher JW. Prediction and evaluation of route dependent dosimetry of BPA in rats at different life stages using a physiologically based pharmacokinetic model. Toxicol Appl Pharmacol 2013; 70: 45-59.
Harley KG, Schall RA, Chevrier J, Tyler K, Aguirre H, Bradman A, Holland NT, Lustig RH, Calafat AM, Eskenazi B. Prenatal and postnatal bisphenol A exposure and body mass index in childhood in the CHAMACOS cohort. Environ Health Perspect 2013; 121: 514-520.
Bromer JG, Wu J, Zhou Y, Taylor HS. Hypermethylation of homeobox A10 by in utero diethylstilbestrol exposure: an epigenetic mechanism for altered developmental programming. Endocrinology 2009; 150: 3376-3382.
Sharpe RM, Fisher JS, Millar MM, Jobling S, Sumpter JP. Gestational and lactational exposure of rats to xenoestrogens results in reduced testicular size and sperm production. Environ Health Perspect 1995; 103: 1136-1143.
Ben-Jonathan N, Hugo ER, Brandebourg TD. Effects of bisphenol A on adipokine release from human adipose tissue: implications for the metabolic syndrome. Mol Cell Endocrinol 2009; 304: 49-54.
Gore AC. Environmental toxicant effects on neuroendocrine function. Endocrine 2001; 14: 235-246.
Bourguignon JP, Rasier G, Lebrethon MC, Gerard A, Naveau E, Parent AS. Neuroendocrine disruption of pubertal timing and interactions between homeostasis of reproduction and energy balance. Mol Cell Endocrinol 2010; 324: 110-120.
Frye CA, Bo E, Calamandrei G, Calza L, Dessi-Fulgheri F, Fernandez M, Fusani L, Kah O, Kajta M, Le Page Y, Patisaul HB, Venerosi A, Wojtowicz AK, Panzica GC. Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J Neuroendocrinol 2012; 24: 144-159.
Bourguignon JP, Parent AS. The Impact of Endocrine Disruptors on Female Pubertal Timing. In: Diamanti-Kandarakis E, Gore AC, eds. Endocrine Disruptors and Puberty. New York, NY: Springer Science + Business Media, 2012: 325-337 chapter 13.
Leijs MM, Koppe JG, Olie K, van Aalderen WM, Voogt P, Vulsma T, Westra M, ten Tusscher GW. Delayed initiation of breast development in girls with higher prenatal dioxin exposure; a longitudinal cohort study. Chemosphere 2008; 73: 999-1004.
Den Hond E, Roels HA, Hoppenbrouwers K, Nawrot T, Thijs L, Vandermeulen C, Winneke G, Vanderschueren D, Staessen JA. Sexual maturation in relation to polychlorinated aromatic hydrocarbons: Sharpe and Skakkebaek's hypothesis revisited. Environ Health Perspect 2002; 110: 771-776.
Wolff MS, Britton JA, Boguski L, Hochman S, Maloney N, Serra N, Liu Z, Berkowitz G, Larson S, Forman J. Environmental exposures and puberty in inner-city girls. Environ Res 2008; 107: 393-400.
Denham M, Schell LM, Deane G, Gallo MV, Ravenscroft J, DeCaprio AP. Relationship of lead, mercury, mirex, dichlorodiphenyldichloroethylene, hexachlorobenzene, and polychlorinated biphenyls to timing of menarche among Akwesasne Mohawk girls. Pediatrics 2005; 115: e127-e134.
Vasiliu O, Muttineni J, Karmaus W. In utero exposure to organochlorines and age at menarche. Hum Reprod 2004; 19: 1506-1512.
Yang CY, Yu ML, Guo HR, Lai TJ, Hsu CC, Lambert G, Guo YL. The endocrine and reproductive function of the female Yucheng adolescents prenatally exposed to PCBs/PCDFs. Chemosphere 2005; 61: 355-360.
Warner M, Samuels S, Mocarelli P, Gerthoux PM, Needham L, Patterson DG Jr, Eskenazi B. Serum dioxin concentrations and age at menarche. Environ Health Perspect 2004; 112: 1289-1292.
Krstevska-Konstantinova M, Charlier C, Craen M, Du Caju M, Heinrichs C, de Beaufort C, Plomteux G, Bourguignon JP. Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides. Hum Reprod 2001; 16: 1020-1026.
Ouyang F, Perry MJ, Venners SA, Chen C, Wang B, Yang F, Fang Z, Zang T, Wang L, Xu X, Wang X. Serum DDT, age at menarche, and abnormal menstrual cycle length. Occup Environ Med 2005; 62: 878-884.
Wohlfahrt-Veje C, Andersen HR, Schmidt IM, Aksglaede L, Sorensen K, Juul A, Jensen TK, Grandjean P, Skakkebaek NE, Main KM. Early breast development in girls after prenatal exposure to non-persistent pesticides. Int J Androl 2012; 35: 273-282.
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: 668-693.
Bourguignon JP, Gerard A, Alvarez Gonzalez ML, Fawe L, Franchimont P. Effects of changes in nutritional conditions on timing of puberty: clinical evidence from adopted children and experimental studies in the male rat. Horm Res 1992; 38(Suppl. 1): 97-105.
Domine F, Parent AS, Rasier G, Lebrethon MC, Bourguignon JP. Assessment and mechanism of variations in pubertal timing in internationally adopted children: a developmental hypothesis. Eur J Endocrinol 2006; 155: S17-S25.
Rasier G, Parent AS, Gerard 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: 734-742.
Rasier G, Parent AS, Gerard A, Denooz R, Lebrethon MC, Charlier C, Bourguignon JP. Mechanisms of interaction of endocrine-disrupting chemicals with glutamate-evoked secretion of gonadotropin-releasing hormone. Toxicol Sci 2008; 102: 33-41.
Matagne V, Lebrethon MC, Gerard A, Bourguignon JP. Kainate/estrogen receptor involvement in rapid estradiol effects in vitro and intracellular signaling pathways. Endocrinology 2005; 146: 2313-2323.
Ohtake F, Takeyama K, Matsumoto T, Kitagawa H, Yamamoto Y, Nohara K, Tohyama C, Krust A, Mimura J, Chambon P, Yanagisawa J, Fujii-Kuriyama Y, Kato S. Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 2003; 423: 545-550.
Franssen D, Ioannou Y, Alvarez-Real A, Gerard A, Mueller J, Heger S, Bourguignon JP, Parent AS. Pubertal timing after neonatal diethylstilbestrol exposure in female rats: neuroendocrine versus peripheral effects and additive role of prenatal food restriction. Reprod Toxicol 2013.
Howdeshell KL, Hotchkiss AK, Thayer KA, Vandenbergh JG, vom Saal FS. Exposure to bisphenol A advances puberty. Nature 1999; 401: 763-764.
Honma S, Suzuki A, Buchanan DL, 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.
Ryan BC, Hotchkiss AK, Crofton KM, Gray LE Jr. In utero and lactational exposure to bisphenol A, in contrast to ethinyl estradiol, does not alter sexually dimorphic behavior, puberty, fertility, and anatomy of female LE rats. Toxicol Sci 2010; 114: 133-148.
Kwon S, Stedman DB, Elswick BA, Cattley RC, 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.
Rubin BS, Murray MK, Damassa DA, King JC, Soto AM. 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.
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: 690-699.
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.
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: 75-81.
Taylor JA, Welshons WV, vom Saal FS. No effect of route of exposure (oral; subcutaneous injection) on plasma bisphenol A throughout 24 h after administration in neonatal female mice. Reprod Toxicol 2008; 25: 169-176.
Gayrard V, Lacroix MZ, Collet SH, Viguié C, Bousquet-Melou A, Toutain PL, Picard-Hagen N. High Bioavailability of Bisphenol A from Sublingual Exposure. Environ Health Perspect 2013; 121: 951-956.
Biro FM, Greenspan LC, Galvez MP. Puberty in girls of the 21st century. J Pediatr Adolesc Gynecol 2012; 25: 289-294.
Ghamari-Langroudi M, Vella KR, Srisai D, Sugrue ML, Hollenberg AN, Cone RD. Regulation of thyrotropin-releasing hormone-expressing neurons in paraventricular nucleus of the hypothalamus by signals of adiposity. Mol Endocrinol 2010; 24: 2366-2381.
Zoeller RT, Brown TR, Doan LL, Gore AC, Skakkebaek NE, Soto AM, Woodruff TJ, vom Saal FS. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology 2012; 153: 4097-4110.
Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Myers JP, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT. Regulatory decisions on endocrine disrupting chemicals should be based on the principles of endocrinology. Reprod Toxicol 2013; 38: C1-C15.
OCSPP harmonized test guidelines. Series 890 - Endocrine disruptor screening program test guidelines. http://www.epa.gov/ocspp/pubs/frs/publications/Test_Guidelines/series890.htm.
Chemical safety and biosafety. Testing of chemicals. http://www.oecd.org/env/ehs/testing/section4healtheffects.htm.
Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, Myers JP. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 2012; 33: 378-455.
Franssen D, Ioannou Y, Alvarez-Real A, Gerard A, Parent AS, Bourguignon JP. Opposing Dose Related Effects of Neonatal DES and BPA Exposure on the Timing of Female Sexual Maturation Through Neuroendocrine Disruption. Paris: PNRPE, 2012.
Rivas A, Fisher JS, McKinnell C, Atanassova N, Sharpe RM. Induction of reproductive tract developmental abnormalities in the male rat by lowering androgen production or action in combination with a low dose of diethylstilbestrol: evidence for importance of the androgen-estrogen balance. Endocrinology 2002; 143: 4797-4808.
McCarthy MM. The two faces of estradiol: effects on the developing brain. Neuroscientist 2009; 2009: 599-610.
Gilbert ME. Impact of low-level thyroid hormone disruption induced by propylthiouracil on brain development and function. Toxicol Sci 2011; 124: 432-445.
Myant NB. Passage of thyroxine and tri-iodol-thyronine from mother to foetus in pregnant women. Clin Sci 1958; 17: 75-7957.
Vulsma T, Gons MH, de Vijlder JJ. Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to a total organification defect or thyroid agenesis. N Engl J Med 1989; 321: 13-16.
Kester MH, Martinez de Mena R, Obregon MJ, Marinkovic D, Howatson A, Visser TJ, Hume R, Morreale de Escobar G. Iodothyronine levels in the human developing brain: major regulatory roles of iodothyronine deiodinases in different areas. J Clin Endocrinol Metab 2004; 89: 3117-3128.
Ahmed OM, El-Gareib AW, El-Bakry AM, Abd El-Tawab SM, Ahmed RG. Thyroid hormones states and brain development interactions. Int J Dev Neurosci 2008; 26: 147-209.
Gilbert ME, Sui L. Dose-dependent reductions in spatial learning and synaptic function in the dentate gyrus of adult rats following developmental thyroid hormone insufficiency. Brain Res 2006; 1069: 10-22.
Zhang L, Blomgren K, Kuhn HG, Cooper-Kuhn CM. Effects of postnatal thyroid hormone deficiency on neurogenesis in the juvenile and adult rat. Neurobiol Dis 2009; 34: 366-374.
Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996; 16: 2027-2033.
Aimone JB, Deng W, Gage FH. Resolving new memories: a critical look at thedentate gyrus, adult neurogenesis, and pattern separation. Neuron 2011; 70: 589-596.
Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 2010; 11: 339-350.
Inokuchi K. Adult neurogenesis and modulation of neural circuit function. Curr Opin Neurobiol 2011; 21: 360-364.
Bansal R, Zoeller RT. Polychlorinated biphenyls (Aroclor 1254) do not uniformly produce agonist actions on thyroid hormone responses in the developing rat brain. Endocrinology 2008; 149: 4001-4008.
Saegusa Y, Fujimoto H, Woo GH, Ohishi T, Wang L, Mitsumori K, Nishikawa A, Shibutani M. Transient aberration of neuronal development in the hippocampal dentate gyrus after developmental exposure to brominated flame retardants in rats. Arch Toxicol 2012; 86: 1431-1442.
Parent AS, Naveau E, Gerard A, Bourguignon JP, Westbrook GL. Early developmental actions of endocrine disruptors on the hypothalamus, hippocampus, and cerebral cortex. J Toxicol Environ Health B Crit Rev 2011; 14: 328-345.
Schantz SL, Widholm JJ, Rice DC. Effects of PCB exposure on neuropsychological function in children. Environ Health Perspect 2003; 111: 357-576.
Eskenazi B, Chevrier J, Rauch SA, Kogut K, Harley KG, Johnson C, Trujillo C, Sjodin A, Bradman A. In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environ Health Perspect 2013; 121: 257-262.
Leranth C, Hajszan T, Szigeti-Buck K, Bober J, MacLusky NJ. Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc Natl Acad Sci USA 2008; 105: 14187-14191.
Xu XH, Zhang J, Wang YM, Ye YP, Luo QQ. Perinatal exposure to bisphenol-A impairs learning-memory by concomitant down-regulation of N-methyl-D-aspartate receptors of hippocampus in male offspring mice. Horm Behav 2010; 58: 326-333.
Cohen RA. Obesity-associated cognitive decline: excess weight affects more than the waistline. Neuroepidemiology 2010; 34: 230-231.
Stranahan AM, Cutler RG, Button C, Telljohann R, Mattson MP. Diet-induced elevations in serum cholesterol are associated with alterations in hippocampal lipid metabolism and increased oxidative stress. J Neurochem 2011; 118: 611-615.
Heyward FD, Walton RG, Carle MS, Coleman MA, Garvey WT, Sweatt JD. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem 2012; 98: 25-32.
Park HR, Park M, Choi J, Park KY, Chung HY, Lee J. A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci Lett 2010; 482: 235-239.