Estradiol stimulation of Pulsatile gonadotropin-releasing hormone secretion in vitro: Correlation with perinatal exposure to sex steroids and induction of sexual precocity in vivo
[en] Our aim was to study the effect of estradiol (E2) on pulsatile GnRH secretion in vitro in relation to sex and development. When hypothalamic explants obtained from 5- and 15-d-old female rats were exposed to E2 (10(-7) m), a reduction of GnRH interpulse interval (IPI) occurred but not at 25 and 50 d of age. This effect was prevented by the estrogen receptor antagonist ICI 182.780 and the AMPA/kainate receptor antagonist DNQX but not by the AMPA and N-methyl-D-aspartate receptor antagonists SYM 2206 and MK-801. E2 did not affect GnRH IPI in hypothalamic explants obtained from male rats. Therefore, the possible relation between the female-specific effects of E2 in vitro and perinatal sexual differentiation was investigated. When using explants obtained from female rats masculinized through testosterone injection on postnatal d 1, E2 was no longer effective in vitro at 5 and 15 d. In addition, with explants obtained from male rats demasculinized through perinatal aromatase inhibitor treatment, E2 became capable of decreasing GnRH IPI in vitro at 15 d. To study the possible pathophysiological significance of early hypothalamic E2 effects, female rats received a single E2 injection on postnatal d 10. This resulted in reduced GnRH IPI in vitro on d 15 as well as advancement in age at vaginal opening and first estrus. In conclusion, E2 decreases the GnRH IPI in the immature female hypothalamus in vitro through a mechanism that depends on perinatal brain sexual differentiation and that could be involved in some forms of female precocious puberty.
Gerard, Arlette ; Centre Hospitalier Universitaire de Liège - CHU > Pédiatrie
Bourguignon, Jean-Pierre ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Language :
English
Title :
Estradiol stimulation of Pulsatile gonadotropin-releasing hormone secretion in vitro: Correlation with perinatal exposure to sex steroids and induction of sexual precocity in vivo
Publication date :
June 2004
Journal title :
Endocrinology
ISSN :
0013-7227
eISSN :
1945-7170
Publisher :
Endocrine Soc, Chevy Chase, United States - Maryland
Pescovitz OH, Comite F, Cassorla F, Dwyer AJ, Poth MA, Sperling MA, Hench K, McNemar A, Skerda M, Loriaux DL 1984 True precocious puberty complicating congenital adrenal hyperplasia: treatment with a luteinizing hormone-releasing hormone analog. J Clin Endocrinol Metab 58:857-861
Hochberg Z, Schechter J, Benderly A, Leiberman E, Rosler A 1985 Growth and pubertal development in patients with congenital adrenal hyperplasia due to 11-ι-hydroxylase deficiency. Am J Dis Child 139:771-776
Kukuvitis A, Matte C, Polychronakos C 1995 Central precocious puberty following feminizing right ovarian granulosa cell tumor. Horm Res 44:268-270
Pasquino AM, Tebaldi L, Cives C, Maciocci M, Boscherini B 1987 Precocious puberty in the McCune-Albright syndrome. Progression from gonadotrophin- independent to gonadotrophin-dependent puberty in a girl. Acta Paediatr Scand 76:841-843
Boepple PA, Frisch LS, Wierman ME, Hoffman WH, Crowley WFJ 1992 The natural history of autonomous gonadal function, adrenarche, and central puberty in gonadotropin-independent precocious puberty. J Clin Endocrinol Metab 75:1550-1555
Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP 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
Grumbach MM, Styne DM 2003 Puberty: ontogeny, neuroendocrinology, physiology, and disorders. In: Wilson JD, Foster DW, Kronenberg HM, Larsen PR, eds. Williams' textbook of endocrinology. Philadelphia WB Saunders; 1509-1625
Ramirez VD, Sawyer CH 1965 Advancement of puberty in the female rat by estrogen. Endocrinology 76:1158-1168
Bourguignon JP, Franchimont P 1984 Puberty-related increase in episodic LHRH release from rat hypothalamus in vitro. Endocrinology 114:1941-1943
Bourguignon JP, Gerard A, Purnelle G, Czajkowski V, Yamanaka C, Lemaitre M, Rigo JM, Moonen G, Franchimont P 1997 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 Neuroendocrinol 9:183-191
Bourguignon JP, Gerard A, Purnelle G, Czajkowski V, Yamanaka C, Lemaitre M, Rigo JM, Moonen G, Franchimont P 1997 Duality of glutamatergic and GABAergic control of pulsatile GnRH secretion by rat hypothalamic explants: II. Reduced NR2C- and GABAA-receptor-mediated inhibition at initiation of sexual maturation. J Neuroendocrinol 9:193-199
Yamanaka C, Lebrethon MC, Vandersmissen E, Gerard A, Purnelle G, Lemaitre M, Wilk S, Bourguignon JP 1999 Early prepubertal ontogeny of pulsatile gonadotropin-releasing hormone (GnRH) secretion: I. Inhibitory autofeedback control through prolyl endopeptidase degradation of GnRH. Endocrinology 140:4609-4615
Bourguignon JP, Gerard A, Alvarez GM, Purnelle G, Franchimont P 1995 Endogenous glutamate involvement in pulsatile secretion of gonadotropin- releasing hormone: evidence from effect of glutamine and developmental changes. Endocrinology 136:911-916
Bourguignon JP, Alvarez GM, Gerard A, Franchimont P1994 Gonadotropin releasing hormone inhibitory autofeedback by subproducts antagonist at N-methyl-D-aspartate receptors: a model of autocrine regulation of peptide secretion. Endocrinology 134:1589-1592
Urbanski HF, Ojeda SR 1987 Activation of luteinizing hormone-releasing hormone release advances the onset of female puberty. Neuroendocrinology 46:273-276
Plant TM, Gay VL, Marshall GR, Arslan M 1989 Puberty in monkeys is triggered by chemical stimulation of the hypothalamus. Proc Natl Acad Sci USA 86:2506-2510
Urbanski HF, Ojeda SR 1990 A role for N-methyl-D-aspartate (NMDA) receptors in the control of LH secretion and initiation of female puberty. Endocrinology 126:1774-1776
Brann DW, Zamorano PL, Ping L, Mahesh VB 1993 Role of excitatory amino acid neurotransmission during puberty in the female rat. Mol Cell Neurosci 4:107-112
Gorski RA 1968 Influence of age on the response to paranatal administration of a low dose of androgen. Endocrinology 82:1001-1004
Corbier P 1985 Sexual differentiation of positive feedback: effect of hour of castration at birth on estradiol-induced luteinizing hormone secretion in immature male rats. Endocrinology 116:142-147
Brand T, Kroonen J, Mos J, Slob AK 1991 Adult partner preference and sexual behavior of male rats affected by perinatal endocrine manipulations. Horm Behav 25:323-341
Gerardin DC, Pereira OC 2002 Reproductive changes in male rats treated perinatally with an aromatase inhibitor. Pharmacol Biochem Behav 71:301-305
Bourguignon JP, Gerard A, Alvarez-Gonzalez ML, Franchimont P 1992 Neuroendocrine mechanism of onset of puberty. Sequential reduction in activity of inhibitory and facilitatory N-methyl-D-aspartate receptors. J Clin Invest 90:1736-1744
Bourguignon JP, Gerard A, Mathieu J, Simons J, Franchimont P 1989 Pulsatile release of gonadotropin-releasing hormone from hypothalamic explants is restrained by blockade of N-methyl-D,L-aspartate receptors. Endocrinology 125:1090-1096
Bourguignon JP, Gerard A, Franchimont P 1989 Direct activation of gonadotropin-releasing hormone secretion through different receptors to neuroexcitatory amino acids. Neuroendocrinology 49:402-408
Dluzen DE, Ramirez VD 1981 Presence and localization of immunoreactive luteinizing hormone-releasing hormone (LHRH) within the olfactory bulbs of adult male and female rats. Peptides 2:493-496
Roselli CE, Klosterman SA 1998 Sexual differenciation of aromatase activity in the rat brain: effects of perinatal steroid exposure. Endocrinology 139:3193-3201
Swaab DF, Slob AK, Houtsmuller EJ, Brand T, Zhou JN 1995 Increased number of vasopressin neurons in the suprachiasmatic nucleus (SCN) of 'bisexual' adult male rats following perinatal treatment with the aromatase blocker ATD. Brain Res Dev Brain Res 85:273-279
Bakker J, Baum MJ, Slob AK 1996 Neonatal inhibition of brain estrogen synthesis alters adult neural Fos responses to mating and pheromonal stimulation in the male rat. Neuroscience 74:251-260
Gogan F, Beattie IA, Hery M, Laplante E, Kordon D 1980 Effect of neonatal administration of steroids or gonadectomy upon oestradiol-induced luteinizing hormone release in rats of both sexes. J Endocrinol 85:69-74
Diaz DR, Fleming DE, Rhees RW 1995 The hormone-sensitive early postnatal periods for sexual differentiation of feminine behavior and luteinizing hormone secretion in male and female rats. Brain Res Dev Brain Res 86:227-232
Silva A, Guimaraes MA, Padmanabhan V, Lara HE 2003 Prepubertal administration of estradiol valerate disrupts cyclicity and leads to cystic ovarian morphology during adult life in the rat: role of sympathetic innervation. Endocrinology 144:4289-4297
Ojeda SR, Urbanski HF 1994 Puberty in the rat. In: Knobil E, Neill JD, eds. The physiology of reproduction. Vol 2. New York: Raven Press Ltd; 363-409
Merriam GR, Wachter KW 1982 Algorithms for the study of episodic hormone secretion. Am J Physiol 243:E310-E318
Bourguignon JP, Gerard A, Mathieu J, Mathieu A, Franchimont P 1990 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 127:873-881
Prevot V, Croix D, Rialas CM, Poulain P, Fricchione GL, Stefano GB, Beauvillain JC 1999 Estradiol coupling to endothelial nitric oxide stimulates gonadotropin-releasing hormone release from rat median eminence via a membrane receptor. Endocrinology 140:652-659
Israel JM, Poulain DA 2000 17-Oestradiol modulates in vitro electrical properties and responses to kainate of oxytocin neurones in lactating rats. J Physiol (Lond) 524:457-470
Sisk CL, Richardson HN, Chappell PE, Levine JE 2001 In vivo gonadotropin-releasing hormone secretion in female rats during peripubertal development and on proestrus. Endocrinology 142:2929-2936
Harris GC, Levine JE 2003 Pubertal acceleration of pulsatile gonadotropin-releasing hormone release in male rats as revealed by microdialysis. Endocrinology 144:163-171
Keen KL, Burich AJ, Mitsushima D, Kasuya E, Terasawa E 1999 Effects of pulsatile infusion of the GABA(A) receptor blocker bicuculline on the onset of puberty in female rhesus monkeys. Endocrinology 140:5257-5266
Klein KO, Baron J, Colli MJ, McDonnell DP, Cutler GBJ 1994 Estrogen levels in childhood determined by an ultrasensitive recombinant cell bioassay. J Clin Invest 94:2475-2480
Sokka TA, Huhtaniemi IT 1995 Functional maturation of the pituitary-gonadal axis in the neonatal female rat. Biol Reprod 52:1404-1409
Andrews WW, Mizejewski GJ, Ojeda SR 1981 Development of estradiol-positive feedback on luteinizing hormone release in the female rat: a quantitative study. Endocrinology 109:1404-1413
Levine JE, Bethea CL, Spies HG 1985 In vitro gonadotropin-releasing hormone release from hypothalamic tissues of ovariectomized estrogen-treated cynomolgus macaques. Endocrinology 116:431-438
Andrews WW, Ojeda SR 1977 On the feedback actions of estrogen on gonadotropin and prolacrin release in infantile female rats. Endocrinology 101:1517-1523
Caligaris L, Astrada JJ, Taleisnik S 1972 Influence of age on the release of luteinizing hormone induced by oestrogen and progesterone in immature rats. J Endocrinol 55:97-103
McGarvey C, Cates PA, Brooks A, Swanson IA, Milligan SR, Coen CW, O'Byrne KT 2001 Phytoestrogens and gonadotropin-releasing hormone pulse generator activity and pituitary luteinizing hormone release in the rat. Endocrinology 142:1202-1208
Dluzen DE, Ramirez VD 1986 In vivo LH-RH output of ovariectomized rats following estrogen treatment. Neuroendocrinology 43:459-465
Evans NP, Dahl GE, Mauger D, Karsch FJ 1995 Estradiol induces both qualitative and quantitative changes in the pattern of gonadotropin-releasing hormone secretion during the presurge period in the ewe. Endocrinology 136:1603-1609
Parent AS, Lebrethon MC, Gerard A, Vandersmissen E, Bourguignon JP 2000 Leptin effects on pulsatile gonadotropin-releasing hormone secretion from the adult rat hypothalamus and interaction with cocaine and amphetamine regulated transcript peptide and neuropeptide Y. Regul Pept 92:17-24
Condon TP, Dykshoorn-Bosch MA, Kelly MJ 1988 Episodic luteinizing-hormone release in the ovariectomized female guinea pig: rapid inhibition by estrogen. Biol Reprod 38:121-126
Butler JA, Sjoberg M, Coen CW 1999 Evidence for oestrogen receptor α-immunoreactivity in gonadotrophin-releasing hormone-expressing neurones. J Neuroendocrinol 11:331-335
Herbison AE, Pape JR 2001 New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front Neuroendocrinol 22:292-308
Nunemaker CS, Straume M, DeFazio RA, Moenter SM 2003 Gonadotropin- releasing hormone neurons generate interacting rhythms in multiple time domains. Endocrinology 144:823-831
Nunemaker CS, DeFazio RA, Moenter SM 2002 Estradiol-sensitive afferents modulate long-term episodic firing patterns of GnRH neurons. Endocrinology 143:2284-2292
DeFazio RA, Moenter SM 2002 Estradiol feedback alters potassium currents and firing properties of gonadotropin-releasing hormone neurons. Mol Endocrinol 16:2255-2265
Purnelle G, Gerard A, Czajkowski V, Bourguignon JP1997 Pulsatile secretion of gonadotropin-releasing hormone by rat hypothalamlc explants without cell bodies of GnRH neurons. Neuroendocrinology 66:305-312
Ojeda SR, Ma YJ, Lee BJ, Prevot V 2000 Glia-to-neuron signaling and the neuroendocrine control of female puberty. Recent Prog Horm Res 55:197-223
Moguilevsky JA, Wuttke W 2001 Changes in the control of gonadotrophin secretion by neurotransmitters during sexual development in rats. Exp Clin Endocrinol Diabetes 109:188-195
Eyigor O, Jennes L 2000 Kainate receptor subunit-positive gonadotropin-releasing hormone neurons express c-Fos during the steroid-induced luteinizing hormone surge in the female rat. Endocrinology 141:779-786
Lopez FJ, Donoso AO, Negro-Vilar A 1990 Endogenous excitatory amino acid neurotransmission regulates the estradiol-induced LH surge in ovariectomized rats. Endocrinology 126:1771-1773
Diano S, Naftolin F, Horvath TL 1998 Kainate glutamate receptors (GluR5-7) in the rat arcuate nucleus: relationship to tanycytes, astrocytes, neurons and gonadal steroid receptors. J Neuroendocrinol 10:239-247
Gu Q, Korach KS, Moss RL 1999 Rapid action of 17β-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors. Endocrinology 140:660-666
Mitsushima D, Hei DL, Terasawa E 1994 γ-Aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty. Proc Natl Acad Sci USA 91:395-399
Moguilevsky JA, Carbone S, Szwarcfarb B, Rondina D 1991 Sexual maturation modifies the GABAergic control of gonadotrophin secretion in female rats. Brain Res 563:12-16
Mansky T, Mestres-Ventura P, Wuttke W 1982 Involvement of GABA in the feedback action of estradiol on gonadotropin and prolactin release: hypothalamic GABA and catecholamine turnover rates. Brain Res 231:353-364
Jarry H, Hirsch B, Leonhardt S, Wuttke W 1992 Amino acid neurotransmitter release in the preoptic area of rats during the positive feedback actions of estradiol on LH release. Neuroendocrinology 56:133-140
Lasaga M, De Laurentiis A, Pampillo M, Pisera D, del Carmen DM, Theas S, Duvilanski B, Seilicovich A 1998 The effect of excitatory amino acids on GABA release from mediobasal hypothalamus of female rats. Neurosci Lett 247:119-122
Pinilla L, Tena-Sempere M, Aguilar E 1998 Sexual differences in the role of kainate receptors in controlling gonadotrophin secretion in prepubertal rats. J Reprod Fertil 113:269-273
Ikeda Y, Nagai A, Ikeda MA, Hayashi S 2003 Sexually dimorphic and estrogen-dependent expression of estrogen receptor β in the ventromedial hypothalamus during rat postnatal development. Endocrinology 144:5098-5104
Kosut SS, Wood RI, Herbosa-Encarnacion C, Foster DL 1997 Prenatal androgens time neuroendocrine puberty in the sheep: effect of T dose. Endocrinology 138:1072-1077