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Semin Reprod Med 2012; 30(01): 23-31
DOI: 10.1055/s-0031-1299594
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Estrogen Receptor-β in the Gonadotropin-Releasing Hormone Neuron

Andrew Wolfe
1   Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland
,
Sheng Wu
1   Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland
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Publikationsdatum:
23. Januar 2012 (online)

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Abstract

Estrogen regulation of gonadotropin-releasing hormone (GnRH) neuronal activity plays a crucial role in homeostatic regulation of the hypothalamic-pituitary-gonadal axis. Estrogen also coordinates a complex series of physiological changes culminating with a surge of gonadotropin secretion that triggers ovulation of a developed follicle from the ovary. The coordinated functions of estrogen ensure that the female will elaborate appropriate reproductive behaviors ultimately designed to deliver sperm to the oocyte and to provide a receptive uterine environment for the fertilized embryo. Although the effects of estrogen on GnRH neuronal function have long been proposed to be indirect due to the presumed lack of estrogen receptors in GnRH neurons, the identification of alternative estrogen signaling pathways, including estrogen receptor (ER)β and membrane ERs such as GPR30, has put the focus back on estrogen’s effect at the level of the GnRH neuron itself. One candidate to mediate the effects of estrogen is the β isoform of the estrogen receptor. We review the evidence for a role for ERβ-mediated regulation of GnRH neuronal function.

Keywords

GnRH - estrogen receptor-β - HPG axis
 

  • References

  • 1 Duffy KR, Pardridge WM. Blood-brain barrier transcytosis of insulin in developing rabbits. Brain Res 1987; 420 (1) 32-38
    CrossrefPubMedGoogle Scholar
  • 2 Karsch FJ, Cummins JT, Thomas GB, Clarke IJ. Steroid feedback inhibition of pulsatile secretion of gonadotropin-releasing hormone in the ewe. Biol Reprod 1987; 36 (5) 1207-1218
    CrossrefPubMedGoogle Scholar
  • 3 Plant TM, Dubey AK. Evidence from the rhesus monkey (Macaca mulatta) for the view that negative feedback control of luteinizing hormone secretion by the testis is mediated by a deceleration of hypothalamic gonadotropin-releasing hormone pulse frequency. Endocrinology 1984; 115 (6) 2145-2153
    CrossrefPubMedGoogle Scholar
  • 4 Mayer C, Acosta-Martinez M, Dubois SL , et al. Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc Natl Acad Sci U S A 2010; 107 (52) 22693-22698
    CrossrefPubMedGoogle Scholar
  • 5 Sisk CL, Richardson HN, Chappell PE, Levine JE. In vivo gonadotropin-releasing hormone secretion in female rats during peripubertal development and on proestrus. Endocrinology 2001; 142 (7) 2929-2936
    CrossrefPubMedGoogle Scholar
  • 6 Clarke IJ. Variable patterns of gonadotropin-releasing hormone secretion during the estrogen-induced luteinizing hormone surge in ovariectomized ewes. Endocrinology 1993; 133 (4) 1624-1632
    CrossrefPubMedGoogle Scholar
  • 7 Moenter SM, Brand RC, Karsch FJ. Dynamics of gonadotropin-releasing hormone (GnRH) secretion during the GnRH surge: insights into the mechanism of GnRH surge induction. Endocrinology 1992; 130 (5) 2978-2984
    CrossrefPubMedGoogle Scholar
  • 8 Xia L, Van Vugt D, Alston EJ, Luckhaus J, Ferin M. A surge of gonadotropin-releasing hormone accompanies the estradiol-induced gonadotropin surge in the rhesus monkey. Endocrinology 1992; 131 (6) 2812-2820
    CrossrefPubMedGoogle Scholar
  • 9 Turzillo AM, DiGregorio GB, Nett TM. Messenger ribonucleic acid for gonadotropin-releasing hormone receptor and numbers of gonadotropin-releasing hormone receptors in ovariectomized ewes after hypothalamic-pituitary disconnection and treatment with estradiol. J Anim Sci 1995; 73 (6) 1784-1788
    PubMedGoogle Scholar
  • 10 Savoy-Moore RT, Schwartz NB, Duncan JA, Marshall JC. Pituitary gonadotropin-releasing hormone receptors during the rat estrous cycle. Science 1980; 209 (4459) 942-944
    CrossrefPubMedGoogle Scholar
  • 11 Kauffman AS, Gottsch ML, Roa J , et al. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 2007; 148 (4) 1774-1783
    CrossrefPubMedGoogle Scholar
  • 12 Smith JT, Clifton DK, Steiner RA. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 2006; 131 (4) 623-630
    CrossrefPubMedGoogle Scholar
  • 13 Dungan HM, Gottsch ML, Zeng H , et al. The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropin-releasing hormone/luteinizing hormone. J Neurosci 2007; 27 (44) 12088-12095
    CrossrefPubMedGoogle Scholar
  • 14 Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005; 146 (9) 3686-3692
    CrossrefPubMedGoogle Scholar
  • 15 Wintermantel TM, Campbell RE, Porteous R , et al. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 2006; 52 (2) 271-280
    CrossrefPubMedGoogle Scholar
  • 16 Plant TM, Ramaswamy S. Kisspeptin and the regulation of the hypothalamic-pituitary-gonadal axis in the rhesus monkey (Macaca mulatta). Peptides 2009; 30 (1) 67-75
    CrossrefPubMedGoogle Scholar
  • 17 Rometo AM, Krajewski SJ, Voytko ML, Rance NE. Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys. J Clin Endocrinol Metab 2007; 92 (7) 2744-2750
    CrossrefPubMedGoogle Scholar
  • 18 Smith JT, Shahab M, Pereira A, Pau KY, Clarke IJ. Hypothalamic expression of KISS1 and gonadotropin inhibitory hormone genes during the menstrual cycle of a non-human primate. Biol Reprod 2010; 83 (4) 568-577
    CrossrefPubMedGoogle Scholar
  • 19 Caraty A, Franceschini I, Hoffman GE. Kisspeptin and the preovulatory gonadotrophin-releasing hormone/luteinising hormone surge in the ewe: basic aspects and potential applications in the control of ovulation. J Neuroendocrinol 2010; 22 (7) 710-715
    PubMedGoogle Scholar
  • 20 Castellano JM, Bentsen AH, Mikkelsen JD, Tena-Sempere M. Kisspeptins: bridging energy homeostasis and reproduction. Brain Res 2010; 1364: 129-138
    CrossrefPubMedGoogle Scholar
  • 21 Castellano JM, Bentsen AH, Romero M , et al. Acute inflammation reduces kisspeptin immunoreactivity at the arcuate nucleus and decreases responsiveness to kisspeptin independently of its anorectic effects. Am J Physiol Endocrinol Metab 2010; 299 (1) E54-E61
    CrossrefPubMedGoogle Scholar
  • 22 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
    CrossrefPubMedGoogle Scholar
  • 23 Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 2005; 102 (6) 2129-2134
    CrossrefPubMedGoogle Scholar
  • 24 Mayer C, Boehm U. Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nat Neurosci 2011; 14 (6) 704-710
    CrossrefPubMedGoogle Scholar
  • 25 Chan YM, Broder-Fingert S, Wong KM, Seminara SB. Kisspeptin/Gpr54-independent gonadotrophin-releasing hormone activity in Kiss1 and Gpr54 mutant mice. J Neuroendocrinol 2009; 21 (12) 1015-1023
    CrossrefPubMedGoogle Scholar
  • 26 Clarkson J, d’Anglemont de Tassigny X, Moreno AS, Colledge WH, Herbison AE. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 2008; 28 (35) 8691-8697
    CrossrefPubMedGoogle Scholar
  • 27 Mangelsdorf DJ, Thummel C, Beato M , et al. The nuclear receptor superfamily: the second decade. Cell 1995; 83 (6) 835-839
    CrossrefPubMedGoogle Scholar
  • 28 Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A 1996; 93 (12) 5925-5930
    CrossrefPubMedGoogle Scholar
  • 29 Mosselman S, Polman J, Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett 1996; 392 (1) 49-53
    CrossrefPubMedGoogle Scholar
  • 30 Kelley ST, Thackray VG. Phylogenetic analyses reveal ancient duplication of estrogen receptor isoforms. J Mol Evol 1999; 49 (5) 609-614
    CrossrefPubMedGoogle Scholar
  • 31 Zhao C, Dahlman-Wright K, Gustafsson JA. Estrogen signaling via estrogen receptor beta. J Biol Chem 2010; 285 (51) 39575-39579
    CrossrefPubMedGoogle Scholar
  • 32 Chung WC, Pak TR, Suzuki S, Pouliot WA, Andersen ME, Handa RJ. Detection and localization of an estrogen receptor beta splice variant protein (ERbeta2) in the adult female rat forebrain and midbrain regions. J Comp Neurol 2007; 505 (3) 249-267
    CrossrefPubMedGoogle Scholar
  • 33 Palmieri C, Saji S, Sakaguchi H , et al. The expression of oestrogen receptor (ER)-beta and its variants, but not ERalpha, in adult human mammary fibroblasts. J Mol Endocrinol 2004; 33 (1) 35-50
    CrossrefPubMedGoogle Scholar
  • 34 Kuiper GG, Shughrue PJ, Merchenthaler I, Gustafsson JA. The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol 1998; 19 (4) 253-286
    CrossrefPubMedGoogle Scholar
  • 35 Katzenellenbogen BS, Bhardwaj B, Fang H , et al. Hormone binding and transcription activation by estrogen receptors: analyses using mammalian and yeast systems. J Steroid Biochem Mol Biol 1993; 47 (1-6) 39-48
    CrossrefPubMedGoogle Scholar
  • 36 Powell E, Wang Y, Shapiro DJ, Xu W. Differential requirements of Hsp90 and DNA for the formation of estrogen receptor homodimers and heterodimers. J Biol Chem 2010; 285 (21) 16125-16134
    CrossrefPubMedGoogle Scholar
  • 37 Pace P, Taylor J, Suntharalingam S, Coombes RC, Ali S. Human estrogen receptor beta binds DNA in a manner similar to and dimerizes with estrogen receptor alpha. J Biol Chem 1997; 272 (41) 25832-25838
    CrossrefPubMedGoogle Scholar
  • 38 Stauffer SR, Coletta CJ, Tedesco R , et al. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 2000; 43 (26) 4934-4947
    CrossrefPubMedGoogle Scholar
  • 39 Meyers MJ, Sun J, Carlson KE, Marriner GA, Katzenellenbogen BS, Katzenellenbogen JA. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 2001; 44 (24) 4230-4251
    CrossrefPubMedGoogle Scholar
  • 40 Arreguin-Arevalo JA, Davis TL, Nett TM. Differential modulation of gonadotropin secretion by selective estrogen receptor 1 and estrogen receptor 2 agonists in ovariectomized ewes. Biol Reprod 2007; 77 (2) 320-328
    CrossrefPubMedGoogle Scholar
  • 41 Sánchez-Criado JE, Martín De Las Mulas J, Bellido C, Tena-Sempere M, Aguilar R, Blanco A. Biological role of pituitary estrogen receptors ERalpha and ERbeta on progesterone receptor expression and action and on gonadotropin and prolactin secretion in the rat. Neuroendocrinology 2004; 79 (5) 247-258
    CrossrefPubMedGoogle Scholar
  • 42 Sánchez-Criado JE, de Las Mulas JM, Bellido C , et al. Gonadotropin-secreting cells in ovariectomized rats treated with different oestrogen receptor ligands: a modulatory role for ERbeta in the gonadotrope?. J Endocrinol 2006; 188 (2) 167-177
    CrossrefPubMedGoogle Scholar
  • 43 Heldring N, Pike A, Andersson S , et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 2007; 87 (3) 905-931
    CrossrefPubMedGoogle Scholar
  • 44 Saville B, Wormke M, Wang F , et al. Ligand-, cell-, and estrogen receptor subtype (alpha/beta)-dependent activation at GC-rich (Sp1) promoter elements. J Biol Chem 2000; 275 (8) 5379-5387
    CrossrefPubMedGoogle Scholar
  • 45 Paech K, Webb P, Kuiper GG , et al. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science 1997; 277 (5331) 1508-1510
    CrossrefPubMedGoogle Scholar
  • 46 Navarro CE, Abdul Saeed S, Murdock C , et al. Regulation of cyclic adenosine 3′,5′-monophosphate signaling and pulsatile neurosecretion by Gi-coupled plasma membrane estrogen receptors in immortalized gonadotropin-releasing hormone neurons. Mol Endocrinol 2003; 17 (9) 1792-1804
    CrossrefPubMedGoogle Scholar
  • 47 Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA, Hathaway HJ. Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu Rev Physiol 2008; 70: 165-190
    CrossrefPubMedGoogle Scholar
  • 48 Noel SD, Keen KL, Baumann DI, Filardo EJ, Terasawa E. Involvement of G protein-coupled receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons. Mol Endocrinol 2009; 23 (3) 349-359
    CrossrefPubMedGoogle Scholar
  • 49 Sun J, Chu Z, Moenter SM. Diurnal in vivo and rapid in vitro effects of estradiol on voltage-gated calcium channels in gonadotropin-releasing hormone neurons. J Neurosci 2010; 30 (11) 3912-3923
    CrossrefPubMedGoogle Scholar
  • 50 Scully KM, Gleiberman AS, Lindzey J, Lubahn DB, Korach KS, Rosenfeld MG. Role of estrogen receptor-alpha in the anterior pituitary gland. Mol Endocrinol 1997; 11 (6) 674-681
    CrossrefPubMedGoogle Scholar
  • 51 Lindzey J, Wetsel WC, Couse JF, Stoker T, Cooper R, Korach KS. Effects of castration and chronic steroid treatments on hypothalamic gonadotropin-releasing hormone content and pituitary gonadotropins in male wild-type and estrogen receptor-alpha knockout mice. Endocrinology 1998; 139 (10) 4092-4101
    CrossrefPubMedGoogle Scholar
  • 52 Singh SP, Wolfe A, Ng Y , et al. Impaired estrogen feedback and infertility in female mice with pituitary-specific deletion of estrogen receptor alpha (ESR1). Biol Reprod 2009; 81 (3) 488-496
    CrossrefPubMedGoogle Scholar
  • 53 Chen M, Wolfe A, Wang X, Chang C, Yeh S, Radovick S. Generation and characterization of a complete null estrogen receptor alpha mouse using Cre/LoxP technology. Mol Cell Biochem 2009; 321 (1-2) 145-153
    CrossrefPubMedGoogle Scholar
  • 54 Couse JF, Curtis SW, Washburn TF , et al. Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene. Mol Endocrinol 1995; 9 (11) 1441-1454
    CrossrefPubMedGoogle Scholar
  • 55 Antal MC, Krust A, Chambon P, Mark M. Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERbeta-null mutant. Proc Natl Acad Sci U S A 2008; 105 (7) 2433-2438
    CrossrefPubMedGoogle Scholar
  • 56 Krege JH, Hodgin JB, Couse JF , et al. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A 1998; 95 (26) 15677-15682
    CrossrefPubMedGoogle Scholar
  • 57 Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000; 127 (19) 4277-4291
    PubMedGoogle Scholar
  • 58 Couse JF, Curtis Hewitt S, Korach KS. Receptor null mice reveal contrasting roles for estrogen receptor alpha and beta in reproductive tissues. J Steroid Biochem Mol Biol 2000; 74 (5) 287-296
    CrossrefPubMedGoogle Scholar
  • 59 Leng G. Might oestrogen act directly on GnRH neurones?. J Neuroendocrinol 1999; 11 (5) 323-324
    PubMedGoogle Scholar
  • 60 Butler JA, Sjöberg M, Coen CW. Evidence for oestrogen receptor alpha-immunoreactivity in gonadotrophin-releasing hormone-expressing neurones. J Neuroendocrinol 1999; 11 (5) 331-335
    PubMedGoogle Scholar
  • 61 Hrabovszky E, Shughrue PJ, Merchenthaler I , et al. Detection of estrogen receptor-beta messenger ribonucleic acid and 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2000; 141 (9) 3506-3509
    CrossrefPubMedGoogle Scholar
  • 62 Hrabovszky E, Steinhauser A, Barabás K , et al. Estrogen receptor-beta immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2001; 142 (7) 3261-3264
    CrossrefPubMedGoogle Scholar
  • 63 Legan SJ, Tsai HW. Oestrogen receptor-alpha and -beta immunoreactivity in gonadotropin-releasing hormone neurones after ovariectomy and chronic exposure to oestradiol. J Neuroendocrinol 2003; 15 (12) 1164-1170
    CrossrefPubMedGoogle Scholar
  • 64 Kalló I, Butler JA, Barkovics-Kalló M, Goubillon ML, Coen CW. Oestrogen receptor beta-immunoreactivity in gonadotropin releasing hormone-expressing neurones: regulation by oestrogen. J Neuroendocrinol 2001; 13 (9) 741-748
    PubMedGoogle Scholar
  • 65 Skinner DC, Dufourny L. Oestrogen receptor beta-immunoreactive neurones in the ovine hypothalamus: distribution and colocalisation with gonadotropin-releasing hormone. J Neuroendocrinol 2005; 17 (1) 29-39
    CrossrefPubMedGoogle Scholar
  • 66 Hrabovszky E, Kalló I, Szlávik N, Keller E, Merchenthaler I, Liposits Z. Gonadotropin-releasing hormone neurons express estrogen receptor-beta. J Clin Endocrinol Metab 2007; 92 (7) 2827-2830
    CrossrefPubMedGoogle Scholar
  • 67 Davies MP, O’Neill PA, Innes H , et al. Correlation of mRNA for oestrogen receptor beta splice variants ERbeta1, ERbeta2/ERbetacx and ERbeta5 with outcome in endocrine-treated breast cancer. J Mol Endocrinol 2004; 33 (3) 773-782
    CrossrefPubMedGoogle Scholar
  • 68 Mitter D, Ortmann O, Treeck O. Estrogen receptor Beta isoforms — functions and clinical relevance in breast cancer. [in German]. Zentralbl Gynakol 2005; 127 (4) 228-234
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 69 Taylor SE, Martin-Hirsch PL, Martin FL. Oestrogen receptor splice variants in the pathogenesis of disease. Cancer Lett 2010; 288 (2) 133-148
    CrossrefPubMedGoogle Scholar
  • 70 Mellon PL, Windle JJ, Goldsmith PC, Padula CA, Roberts JL, Weiner RI. Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 1990; 5 (1) 1-10
    CrossrefPubMedGoogle Scholar
  • 71 Radovick S, Wray S, Lee E , et al. Migratory arrest of gonadotropin-releasing hormone neurons in transgenic mice. Proc Natl Acad Sci U S A 1991; 88 (8) 3402-3406
    CrossrefPubMedGoogle Scholar
  • 72 Zakaria M, Dunn IC, Zhen S , et al. Phorbol ester regulation of the gonadotropin-releasing hormone (GnRH) gene in GnRH-secreting cell lines: a molecular basis for species differences. Mol Endocrinol 1996; 10 (10) 1282-1291
    CrossrefPubMedGoogle Scholar
  • 73 Martínez-Morales JR, López-Coviella I, Hernández-Jiménez JG , et al. Sex steroids modulate luteinizing hormone-releasing hormone secretion in a cholinergic cell line from the basal forebrain. Neuroscience 2001; 103 (4) 1025-1031
    CrossrefPubMedGoogle Scholar
  • 74 Roy D, Angelini NL, Belsham DD. Estrogen directly represses gonadotropin-releasing hormone (GnRH) gene expression in estrogen receptor-alpha (ERalpha)- and ERbeta-expressing GT1-7 GnRH neurons. Endocrinology 1999; 140 (11) 5045-5053
    CrossrefPubMedGoogle Scholar
  • 75 Ng Y, Wolfe A, Novaira HJ, Radovick S. Estrogen regulation of gene expression in GnRH neurons. Mol Cell Endocrinol 2009; 303 (1–2) 25-33
    CrossrefPubMedGoogle Scholar
  • 76 Otani H, Otsuka F, Takeda M , et al. Regulation of GNRH production by estrogen and bone morphogenetic proteins in GT1-7 hypothalamic cells. J Endocrinol 2009; 203 (1) 87-97
    CrossrefPubMedGoogle Scholar
  • 77 Martínez-Morales JR, Morales A, Marín R , et al. Estrogen modulates norepinephrine-induced accumulation of adenosine cyclic monophosphate in a subpopulation of immortalized luteinizing hormone-releasing hormone secreting neurons from the mouse hypothalamus. Neurosci Lett 2001; 298 (1) 61-64
    CrossrefPubMedGoogle Scholar
  • 78 Sharifi N, Reuss AE, Wray S. Prenatal LHRH neurons in nasal explant cultures express estrogen receptor beta transcript. Endocrinology 2002; 143 (7) 2503-2507
    CrossrefPubMedGoogle Scholar
  • 79 Hu L, Gustofson RL, Feng H , et al. Converse regulatory functions of estrogen receptor-alpha and -beta subtypes expressed in hypothalamic gonadotropin-releasing hormone neurons. Mol Endocrinol 2008; 22 (10) 2250-2259
    CrossrefPubMedGoogle Scholar
  • 80 Spergel DJ, Krüth U, Hanley DF, Sprengel R, Seeburg PH. GABA- and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci 1999; 19 (6) 2037-2050
    PubMedGoogle Scholar
  • 81 Suter KJ, Song WJ, Sampson TL , et al. Genetic targeting of green fluorescent protein to gonadotropin-releasing hormone neurons: characterization of whole-cell electrophysiological properties and morphology. Endocrinology 2000; 141 (1) 412-419
    CrossrefPubMedGoogle Scholar
  • 82 Chu Z, Andrade J, Shupnik MA, Moenter SM. Differential regulation of gonadotropin-releasing hormone neuron activity and membrane properties by acutely applied estradiol: dependence on dose and estrogen receptor subtype. J Neurosci 2009; 29 (17) 5616-5627
    CrossrefPubMedGoogle Scholar
  • 83 Temple JL, Laing E, Sunder A, Wray S. Direct action of estradiol on gonadotropin-releasing hormone-1 neuronal activity via a transcription-dependent mechanism. J Neurosci 2004; 24 (28) 6326-6333
    CrossrefPubMedGoogle Scholar
  • 84 Romanò N, Lee K, Abrahám IM, Jasoni CL, Herbison AE. Nonclassical estrogen modulation of presynaptic GABA terminals modulates calcium dynamics in gonadotropin-releasing hormone neurons. Endocrinology 2008; 149 (11) 5335-5344
    CrossrefPubMedGoogle Scholar
  • 85 Abe H, Keen KL, Terasawa E. Rapid action of estrogens on intracellular calcium oscillations in primate luteinizing hormone-releasing hormone-1 neurons. Endocrinology 2008; 149 (3) 1155-1162
    PubMedGoogle Scholar
  • 86 Abe H, Terasawa E. Firing pattern and rapid modulation of activity by estrogen in primate luteinizing hormone releasing hormone-1 neurons. Endocrinology 2005; 146 (10) 4312-4320
    CrossrefPubMedGoogle Scholar
  • 87 Nishimura I, Ui-Tei K, Saigo K, Ishii H, Sakuma Y, Kato M. 17beta-estradiol at physiological concentrations augments Ca(2+) -activated K+ currents via estrogen receptor beta in the gonadotropin-releasing hormone neuronal cell line GT1-7. Endocrinology 2008; 149 (2) 774-782
    PubMedGoogle Scholar
  • 88 Morales A, Gonzalez M, Marin R, Diaz M, Alonso R. Estrogen inhibition of norepinephrine responsiveness is initiated at the plasma membrane of GnRH-producing GT1-7 cells. J Endocrinol 2007; 194 (1) 193-200
    CrossrefPubMedGoogle Scholar
  • 89 Kurita T, Lee K, Saunders PT , et al. Regulation of progesterone receptors and decidualization in uterine stroma of the estrogen receptor-alpha knockout mouse. Biol Reprod 2001; 64 (1) 272-283
    CrossrefPubMedGoogle Scholar
  • 90 Kraus WL, Montano MM, Katzenellenbogen BS. Cloning of the rat progesterone receptor gene 5′-region and identification of two functionally distinct promoters. Mol Endocrinol 1993; 7 (12) 1603-1616
    CrossrefPubMedGoogle Scholar
  • 91 Kastner P, Krust A, Turcotte B , et al. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 1990; 9 (5) 1603-1614
    PubMedGoogle Scholar
  • 92 Pak TR, Chung WC, Roberts JL, Handa RJ. Ligand-independent effects of estrogen receptor beta on mouse gonadotropin-releasing hormone promoter activity. Endocrinology 2006; 147 (4) 1924-1931
    PubMedGoogle Scholar
  • 93 Abrahám IM, Han SK, Todman MG, Korach KS, Herbison AE. Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J Neurosci 2003; 23 (13) 5771-5777
    PubMedGoogle Scholar