Control of CNS neuronal excitability by estrogens via membrane-initiated signaling

Molecular and Cellular Endocrinology

Volumn 308, Issue 1-2, 2009, Pages 17-25

  Kelly, Martin J ^a   Rønnekleiv, Oline K ^a,b,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

ER ; ER ; GPR30; mER (a plasma membrane E2 receptor that is G protein coupled)

Indexed keywords

CALCIUM CHANNEL T TYPE; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR; GONADORELIN; LUTEINIZING HORMONE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN; SOMATOMEDIN C;

CALCIUM CELL LEVEL; CELL MEMBRANE; ENERGY BALANCE; ESTROGEN BINDING; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; LEARNING; LONG TERM POTENTIATION; MEMORY; NERVE EXCITABILITY; NEUROSECRETION; NONHUMAN; POSTMENOPAUSE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR AFFINITY; REPRODUCTIVE SUCCESS; REVIEW; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION;

CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; ESTRADIOL; ESTROGENS; GONADOTROPIN-RELEASING HORMONE; HOMEOSTASIS; LEARNING; MEMORY; NEURONS; SIGNAL TRANSDUCTION;

EID: 67449123067     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.03.008     Document Type: Review

References (153)

1. Abe H., Keen K.L., and Terasawa E. Rapid action of estrogens on intracellular calcium oscillations in primate LHRH-1 neurons. Endocrinology 149 (2008) 1155-1162
2. Abe H., and Terasawa E. Firing pattern and rapid modulation of activity by estrogen in primate luteinizing hormone releasing hormone-1 neurons. Endocrinology 146 (2005) 4312-4320
3. Abraham I.M., Han S.K., Todman M.G., Korach K.S., and Herbison A.E. Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J. Neurosci. 23 (2003) 5771-5777
4. Abraham I.M., Todman M.G., Korach K.S., and Herbison A.E. Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signaling in mouse brain. Endocrinology 145 (2004) 3055-3061
5. Ahdieh H.B., and Wade G.N. Effects of hysterectomy on sexual receptivity, food intake, running wheel activity, and hypothalamic estrogen and progestin receptors in rats. J. Comp. Physiol. Psychol. 96 (1982) 886-892
6. Antal M.C., Krust A., Chambon P., and Mark M. Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERβ-null mutant. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 2433-2438
7. Apostolakis E.M., Garai J., Lohmann J.E., Clark J.H., and O'Malley B.W. Epidermal growth factor activates reproductive behavior independent of ovarian steroids in female rodents. Mol. Endocrinol. 14 (2000) 1086-1098
8. Appleyard S.M., Hayward M., Young J.I., Butler A.A., Cone R.D., Rubinstein M., and Low M.J. A role for the endogenous opioid beta-endorphin in energy homeostasis. Endocrinology 144 (2003) 1753-1760
9. Asarian L., and Geary N. Cyclic estradiol treatment normalizes body weight and restores physiological patterns of spontaneous feeding and sexual receptivity in ovariectomized rats. Horm. Behav. 42 (2002) 461-471
10. Bethea C.L., Hess D.L., Widmann A.A., and Henningfeld J.M. Effects of progesterone on prolactin, hypothalamic beta-endorphin, hypothalamic substance P, and midbrain serotonin in guinea pigs. Neuroendocrinology 61 (1995) 695-703
11. Bi R., Broutman G., Foy M.R., Thompson R.F., and Baudry M. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 3602-3607
12. Bliss T.V.P., and Lømo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J. Physiol. 232 (1973) 331-356
13. Bologa C.G., Revankar C.M., Young S.M., Edwards B.S., Arterburn J.B., Kiselyov A.S., Parker M.A., Tkachenko S.E., Savchuck N.P., Sklar L.A., Oprea T.I., and Prossnitz E.R. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol. 2 (2006) 207-212
14. Bosch M.A., Hou J., Kelly M.J., and Rønnekleiv O.K. 17β-Estradiol regulation of the mRNA expression of T-type calcium channel subunits: role of estrogen receptor a and estrogen receptor b. J. Comp. Neurol. 512 (2009) 347-358
15. Boulware M.I., Kordasiewicz H., and Mermelstein P.G. Caveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons. J. Neurosci. 27 (2007) 9941-9950
16. Boulware M.I., Weick J.P., Becklund B.R., Kuo S.P., Groth R.D., and Mermelstein P.G. Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J. Neurosci. 25 (2005) 5066-5078
17. Brailoiu E., Dun S.L., Brailoiu G.C., Mizuo K., Sklar L.A., Oprea T.I., Prossnitz E.R., and Dun N.J. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 193 (2007) 311-321
18. Brann D.W., Dhandapani K., Wakade C., Mahesh V.B., and Khan M.M. Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications. Steroids 72 (2007) 381-405
19. Bryant D.N., Sheldahl L.C., Marriott L.K., Shapiro R.A., and Dorsa D.M. Multiple pathways transmit neuroprotective effects of gonadal steroids. Endocrine 29 (2006) 199-207
20. Butera P.C., and Czaja J.A. Intracranial estradiol in ovariectomized guinea pigs: effects on ingestive behaviors and body weight. Brain Res. 322 (1984) 41-48
21. Cardona-Gómez G.P., Mendez P., and Garcia-Segura L.M. Synergistic interaction of estradiol and insulin-like growth factor-I in the activation of PI3K/Akt signaling in the adult rat hypothalamus. Mol. Brain Res. 107 (2002) 80-88
22. + current in hippocampal pyramidal neurons. J. Neurosci. 23 (2003) 6338-6344
23. Christian C.A., Glidewell-Kenney C., Jameson J.L., and Moenter S.M. Classical estrogen receptor a signaling mediates negative and positive feedback on gonadotropin-releasing hormone neuron firing. Endocrinology 149 (2008) 5328-5334
24. Christian C.A., and Moenter S.M. Estradiol induces diurnal shifts in GABA transmission to gonadotropin-releasing hormone neurons to provide a neural signal for ovulation. J. Neurosci. 27 (2007) 1913-1921
25. Clarkson J., d'Anglemont de Tassigny X., Moreno A.S., Colledge W.H., and Herbison A.E. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J. Neurosci. 28 (2008) 8691-8697
26. Clegg D.J., Brown L.M., Woods S.C., and Benoit S.C. Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 55 (2006) 978-987
27. Clegg D.J., Brown L.M., Zigman J.M., Kemp C.J., Strader A.D., Benoit S.C., Woods S.C., Mangiaracina M., and Geary N. Estradiol-dependent decrease in the orexigenic potency of ghrelin in female rats. Diabetes 56 (2007) 1051-1058
28. Colvin G.B., and Sawyer C.H. Induction of running activity by intracerebral implants of estrogen in overiectomized rats. Neuroendocrinology 4 (1969) 309-320
29. 1-adrenergic response of hypothalamic neurons. Neuroendocrinology 50 (1989) 51-58
30. Couse J.F., and Korach K.S. Estrogen receptor null mice: What have we learned and where will they lead us?. Endocr. Rev. 20 (1999) 358-417
31. 35S]GTPγS binding in guinea pig hypothalamus: effects of estrogen. Brain Res. 791 (1998) 341-346
32. Czaja J.A. Sex differences in the activational effects of gonadal hormones on food intake and body weight. Physiol. Behav. 33 (1984) 553-558
33. Czaja J.A., and Goy R.W. Ovarian hormones and food intake in female guinea pigs and rhesus monkeys. Horm. Behav. 6 (1975) 329-349
34. DeFazio R.A., Heger S., Ojeda S.R., and Moenter S.M. Activation of A-type gamma-aminobutyric receptors excites gonadotropin-releasing hormone neurons. Mol. Endocrinol. 16 (2002) 2872-2891
35. Dewing P., Boulware M.I., Sinchak K., Christensen A., Mermelstein P.G., and Micevych P. Membrane estrogen receptor-α interactions with metabotropic glutamate receptor 1a modulate female sexual receptivity in rats. J. Neurosci. 27 (2007) 9294-9300
36. Dubal D.B., Zhu H., Yu J., Rau S.W., Shughrue P.J., Merchenthaler I., Kindy M.S., and Wise P.M. Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 1952-1957
37. Dupont S., Krust A., Gansmuller A., Dierich A., Chambon P., and Mark M. Effect of single and compound knockouts of estrogen receptors α (ERα) and β (ERβ) on mouse reproductive phenotypes. Development 127 (2000) 4277-4291
38. Erickson K.R., Rønnekleiv O.K., and Kelly M.J. Role of a T-type calcium current in supporting a depolarizing potential, damped oscillations, and phasic firing in vasopressinergic guinea pig supraoptic neurons. Neuroendocrinology 57 (1993) 789-800
39. Etgen A.M., and Acosta-Martinez M. Participation of growth factor signal transduction pathways in estradiol facilitation of female reproductive behavior. Endocrinology 144 (2003) 3828-3835
40. Etgen A.M., Ansonoff M.A., and Quesada A. Mechanisms of ovarian steroid regulation of norepinephrine receptor-mediated signal transduction in the hypothalamus: implications for female reproductive physiology. Horm. Behav. 40 (2001) 169-177
41. Etgen A.M., González-Flores O., and Todd B.J. The role of insulin-like growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors. Front. Neuroendocrinol. 27 (2006) 363-375
42. Fehrenbacher J.C., LoVerme J., Clarke W., Hargreaves K.M., Piomelli D., and Taylor B.K. Rapid pain modulation with nuclear receptor ligands. Brain Res Rev 60 (2009) 114-124
43. Filardo E.J. Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J. Steroid Biochem. Mol. Biol. 80 (2002) 231-238
44. Filardo E.J., Quinn J.A., Bland K.I., and Frackelton A.R.J. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14 (2000) 1649-1660
45. Filardo E.J., Quinn J.A., Frackelton Jr. A.R., and Bland K.I. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol. 16 (2002) 70-84
46. Filardo E.J., and Thomas P. GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol. Metab. 16 (2005) 362-367
47. Foy M.R. 17β-Estradiol: effect on CA1 hippocampal synaptic plasticity. Neurobiol. Learn. Mem. 76 (2001) 239-252
48. Foy M.R., Xu J., Xie X., Brinton R.D., Thompson R.F., and Berger T.W. 17β-Estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J. Neurophysiol. 81 (1999) 925-929
49. Funakoshi T., Yanai A., Shinoda K., Kawano M.M., and Mizukami Y. G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem. Biophys. Res. Commun. 346 (2006) 904-910
50. Geary N. Estradiol, CCK and satiation. Peptides 22 (2001) 1251-1263
51. Glidewell-Kenney C., Weiss J., Hurley L.A., Levine J.E., and Jameson J.L. Estrogen receptor α signaling pathways differentially regulate gonadotropin subunit gene expression and serum follicle-stimulating hormone in the female mouse. Endocrinology 149 (2008) 4168-4176
52. Gu G., Rojo A.A., Zee M.C., Yu J., and Simerly R.B. Hormonal regulation of CREB phosphorylation in the anteroventral periventricular nucleus. J. Neurosci. 16 (1996) 3035-3044
53. Gu Q., Korach K.S., and Moss R.L. Rapid action of 17β-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors. Endocrinology 140 (1999) 660-666
54. Gu Q., and Moss R.L. 17β-Estradiol potentiates kainate-induced currents via activation of the cAMP cascade. J. Neurosci. 16 (1996) 3620-3629
55. Gu Q., and Moss R.L. Novel mechanism for non-genomic action of 17β-estradiol on kainate-induced currents in isolated rat CA1 hippocampal neurones. J. Physiol. (Lond.) 506 (1998) 745-754
56. Han S.-K., Gottsch M.L., Lee K.J., Popa S.M., Smith J.T., Jakawich S.K., Clifton D.K., Steiner R.A., and Herbison A.E. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J. Neurosci. 25 (2005) 11349-11356
57. Harrington W.R., Kim S.H., Funk C.C., Madak-Erdogan Z., Schiff R., Katzenellenbogen J.A., and Katzenellenbogen B.S. Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action. Mol. Endocrinol. 20 (2006) 491-502
58. Harrington W.R., Sheng S., Barnett D.H., Petz L.N., Katzenellenbogen J.A., and Katzenellenbogen B.S. Activities of estrogen receptor alpha-and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol. Cell. Endocrinol. 206 (2003) 13-22
59. Hayward M.D., Pintar J.E., and Low M.J. Selective reward deficit in mice lacking β-endorphin and enkephalin. J. Neurosci. 22 (2002) 8251-8258
60. Herbison A.E. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr. Rev. 19 (1998) 302-330
61. Herbison A.E., and Pape J.R. New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front. Neuroendocrinol. 22 (2001) 292-308
62. 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 141 (2000) 3506-3509
63. Hrabovszky E., Steinhauser A., Barabas K., Shughrue P.J., Petersen S.L., Merchenthaler I., and Liposits Z. Estrogen receptor-beta immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 142 (2001) 3261-3264
64. 2 and its stabilization by Gbg. Nature 391 (1998) 803-806
65. Huguenard J.R., and McCormick D.A. Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J. Neurophysiol. 68 (1992) 1373-1383
66. Jackson G.L., and Kuehl D. Gamma-aminobutyric acid (GABA) regulation of GnRH secretion in sheep. Reproduction 59 (2002) 15-24
67. Jones M.E.E., Thorburn A.W., Britt K.L., Hewitt K.N., Wreford N.G., Proietto J., Oz O.K., Leury B.J., Robertson K.M., Yao S.G., and Simpson E.R. Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 12735-12740
68. Kallo I., Butler J.A., Barkovics-Kallo M., Goubillon M.L., and Coen C.W. Oestrogen receptor beta-immunoreactivity in gonadotropin releasing hormone-expressing neurones: regulation by oestrogen. J. Neuroendocrinol. 13 (2001) 741-748
69. Kato M., Ui-Tei K., Watanabe M., and Sakuma Y. Characterization of voltage-gated calcium currents in gonadotropin-releasing hormone neurons tagged with green fluorescent protein in rats. Endocrinology 144 (2003) 5118-5125
70. B-mediated hyperpolarization of hypothalamic arcuate neurons. J. Neurosci. 12 (1992) 2745-2750
71. Kelly M.J., Qiu J., Wagner E.J., and Rønnekleiv O.K. Rapid effects of estrogen on G protein-coupled receptor activation of potassium channels in the central nervous system (CNS). J. Steroid Biochem. Mol. Biol. 83 (2003) 187-193
72. Kelly M.J., and Rønnekleiv O.K. Rapid membrane effects of estrogen in the central nervous system. In: Pfaff D.W. (Ed). Hormones, Brain and Behavior (2002), Academic Press, San Diego 361-380
73. Kelly M.J., Rønnekleiv O.K., and Eskay R.L. Identification of estrogen-responsive LHRH neurons in the guinea pig hypothalamus. Brain Res. Bull. 12 (1984) 399-407
74. Kow L.M., and Pfaff D.W. The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 12354-12357
75. Krege J.H., Hodgin J.B., Couse J.F., Enmark E., Warner M., Mahler J.F., Sar M., Korach K.S., Gustafsson J.A., and Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 15677-15682
76. Kuiper G.G., Enmark E., Pelto-Huikko M., Nilsson S., and Gustafsson J.A. Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 5925-5930
77. Lagrange A.H., Rønnekleiv O.K., and Kelly M.J. Modulation of G protein-coupled receptors by an estrogen receptor that activates protein kinase A. Mol. Pharmacol. 51 (1997) 605-612
78. Lagrange A.H., Rønnekleiv O.K., and Kelly M.J. Estradiol-17β and μ-opioid peptides rapidly hyperpolarize GnRH neurons: a cellular mechanism of negative feedback?. Endocrinology 136 (1995) 2341-2344
79. Lagrange A.H., Rønnekleiv O.K., and Kelly M.J. The potency of μ-opioid hyperpolarization of hypothalamic arcuate neurons is rapidly attenuated by 17β-estradiol. J. Neurosci. 14 (1994) 6196-6204
80. B response in hypothalamic neurons. Neuroendocrinology 64 (1996) 114-123
81. Leal S., Andrade J.P., Paula-Barbosa M.M., and Madeira M.D. Arcuate nucleus of the hypothalamus: effects of age and sex. J. Comp. Neurol. 401 (1998) 65-88
82. Lee A.W., Kyrozis A., Chevaleyre V., Kow L.-M., Zhou J., Devidze N., Zhang Q., Etgen A.M., and Pfaff D.W. Voltage-dependent calcium channels in ventromedial hypothalamic neurones of postnatal rats: modulation by oestradiol and phenylephrine. J. Neuroendocrinol. 20 (2008) 188-198
83. Loose M.D., Rønnekleiv O.K., and Kelly M.J. Membrane properties and response to opioids of identified dopamine neurons in the guinea pig hypothalamus. J. Neurosci. 10 (1990) 3627-3634
84. Lund T.D., Hinds L.R., and Handa R.J. The androgen 5α-dihydrotestosterone and its metabolite 5α-androstan-3β,17 β-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor β-expressing neurons in the hypothalamus. J. Neurosci. 26 (2006) 1448-1456
85. Malyala A., Kelly M.J., and Rønnekleiv O.K. Estrogen modulation of hypothalamic neurons: activation of multiple signaling pathways and gene expression changes. Steroids 70 (2005) 397-406
86. Malyala A., Zhang C., Bryant D., Kelly M.J., and Rønnekleiv O.K. PI3K signaling effects in hypothalamic neurons mediated by estrogen. J. Comp. Neurol. 506 (2008) 895-911
87. Matsuda K., Sakamoto H., Mori H., Hosokawa K., Kawamura A., Itose M., Nishi M., Prossnitz E.R., and Kawata M. Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation. Neurosci. Lett. 441 (2008) 94-99
88. McCaffrey T.A., and Czaja J.A. Diverse effects of estradiol-17 beta: concurrent suppression of appetite, blood pressure and vascular reactivity in conscious, unrestrained animals. Physiol. Behav. 45 (1989) 649-657
89. McDevitt M.A., Glidewell-Kenney C., Jimenez M.A., Ahearn P.C., Weiss J., Jameson J.L., and Levine J.E. New insights into the classical and non-classical actions of estrogen: evidence from estrogen receptor knock-out and knock-in mice. Mol. Cell. Endocrinol. 290 (2008) 24-30
90. Mendez P., Azcoitia I., and Garcia-Segura L.M. Estrogen receptor alpha forms estrogen-dependent multimolecular complexes with insulin-like growth factor receptor and phosphatidylinositol 3-kinase in the adult rat brain. Mol. Brain Res. 112 (2003) 170-176
91. Micevych P.E., and Mermelstein P.G. Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol. Neurobiol. 38 (2008) 66-77
92. Milewicz A., Bidzinska B., Mikulski E., Demissie M., and Tworowska U. Influence of obesity and menopausal status on serum leptin, cholecystokinin, galanin and neuropeptide Y levels. Gynecol. Endocrinol. 14 (2000) 196-203
93. 1 receptor activation in the arcuate nucleus of female rats. J. Neurosci. 24 (2004) 947-955
94. i-coupled plasma membrane estrogen receptors in immortalized gonadotrophin-releasing hormone neurons. Mol. Endocrinol. 17 (2003) 1792-1804
95. Noel S.D., Keen K.L., Baumann D.I., Filardo E.J., and Terasawa E. Involvement of G-protein couple receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons. Mol. Endocrinol. 23 (2009) 349-359
96. Ogawa S., Eng V., Taylor J., Lubahn D.B., Korach K.S., and Pfaff D.W. Roles of estrogen receptor-alpha gene expression in reproduction-related behaviors in female mice. Endocrinology 139 (1998) 5070-5081
97. Pedram A., Razandi M., and Levin E.R. Nature of functional estrogen receptors at the plasma membrane. Mol. Endocrinol. 20 (2006) 1996-2009
98. atp channel activation and leads to diet-sensitive obesity. J. Clin. Invest. 116 (2006) 1886-1901
99. Poehlman E.T. Menopause, energy expenditure, and body composition. Acta Obstet. Gynecol. Scand. 81 (2002) 603-611
100. Prossnitz E.R., Arterburn J.B., and Sklar L.A. GPR30: a G protein-coupled receptor for estrogen. Mol. Cell. Endocrinol. 265-266 (2007) 138-142
101. Qiu J., Bosch M.A., Jamali K., Xue C., Kelly M.J., and Rønnekleiv O.K. Estrogen upregulates T-type calcium channels in the hypothalamus and pituitary. J. Neurosci. 26 (2006) 11072-11082
102. Qiu J., Bosch M.A., Tobias S.C., Grandy D.K., Scanlan T.S., Rønnekleiv O.K., and Kelly M.J. Rapid signaling of estrogen in hypothalamic neurons involves a novel G protein-coupled estrogen receptor that activates protein kinase C. J. Neurosci. 23 (2003) 9529-9540
103. Qiu J., Bosch M.A., Tobias S.C., Krust A., Graham S., Murphy S., Korach K.S., Chambon P., Scanlan T.S., Rønnekleiv O.K., and Kelly M.J. A G protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis. J. Neurosci. 26 (2006) 5649-5655
104. Qiu J., Rønnekleiv O.K., and Kelly M.J. Modulation of hypothalamic neuronal activity through a novel G-protein coupled estrogen membrane receptor. Steroids 73 (2008) 985-991
105. 1-adrenergic receptor signaling is estradiol dependent in the preoptic area and hypothalamus of female rats. Endocrinology 142 (2001) 599-607
106. 1B-adrenoceptors and female reproductive function. J. Neurosci. 22 (2002) 2401-2408
107. Rapp P.R., Morrison J.H., and Roberts J.A. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J. Neurosci. 23 (2003) 5708-5714
108. Razandi M., Pedram A., Greene G.L., and Levin E.R. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERα and ERβ expressed in Chinese hamster ovary cells. Mol. Endocrinol. 13 (1999) 307-319
109. Revankar C.M., Cimino D.F., Sklar L.A., Arterburn J.B., and Prossnitz E.R. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307 (2005) 1625-1630
110. + channel signaling in the arcuate nucleus. Endocrinology 148 (2007) 4937-4951
111. Roepke T.A., Xue C., Bosch M.A., Scanlan T.S., Kelly M.J., and Rønnekleiv O.K. Genes associated with membrane-initiated signaling of estrogen and energy homeostasis. Endocrinology 149 (2008) 6113-6124
112. Romanò N., Lee K., Ábrahám I.M., Jasoni C.L., and Herbison A.E. Non-classical estrogen modulation of presynaptic GABA terminals modulates calcium dynamics in gonadotropin-releasing hormone (GnRH) neurons. Endocrinology 149 (2008) 5335-5344
113. Rønnekleiv O.K., and Kelly M.J. Diversity of ovarian steroid signaling in the hypothalamus. Front. Neuroendocrinol. 26 (2005) 65-84
114. Rudick C.N., and Woolley C.S. Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. J. Neurosci. 21 (2001) 6532-6543
115. Sah P., and Davies P. Calcium-activated potassium currents in mammalian neurons. Clin. Exp. Pharmacol. Physiol. 27 (2000) 657-663
116. Schild H.O. pA, a new scale for the measurement of drug antagonism. Br. J. Pharmacol. 2 (1947) 189-206
117. Sherwin B.B. Surgical menopause, estrogen, and cognitive function in women: what do the findings tell us?. Ann. N. Y. Acad. Sci. 1052 (2005) 3-10
118. Shimizu H., Ohtani K., Kato Y., Tanaka Y., and Mori M. Estrogen increases hypothalamic neuropeptide Y (NPY) mRNA expression in ovariectomized obese rat. Neurosci. Lett. 204 (1996) 81-84
119. Shimomura Y., Shimizu H., Takahashi M., Sato N., Uehara Y., Fukatsu A., Negishi M., Kobayashi I., and Kobayashi S. The significance of decreased ambulatory activity during the generation by long-term observation of obesity in ovariectomized rats. Physiol. Behav. 47 (1990) 155-159
120. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J. Comp. Neurol. 388 (1997) 507-525
121. Simerly R.B., McCall L.D., and Watson S.J. Distribution of opioid peptides in the preoptic region: immunohistochemical evidence for a steroid-sensitive enkephalin sexual dimorphism. J. Comp. Neurol. 276 (1988) 442-459
122. Singer C.A., Figueroa-Masot X.A., Batchelor R.H., and Dorsa D.M. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J. Neurosci. 19 (1999) 2455-2463
123. Singh M., Setalo G.J., Guan X., Frail D.E., and Toran-Allerand C.D. Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-alpha knock-out mice. J. Neurosci. 20 (2000) 1694-1700
124. Singh M., Setalo Jr. G., Guan X., Warren M., and Toran-Allerand C.D. Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J. Neurosci. 19 (1999) 1179-1188
125. Smith J.T., Popa S.M., Clifton D.K., Hoffman G.E., and Steiner R.A. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J. Neurosci. 26 (2006) 6687-6694
126. Smith Y.R., Giordani B., Lajiness-O'Neill R., and Zubieta J.K. Long-term estrogen replacement is associated with improved nonverbal memory and attentional measures in postmenopausal women. Fertil. Steril. 76 (2001) 1101-1107
127. Spergel D.J., Kruth U., Hanley D.F., Sprengel R., and Seeburg P.H. GABA-and glutamate activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J. Neurosci. 19 (1999) 2037-2050
128. + current in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 4662-4667
129. Suh B.-C., and Hille B. Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 35 (2002) 507-520
130. Suter K.J., and O'Farrell L. Impaired episodic LH secretion in female mice with GFP in GnRH neurons. Am. J. Physiol. Endocrinol. Metab. 295 (2008) E130-E136
131. Suter K.J., Song W.J., Sampson T.L., Wuarin J.-P., Saunders J.T., Dudek F.E., and Moenter S.M. Genetic targeting of green fluorescent protein to gonadotropin-releasing hormone neurons: characterization of whole-cell electrophysiological properties and morphology. Endocrinology 141 (2000) 412-419
132. Szegõ E.M., Barabás K., Balog J., Szilágyi N., Korach K.S., Juhász G., and Abrahám I.M. Estrogen induces estrogen receptor a-dependent cAMP response element-binding protein phosphorylation via mitogen activated protein kinase pathway in basal forebrain cholinergic neurons in vivo. J. Neurosci. 26 (2006) 4104-4110
133. Temple J.L., Laing E., Sunder A., and Wray S. Direct action of estradiol on gonadotropin-releasing hormone-1 neuronal activity via a transcription-dependent mechanism. J. Neurosci. 24 (2004) 6326-6333
134. Temple J.L., and Wray S. BSA-estrogen compounds differentially alter gonadotropin-releasing hormone-1 neuronal activity. Endocrinology 146 (2005) 558-563
135. Thomas P., Pang Y., Filardo E.J., and Dong J. Identity of an estrogen membrane receptor coupled to a G-protein in human breast cancer cells. Endocrinology 146 (2005) 624-632
136. Thornton J.E., Loose M.D., Kelly M.J., and Rønnekleiv O.K. Effects of estrogen on the number of neurons expressing β-endorphin in the medial basal hypothalamus of the female guinea pig. J. Comp. Neurol. 341 (1994) 68-77
137. Toran-Allerand C.D. Estrogen and the brain: beyond ERα, ER-β and 17β-estradiol. Ann. N. Y. Acad. Sci. 1052 (2005) 136-144
138. Toran-Allerand C.D. Minireview: a plethora of estrogen receptors in the brain: Where will it end?. Endocrinology 145 (2004) 1069-1074
139. Toran-Allerand C.D., Guan X., MacLusky N.J., Horvath T.L., Diano S., Singh M., Connolly Jr. E.S., Nethrapalli I.S., and Tinnikov A.A. ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J. Neurosci. 22 (2002) 8391-8401
140. Toran-Allerand C.D., Singh M., and Setalo G.J. Novel mechanisms of estrogen action in the brain: new players in an old story. Front. Neuroendocrinol. 20 (1999) 97-121
141. Vasudevan N., Kow L.M., and Pfaff D.W. Early membrane estrogenic effects required for full expression of slower genomic actions in a nerve cell line. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 12267-12271
142. Wade C.B., Robinson S., Shapiro R.A., and Dorsa D.M. Estrogen receptor (ER)alpha and ERbeta exhibit unique pharmacologic properties when coupled to activation of the mitogen-activated protein kinase pathway. Endocrinology 142 (2001) 2336-2342
143. Wagner E.J., Rønnekleiv O.K., Bosch M.A., and Kelly M.J. Estrogen biphasically modifies hypothalamic GABAergic function concomitantly with negative and positive control of luteinizing hormone release. J. Neurosci. 21 (2001) 2085-2093
144. + channel in hypothalamic γ-aminobutyric acid neurons: pharmacology, estrogen sensitivity and relevance to the control of the reproductive axis. J. Pharmacol. Exp. Ther. 299 (2001) 21-30
145. Weatherill P.J., Wilson A.P.M., Nicholson R.I., Davies P., and Wakeling A.E. Interaction of the antioestrogen ICI 164,384 with the oestrogen receptor. J. Ster. Biochem. Mol. Biol. 30 (1988) 263-266
146. Wintermantel T.M., Campbell R.E., Porteous R., Bock D., Gröne H.-J., Todman M.G., Korach K.S., Greiner E., Perez C.A., Schutz G., and Herbison A.E. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 52 (2006) 271-280
147. Wong M., and Moss R.L. Electrophysiological evidence for a rapid membrane action of the gonadal steroid 17β-estradiol, on CA1 pyramidal neurons of the rat hippocampus. Brain Res. 543 (1991) 148-152
148. Wong M., and Moss R.L. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J. Neurosci. 12 (1992) 3217-3225
149. Wong M., and Moss R.L. Patch-clamp analysis of direct steroidal modulation of glutamate receptor-channels. J. Neuroendocrinol. 6 (1994) 347-355
150. Woolley C.S. Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 47 (2007) 657-680
151. Xu A.W., Kaelin C.B., Takeda K., Akira S., Schwartz M.W., and Barsh G.S. PI3K integrates the action of insulin and leptin on hypothalamic neurons. J. Clin. Invest. 115 (2005) 951-958
152. ATP channels that are regulated by estrogen and responsive to glucose and metabolic inhibition. J. Neurosci. 27 (2007) 10153-10164
153. + channels by distinct PtdIns(4,5)P2 interactions. Nat. Cell. Biol. 1 (1999) 183-188