A selective membrane estrogen receptor agonist maintains autonomic functions in hypoestrogenic states

Brain Research

Volumn 1514, Issue , 2013, Pages 75-82

  Kelly, Martin J ^a,b   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

Desensitization; G protein coupled; G q mER; GABAB and opioid receptors; Hot flash; Inwardly rectifying K+ (GIRK) channel; Obesity; Osteoporosis; Proopiomelanocortin (POMC)

Indexed keywords

BETA ENDORPHIN; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; HORMONE RECEPTOR STIMULATING AGENT; MESSENGER RNA; METABOTROPIC RECEPTOR 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROPEPTIDE Y; PHOSPHATIDYLINOSITOL 3 KINASE; TAMOXIFEN;

AFTERHYPERPOLARIZATION; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; BINDING AFFINITY; BONE DENSITY; BONE REMODELING; CORE TEMPERATURE; DESENSITIZATION; DIMERIZATION; DRUG POTENCY; ENERGY BALANCE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEEDBACK SYSTEM; GENE DELETION; GENETIC TRANSCRIPTION; GONADECTOMY; HOT FLUSH; HUMAN; HYPOTHALAMUS; IN VITRO STUDY; INTRACELLULAR SIGNALING; LONG TERM POTENTIATION; LOSS OF FUNCTION MUTATION; MENOPAUSE; NONHUMAN; OSTEOPOROSIS; OVARIECTOMY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; THERMOREGULATION;

ANIMALS; AUTONOMIC NERVOUS SYSTEM DISEASES; ESTROGENS; HUMANS; HYPOGONADISM; HYPOTHALAMUS; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 84878479510     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.03.020     Document Type: Article

References (119)

1. T.W. Abel, and N.E. Rance Proopiomelanocortin gene expression is decreased in the infundibular nucleus of postmenopausal women Mol. Brain Res. 69 1999 202 208
2. I.M. Abraham, S.K. Han, M.G. Todman, K.S. Korach, and A.E. Herbison Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo J. Neurosci. 23 2003 5771 5777
3. I.M. Abrahám, M.G. Todman, K.S. Korach, and A.E. Herbison Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signaling in mouse brain Endocrinology 145 2004 3055 3061
4. H.B. Ahdieh, and G.N. Wade 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
5. S.M. Appleyard, M. Hayward, J.I. Young, A.A. Butler, R.D. Cone, M. Rubinstein, and M.J. Low A role for the endogenous opioid beta-endorphin in energy homeostasis Endocrinology 144 2003 1753 1760
6. L. Asarian, and N. Geary 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
7. H.H.G. Berendsen, A.H.J. Weekers, and H.J. Kloosterboer Effect of tibolone and raloxifene on the tail temperature of oestrogen-deficient rats Eur. J. Pharmacol. 419 2001 47 54
8. C.L. Bethea, D.L. Hess, A.A. Widmann, and J.M. Henningfeld Effects of progesterone on prolactin, hypothalamic beta-endorphin, hypothalamic substance P, and midbrain serotonin in guinea pigs Neuroendocrinology 61 1995 695 703
9. R. Bi, M.R. Foy, R.M. Vouimba, R.F. Thompson, and M. Baudry Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway Proc. Natl. Acad. Sci. USA 98 2001 13391 13395
10. C.G. Bologa, C.M. Revankar, S.M. Young, B.S. Edwards, J.B. Arterburn, A.S. Kiselyov, M.A. Parker, S.E. Tkachenko, N.P. Savchuck, L.A. Sklar, T.I. Oprea, and E.R. Prossnitz Virtual and biomolecular screening converge on a selective agonist for GPR30 Nat. Chem. Biol. 2 2006 207 212
11. G. Bondar, J. Kuo, N. Hamid, and P. Micevych Estradiol-induced estrogen receptor-α trafficking J. Neurosci. 29 2009 15323 15330
12. J.A. Boulant Neuronal basis of Hammel's model for set-point thermoregulation J. Appl. Physiol. 100 2006 1347 1354
13. M.I. Boulware, H. Kordasiewicz, and P.G. Mermelstein Caveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons J. Neurosci. 27 2007 9941 9950
14. M.I. Boulware, J.P. Weick, B.R. Becklund, S.P. Kuo, R.D. Groth, and P.G. Mermelstein 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
15. E. Brailoiu, S.L. Dun, G.C. Brailoiu, K. Mizuo, L.A. Sklar, T.I. Oprea, E.R. Prossnitz, and N.J. Dun Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system J. Endocrinol. 193 2007 311 321
16. E.M. Brooks, A.L. Morgan, J.M. Pierzga, S.L. Wladkowski, J.T. O'Gorman, J.A. Derr, and W.L. Kenney Chronic hormone replacement therapy alters thermoregulatory and vasomotor function in postmenopausal women J. Appl. Physiol. 97 1997 477 484
17. P.C. Butera, and J.A. Czaja Intracranial estradiol in ovariectomized guinea pigs: effects on ingestive behaviors and body weight Brain Res. 322 1984 41 48
18. + current in hippocampal pyramidal neurons J. Neurosci. 23 2003 6338 6344
19. A.C.B. Cato, A. Nestl, and S. Mink Rapid actions of steroid receptors in cellular signaling pathways Science's STKE 2002 2002 re9 re21
20. D.J. Clegg, L.M. Brown, S.C. Woods, and S.C. Benoit Gonadal hormones determine sensitivity to central leptin and insulin Diabetes 55 2006 978 987
21. D.J. Clegg, L.M. Brown, J.M. Zigman, C.J. Kemp, A.D. Strader, S.C. Benoit, S.C. Woods, M. Mangiaracina, and N. Geary Estradiol-dependent decrease in the orexigenic potency of ghrelin in female rats Diabetes 56 2007 1051 1058
22. G.B. Colvin, and C.H. Sawyer Induction of running activity by intracerebral implants of estrogen in overiectomized rats Neuroendocrinology 4 1969 309 320
23. J.F. Couse, and K.S. Korach Estrogen receptor null mice: what have we learned and where will they lead us? Endocr. Rev. 20 1999 358 417
24. W.R. Crowley, R.E. Tessel, T.L. O'Donohue, B.A. Adler, and S.P. Kalra Effects of ovarian hormones on the concentrations of immunoreactive neuropeptide Y in discrete brain regions of the female rat: correlation with serum luteinizing hormone (LH) and median eminence LH-releasing hormone Endocrinology 117 1985 1151 1155
25. 35S]GTPgammaS binding in guinea pig hypothalamus: effects of estrogen Brain Res. 791 1998 341 346
26. J.A. Czaja Sex differences in the activational effects of gonadal hormones on food intake and body weight Physiol. Behav. 33 1984 553 558
27. J.A. Czaja, and R.W. Goy Ovarian hormones and food intake in female guinea pigs and rhesus monkeys Horm. Behav. 6 1975 329 349
28. D.C. Deecher, P.D. Alfinito, L. Leventhal, S. Cosmi, G.H. Johnston, I. Merchanthaler, and R. Winneker Alleviation of thermoregulatory dysfunction with the new serotonin and norepinephrine reuptake inhibitor desvenlafaxine succinate in ovariectomized rodent models Endocrinology 148 2007 1376 1383
29. K. Deisseroth, P.G. Mermelstein, H. Xia, and R.W. Tsien Signaling from synapse to nucleus: the logic behind the mechanisms Curr. Opin. Neurobiol. 13 2003 354 365
30. P. Dewing, M.I. Boulware, K. Sinchak, A. Christensen, P.G. Mermelstein, and P.E. Micevych Membrane estrogen receptor-α interactions with metabotropic glutamate receptor 1a modulate female sexual receptivity in rats J. Neurosci. 27 2007 9294 9300
31. R. Dominguez, and P. Micevych Estradiol rapidly regulates membrane estrogen receptor levels in hypothalamic neurons J. Neurosci. 30 2010 12589 12596
32. D.B. Dubal, H. Zhu, J. Yu, S.W. Rau, P.J. Shughrue, I. Merchenthaler, M.S. Kindy, and P.M. Wise Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury Proc. Natl. Acad. Sci. USA 98 2001 1952 1957
33. F. Elefteriou, J.D. Ahn, S. Takeda, M. Starbuck, X. Yang, X. Liu, H. Kondo, W.G. Richards, T.W. Bannon, M. Noda, K. Clement, C. Valsse, and G. Karsenty Leptin regulation of bone resorption by the sympathetic nervous system and CART Nature 434 2005 514 520
34. H. Endoh, H. Sasaki, K. Maruyama, K. Takeyama, I. Waga, T. Shimizu, S. Kato, and H. Kawashima Rapid activation of MAP Kinase by estrogen in the bone cell line Biochem. Biophys. Res. Commun. 235 1997 99 102
35. E.J. Filardo 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
36. E.J. Filardo, J.A. Quinn, K.I. Bland, and A.R.J. Frackelton 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
37. E.J. Filardo, J.A. Quinn, A.R. Frackelton Jr.; and K.I. Bland 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
38. E.J. Filardo, and P. Thomas GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release Trends Endocrinol. Metab. 16 2005 362 367
39. M.R. Foy, J. Xu, X. Xie, R.D. Brinton, R.F. Thompson, and T.W. Berger 17 β-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation J. Neurophysiol. 81 1999 925 929
40. R.R. Freedman Hot flashes: behavorial treatments, mechanisms, and relation to sleep Am. J. Med. 118 2005 1245 1305
41. R.R. Freedman, and C.M. Blacker Estrogen raises the sweating threshold in postmenopausal women with hot flashes Fertil. Steril. 77 2002 487 490
42. R.R. Freedman, D. Norton, S. Woodward, and G. Cornelissen Core body temperature and circadian rhythm of hot flashes in meopausal women J. Clin. Endocrinol. Metab. 80 1995 2354 2358
43. T. Funakoshi, A. Yanai, K. Shinoda, M.M. Kawano, and Y. Mizukami G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane Biochem. Biophys. Res. Commun. 346 2006 904 910
44. R.F. Furchgott Pharmacological characterization of receptors: its relation to radioligand-binding studies Fed. Proc. 37 1978 115 120
45. R.R. Gainetdinov, R.T. Premont, L.M. Bohn, R.J. Lefkowitz, and M.G. Caron Desensitization of G protein-coupled receptors and neuronal functions Annu. Rev. Neurosci. 27 2004 107 144
46. N. Geary, L. Asarian, K.S. Korach, D.W. Pfaff, and S. Ogawa Deficits in E2-dependent control of feeding, weight gain, and cholecystokinin satiation in ER-alpha null mice Endocrinol. 142 2001 4751 4757
47. J.D. Griffin, C.B. Saper, and J.A. Boulant Synaptic and morphological characteristics of temperature-sensitive and -insensitive rat hypothalamic neurons J. Physiol. 537 2 2001 521 535
48. G. Gu, A.A. Rojo, M.C. Zee, J. Yu, and R.B. Simerly Hormonal regulation of CREB phosphorylation in the anteroventral periventricular nucleus J. Neurosci. 16 1996 3035 3044
49. Q. Gu, K.S. Korach, and R.L. Moss Rapid action of 17beta-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors Endocrinology 140 1999 660 666
50. Q. Gu, and R.L. Moss 17beta-estradiol potentiates kainate-induced currents via activation of the cAMP cascade J. Neurosci. 16 1996 3620 3629
51. Q. Gu, and R.L. Moss Novel mechanism for non-genomic action of 17beta-oestradiol on kainate-induced currents in isolated rat CA1 hippocampal neurons J. Physiol. (London) 506 1998 745 754
52. M.D. Hayward, J.E. Pintar, and M.J. Low Selective reward deficit in mice lacking β-endorphin and enkephalin J. Neurosci. 22 2002 8251 8258
53. S.C. Hewitt, B.J. Deroo, K. Hansen, J. Collins, S. Grissom, C. Afshari, and K.S. Korach Estrogen receptor-dependent genomic responses in the uterus mirror the biphasic physiological response to estrogen Mol. Endocrinol. 17 2003 2070 2083
54. G.Z. Huang, and C.S. Woolley Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism Neuron 74 2012 801 808
55. M.E.E. Jones, A.W. Thorburn, K.L. Britt, K.N. Hewitt, N.G. Wreford, J. Proietto, O.K. Oz, B.J. Leury, K.M. Robertson, S.G. Yao, and E.R. Simpson Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity Proc. Natl. Acad. Sci. USA 97 2000 12735 12740
56. M.J. Kelly, and O.K. Rønnekleiv Rapid membrane effects of estrogen in the central nervous system D.W. Pfaff, Hormones, Brain and Behavior 2002 Academic Press San Diego 361 380
57. B.P. Kenealy, K.L. Keen, O.K. Rønnekleiv, and E. Terasawa STX, a novel nonsteroidal estrogenic compound, induces rapid action in primate GnRH neuronal calcium dynamics and peptide release Endocrinology 152 2011 182 191
58. B.S. Komm, Y.P. Kharode, P.V.N. Bodine, H.A. Harris, C.P. Miller, and C.R. Lyttle Bazedoxifene Acetate: a selective estrogen receptor modulator with improved selectivity Endocrinology 146 2005 3999 4008
59. J. Kuo, O.R. Hariri, G. Bondar, J. Ogi, and P. Micevych Membrane estrogen receptor-α interacts with metabotropic glutamate receptor type 1a to mobilize intracellular calcium in hypothalamic astrocytes Endocrinology 150 2009 1369 1376
60. A.H. Lagrange, O.K. Rønnekleiv, and M.J. Kelly Modulation of G protein-coupled receptors by an estrogen receptor that activates protein kinase A Mol. Pharmacol. 51 1997 605 612
61. D. Lebesgue, M. Traub, M. De Butte-Smith, C. Chen, R.S. Zukin, M.J. Kelly, and A.M. Etgen Acute administration of non-classical estrogen receptor agonists attenuates ischemia-induced hippocampal neuron loss in middle-aged female rats PLos One 5 2010 1 8
62. A. Malyala, P. Pattee, S.R. Nagalla, M.J. Kelly, and O.K. Rønnekleiv Suppression subtractive hybridization and microarray identification of estrogen regulated hypothalamic genes Neurochem. Res. 29 2004 1189 1200
63. A. Malyala, C. Zhang, D. Bryant, M.J. Kelly, and O.K. Rønnekleiv PI3K signaling effects in hypothalamic neurons mediated by estrogen J. Comp. Neurol. 506 2008 895 911
64. T.A. McCaffrey, and J.A. Czaja 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
65. I. Merchenthaler, J.M. Funkhouser, J.M. Carver, S.G. Lundeen, K. Ghosh, and R.C. Winneker The effect of estrogens and antiestrogens in a rat model for hot flush Maturitas 30 1998 307 316
66. P. Micevych, and R. Dominguez Membrane estradiol signaling in the brain Front. Neuroendocrinol. 30 2009 315 327
67. M.L. Moline, L. Broch, R. Zak, and V. Gross Sleep in women across the life cycle from adulthood through menopause Sleep Med. Rev. 7 2003 155 177
68. S. Musatov, W. Chen, D.W. Pfaff, C.V. Mobbs, X.-J. Yang, D.J. Clegg, M.G. Kaplitt, and S. Ogawa Silencing of estrogen receptor α in the ventromedial nucleus of hypothalamus leads to metabolic syndrome Proc. Natl. Acad. Sci. USA 104 2007 2501 2506
69. K. Nakamura, K. Matsumura, T. Kaneko, S. Kobayashi, H. Katoh, and M. Negishi The rostral raphe pallidus nucleus mediates pyrogenic transmission from the preoptic area J. Neurosci. 22 2002 4600 4610
70. K. Nakamura, and S.F. Morrison A thermosensory pathway mediating heat-defense responses Proc. Natl. Acad. Sci. USA 107 2010 8848 8853
71. S.D. Noel, K.L. Keen, D.I. Baumann, E.J. Filardo, and E. Terasawa Involvement of G-protein couple receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons Mol. Endocrinol. 3 2009 349 359
72. S.L. Padilla, J.S. Carmody, and L.M. Zeltser Pomc-expressing progenitors give rise to antagonistic neuronal populations in hypothalamic feeding circuits Nat. Med. 16 2010 403 405
73. S.L. Padilla, D. Reef, and L.M. Zeltser Defining POMC neurons using transgenic reagents: impact of transient Pomc expression in diverse immature neuronal populations Endocrinology 153 2012 1 13
74. C.J. Park, Z. Zhao, C. Glidewell-Kenney, M. Lazic, P. Chambon, A. Krust, J. Weiss, D.J. Clegg, A. Dunaif, J.L. Jameson, and J.E. Levine Genetic rescue of nonclassical ERα signaling normalizes energy balance in obese Erα-null mutant mice J. Clin. Invest. 121 2011 604 612
75. A. Pedram, M. Razandi, and E.R. Levin Nature of functional estrogen receptors at the plasma membrane Mol. Endocrinol. 20 2006 1996 2009
76. G. Pelletier, S. Li, V. Luu-The, and F. Labrie Oestrogenic regulation of pro-opiomelanocortin, neuropeptide Y and corticotrophin-releasing hormone mRNAs in mouse hypothalamus J. Neuroendocrinol. 19 2007 426 431
77. E.R. Prossnitz, J.B. Arterburn, and L.A. Sklar GPR30: A G protein-coupled receptor for estrogen Mol. Cell. Endocrinol. 265-266 2007 138 142
78. E.R. Prossnitz, J.B. Arterburn, H.O. Smith, T.I. Oprea, L.A. Sklar, and H.J. Hathaway Estrogen signaling through the transmembrane G protein-coupled receptor GPR30 Annu. Rev. Physiol. 70 2008 165 190
79. J. Qiu, M.A. Bosch, S.C. Tobias, D.K. Grandy, T.S. Scanlan, O.K. Rønnekleiv, and M.J. Kelly 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
80. J. Qiu, M.A. Bosch, S.C. Tobias, A. Krust, S. Graham, S. Murphy, K.S. Korach, P. Chambon, T.S. Scanlan, O.K. Rønnekleiv, and M.J. Kelly A G protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis J. Neurosci. 26 2006 5649 5655
81. J. Qiu, O.K. Rønnekleiv, and M.J. Kelly Modulation of hypothalamic neuronal activity through a novel G-protein coupled estrogen membrane receptor Steroids 73 2008 985 991
82. J. Qiu, C. Xue, M.A. Bosch, J.G. Murphy, W. Fan, O.K. Rønnekleiv, and M.J. Kelly Serotonin 5HT2c receptor signaling in hypothalamic POMC neurons: role in energy homeostasis in females Mol. Pharm. 72 2007 885 896
83. A.J. Rapkin Vasomotor symptoms in menopause: physiologic condition and central nervous system approaches to treatment Am. J. Obstet. Gynecol. 196 2007 97 106
84. M. Razandi, A. Pedram, G.L. Greene, and E.R. Levin 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
85. T.A. Roepke Oestrogen modulates hypothalmic control of energy homeostasis through multiple mechanisms J. Neuroendocrinol. 21 2009 141 150
86. T.A. Roepke, M.A. Bosch, E.A. Rick, B. Lee, E.J. Wagner, D. Seidlová-Wuttke, W. Wuttke, T.S. Scanlan, O.K. Rønnekleiv, and M.J. Kelly Contribution of a membrane estrogen receptor to the estrogenic regulation of body temperature and energy homeostasis Endocrinology 151 2010 4926 4937
87. T.A. Roepke, C. Xue, M.A. Bosch, T.S. Scanlan, M.J. Kelly, and O.K. Rønnekleiv Genes associated with membrane-initiated signaling of estrogen and energy homeostasis Endocrinology 149 2008 6113 6124
88. O.K. Rønnekleiv, and M.J. Kelly Diversity of ovarian steroid signaling in the hypothalamus Front. Neuroendocrinol. 26 2005 65 84
89. C.N. Rudick, and C.S. Woolley Selective estrogen receptor modulators regulate phasic activation of hippocampal CA1 pyramidal cells by estrogen Endocrinology 144 2003 179 187
90. H. Shimizu, K. Ohtani, Y. Kato, Y. Tanaka, and M. Mori Estrogen increases hypothalamic neuropeptide Y (NPY) mRNA expression in ovariectomized obese rat Neurosci. Lett. 204 1996 81 84
91. J.W. Simpkins, M.J. Katovich, and C. Song Similarities between morphine withdrawal in the rat and the menopausal hot flush Life Sci. 32 1983 1957 1966
92. C.A. Singer, X.A. Figueroa-Masot, R.H. Batchelor, and D.M. Dorsa The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons J. Neurosci. 19 1999 2455 2463
93. K. Sipe, L. Leventhal, K. Burroughs, S. Cosmi, G.H. Johnston, and D.C. Deecher Serotonin 2A receptors modulate tail-skin temperature in two rodent models of estrogen deficiency-related thermoregulatory dysfunction Brain Res. 1028 2004 191 202
94. T. Smejkalova, and C.S. Woolley Estradiol acutely potentiates hippocampal excitatory synaptic transmission through a presynaptic mechanism J. Neurosci. 30 2010 16137 16148
95. E.P. Smith, J. Boyd, G.R. Frank, H. Takahashi, R.M. Cohen, B. Specker, T.C. Williams, D.B. Lubahn, and K.S. Korach Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man N. Engl. J. Med. 331 No. 16 1994 1056 1061
96. V. Stearns, L. Ullmer, J.F. Lopez, Y. Smith, C. Isaacs, and D.F. Hayes Hot flushes Lancet 360 2002 1851 1861
97. V.L. Sylvia, J. Walton, D. Lopez, D.D. Dean, B.D. Boyan, and Z. Schwartz 17 beta-estradiol-BSA conjugates and 17 beta-estradiol regulate growth plate chondrocytes by common membrane associated mechanisms involving PKC dependent and independent signal transduction J. Cell. Biochem. 81 2002 413 429
98. É.M. Szegõ, K. Barabás, J. Balog, N. Szilágyi, K.S. Korach, G. Juhász, and I.M. Abrahám Estrogen induces estrogen receptor α-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
99. S. Takeda, F. Elefteriou, R. Levasseur, X. Liu, L. Zhao, K.L. Parker, D. Armstrong, P. Ducy, and G. Karsenty Leptin regulates bone formation via the sympathetic nervous system Cell 111 2002 305 317
100. C.G. Tankersley, W.C. Nicholas, D.R. Deaver, D. Mikita, and W.L. Kenney Estrogen replacement in middle-aged women: thermoregulatory responses to exercise in the heat J. Appl. Physiol. 73 1992 1238 1245
101. P. Thomas, Y. Pang, E.J. Filardo, and J. Dong Identity of an estrogen membrane receptor coupled to a G-protein in human breast cancer cells Endocrinology 146 2005 624 632
102. J.E. Thornton, M.D. Loose, M.J. Kelly, and O.K. Rønnekleiv 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
103. S.C. Tobias, J. Qiu, M.J. Kelly, and T.S. Scanlan Synthesis and biological evaluation of SERMs with potent nongenomic estrogenic activity ChemMedChem 1 2006 565 571
104. C.D. Toran-Allerand Estrogen and the brain: beyond ER-α, ER-β and 17β-estradiol Ann. NY Acad. Sci. 1052 2005 136 144
105. C.D. Toran-Allerand Minireview: a plethora of estrogen receptors in the brain: where will it end? Endocrinology 145 2004 1069 1074
106. C.B. Wade, S. Robinson, R.A. Shapiro, and D.M. Dorsa 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
107. E.J. Wagner, O.K. Rønnekleiv, M.A. Bosch, and M.J. Kelly Estrogen biphasically modifies hypothalamic GABAergic function concomitantly with negative and positive control of luteinizing hormone release J. Neurosci. 21 2001 2085 2093
108. J.J. Watters, J.S. Campbell, M.J. Cunningham, E.G. Krebs, and D.M. Dorsa Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription Endocrinology 138 1997 4030 4033
109. J.J. Watters, and D.M. Dorsa Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signaling mechanisms J. Neurosci. 18 1998 6672 6680
110. P.J. Weatherill, A.P.M. Wilson, R.I. Nicholson, P. Davies, and A.E. Wakeling Interaction of the antioestrogen ICI 164,384 with the oestrogen receptor J. Steroid Biochem. Mol. Biol. 30 1988 263 266
111. M. Wong, and R.L. Moss Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons J. Neurosci. 12 1992 3217 3225
112. J.-P. Wuarin, and F.E. Dudek Direct effects of an opioid peptide selective for μ-receptors: intracellular recordings in the paraventricular and supraoptic nuclei of the guinea pig Neuroscience 36 1990 291 298
113. Y. Xu, T.P. Nedugadi, L. Zhu, N. Sobhani, B.G. Irani, K.E. Davis, X. Zhang, F. Zou, L.M. Gent, L.D. Hahner, S.A. Khan, C.F. Elias, J.K. Elmquist, and D.J. Clegg Distinct hypothalamic neurons mediate estrogenic effects on energy homeostasis and reproduction Cell Metab. 14 2011 453 465
114. V.K. Yadav, F. Oury, N. Suda, Z.-W. Liu, X.-B. Gao, C. Confavreux, K.C. Klemenhagen, K.F. Tanaka, J.A. Gingrich, X.E. Guo, L.H. Tecott, J.J. Mann, R. Hen, T.L. Horvath, and G. Karsenty A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure Cell 138 2009 976 989
115. S.-H. Yang, A.D. Sharrocks, and A.J. Whitmarsh Transcriptional regulation by the MAP kinase signaling cascades Gene 320 2003 3 21
116. K. Yoshida, X. Li, G. Cano, M. Lazarus, and C.B. Saper Parallel preoptic pathways for thermoregulation J. Neurosci. 29 2009 11954 11964
117. C. Zhang, M.A. Bosch, E.A. Rick, M.J. Kelly, and O.K. Rønnekleiv 17β-estradiol regulation of T-type calcium channels in gonadotropin- releasing hormone neurons J. Neurosci. 29 2009 10552 10562
118. C. Zhang, M.J. Kelly, and O.K. Rønnekleiv 17β-estradiol rapidly increases adenosine 5′-triphosphate-sensitive potassium channel activity in gonadotropin-releasing hormone neurons via a protein kinase signaling pathway Endocrinology 151 2010 4477 4484
119. Y. Zhou, J.J. Watters, and D.M. Dorsa Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain Endocrinology 137 1996 2163 2166