Estrogen actions on neuroendocrine glia

Neuroendocrinology

Volumn 91, Issue 3, 2010, Pages 211-222

  Micevych, Paul ^a   Bondar, Galyna ^a   Kuo, John ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocytes; Estrogen receptor alpha trafficking; Surface biotinylation

Indexed keywords

CALCIUM ION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; LUTEINIZING HORMONE; MEMBRANE RECEPTOR; METABOTROPIC RECEPTOR 1; PROGESTERONE; PROGESTERONE RECEPTOR; METABOTROPIC RECEPTOR;

ASTROCYTE; BIOTINYLATION; BRAIN REGION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL COMMUNICATION; CELL MEMBRANE; ESTRADIOL BLOOD LEVEL; ESTROGEN ACTIVITY; ESTROGEN SYNTHESIS; GLIA; HORMONAL REGULATION; HYPOTHALAMUS; LUTEINIZING HORMONE RELEASE; NEUROSECRETORY CELL; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; PHENOTYPE; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROESTRUS; PROGESTERONE SYNTHESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; REVIEW; ANIMAL; BIOLOGICAL MODEL; FEMALE; HUMAN; METABOLISM; PHYSIOLOGY; REPRODUCTION; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; HYPOTHALAMUS; MODELS, BIOLOGICAL; PROGESTERONE; RECEPTORS, METABOTROPIC GLUTAMATE; REPRODUCTION; SIGNAL TRANSDUCTION;

EID: 77953363544     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000289568     Document Type: Review

References (137)

1. Nedergaard M, Ransom B, Goldman SA: New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 2003; 26: 523-530.
2. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA: Control of synapse number by glia. Science 2001; 291: 657-661.
3. Hatton GI, Tweedle CD: Magnocellular neuropeptidergic neurons in hypothalamus: increases in membrane apposition and number of specialized synapses from pregnancy to lactation. Brain Res Bull 1982; 8: 197-204.
4. Tweedle CD, Hatton GI: Ultrastructural changes in rat hypothalamic neurosecretory cells and their associated glia during minimal dehydration and rehydration. Cell Tissue Res 1977; 181: 59-72.
5. Theodosis DT, Poulain DA: Evidence for structural plasticity in the supraoptic nucleus of the rat hypothalamus in relation to gestation and lactation. Neuroscience 1984; 11: 183-193.
6. Theodosis DT, Poulain DA, Vincent JD: Possible morphological bases for synchronisation of neuronal firing in the rat supraoptic nucleus during lactation. Neuroscience 1981; 6: 919-929.
7. Hawrylak N, Boone D, Salm AK: The surface density of glial fibrillary acidic protein immunopositive astrocytic processes in the rat supraoptic nucleus is reversibly altered by dehydration and rehydration. Neurosci Lett 1999; 277: 57-60.
8. Haydon PG, Carmignoto G: Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 2006; 86: 1009-1031.
9. Theodosis DT, Poulain DA, Oliet SH: Activity- dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev 2008; 88: 983-1008.
10. Mong JA, Blutstein T: Estradiol modulation of astrocytic form and function: implications for hormonal control of synaptic communication. Neuroscience 2006; 138: 967-975.
11. Garcia-Segura LM, McCarthy MM: Minireview: role of glia in neuroendocrine function. Endocrinology 2004; 145: 1082-1086.
12. Csakvari E, Hoyk Z, Gyenes A, Garcia-Ovejero D, Garcia-Segura LM, Parducz A: Fluctuation of synapse density in the arcuate nucleus during the estrous cycle. Neuroscience 2007; 144: 1288-1292.
13. Matsumoto A, Arai Y: Neuronal plasticity in the deafferented hypothalamic arcuate nucleus of adult female rats and its enhancement by treatment with estrogen. J Comp Neurol 1981; 197: 197-205.
14. Schwarz JM, Liang SL, Thompson SM, Mc- Carthy MM: Estradiol induces hypothalamic dendritic spines by enhancing glutamate release: a mechanism for organizational sex differences. Neuron 2008; 58: 584-598.
15. Chneiweiss H, Glowinski J, Premont J: Modulation by monoamines of somatostatinsensitive adenylate cyclase on neuronal and glial cells from the mouse brain in primary cultures. J Neurochem 1985; 44: 1825-1831.
16. el-Etr M, Cordier J, Torrens Y, Glowinski J, Premont J: Pharmacological and functional heterogeneity of astrocytes: regional differences in phospholipase C stimulation by neuromediators. J Neurochem 1989; 52: 981-984.
17. Mothet JP, Pollegioni L, Ouanounou G, Martineau M, Fossier P, Baux G: Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D -serine. Proc Natl Acad Sci USA 2005; 102: 5606-5611.
18. Morga E, Faber C, Heuschling P: Regional heterogeneity of the astroglial immunoreactive phenotype: effect of lipopolysaccharide. J Neurosci Res 1999; 57: 941-952.
19. Hansson E: Co-existence between receptors, carriers, and second messengers on astrocytes grown in primary cultures. Neurochem Res 1989; 14: 811-819.
20. Porter JT, McCarthy KD: Astrocytic neurotransmitter receptors in situ and in vivo. Prog Neurobiol 1997; 51: 439-455.
21. Schwartz JP, Taniwaki T: Heterogeneity of expression of neuropeptide genes by astrocytes: functional implications. Perspect Dev Neurobiol 1994; 2: 251-257.
22. Chaban VV, Lakhter AJ, Micevych P: A Membrane Estrogen Receptor Mediates Intracellular Calcium Release in Astrocytes. Endocrinology 2004; 145: 3788-3795.
23. Langub MC Jr, Watson RE Jr: Estrogen receptor-immunoreactive glia, endothelia, and ependyma in guinea pig preoptic area and median eminence: electron microscopy. Endocrinology 1992; 130: 364-372.
24. Donahue JE, Stopa EG, Chorsky RL, King JC, Schipper HM, Tobet SA, Blaustein JD, Reichlin S: Cells containing immunoreactive estrogen receptor-alpha in the human basal forebrain. Brain Res 2000; 856: 142-151.
25. Kruijver FP, Balesar R, Espila AM, Unmehopa UA, Swaab DF: Estrogen receptor-alpha distribution in the human hypothalamus in relation to sex and endocrine status. J Comp Neurol 2002; 454: 115-139.
26. Hosli L, Hosli E: Receptors for dopamine and serotonin on astrocytes of cultured rat central nervous system. J Physiol (Paris) 1987; 82: 191-195.
27. Sharma G, Vijayaraghavan S: Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci USA 2001; 98: 4148-4153.
28. Verkhratsky A, Steinhauser C: Ion channels in glial cells. Brain Res Brain Res Rev 2000; 32: 380-412.
29. Caruso C, Durand D, Schioth HB, Rey R, Seilicovich A, Lasaga M: Activation of melanocortin 4 receptors reduces the inflammatory response and prevents apoptosis induced by lipopolysaccharide and interferon- gamma in astrocytes. Endocrinology 2007; 148: 4918-4926.
30. Garcia-Segura LM, Chowen JA, Naftolin F: Endocrine glia: roles of glial cells in the brain actions of steroid and thyroid hormones and in the regulation of hormone secretion. Front Neuroendocrinol 1996; 17: 180-211.
31. Dhandapani KM, Brann DW: Role of astrocytes in estrogen-mediated neuroprotection. Exp Gerontol 2007; 42: 70-75.
32. Micevych PE, Chaban V, Ogi J, Dewing P, Lu JK, Sinchak K: Estradiol stimulates progesterone synthesis in hypothalamic astrocyte cultures. Endocrinology 2007; 148: 782-789.
33. Hansson E, Ronnback L: Glial neuronal signaling in the central nervous system. Faseb J 2003; 17: 341-348.
34. Volterra A, Meldolesi J: Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 2005; 6: 626-640.
35. Chaban VV, Mayer EA, Ennes HS, Micevych PE: Estradiol inhibits ATP-induced intracellular calcium concentration increase in dorsal root ganglia neurons. Neuroscience 2003; 118: 941-948.
36. Micevych PE, Abelson L: Distribution of mRNAs coding for liver and heart gap junction proteins in the rat central nervous system. J Comp Neurol 1991; 305: 96-118.
37. Spray DC: Gap junctions in the nervous system; in Spray DC, Dermietzel R (eds): Gap Junctions in the Nervous System. Georgetown, Landes, 1996, pp 1-11.
38. Giaume C, McCarthy KD: Control of gapjunctional communication in astrocytic networks. Trends Neurosci 1996; 19: 319-325.
39. Newman EA: Propagation of intercellular calcium waves in retinal astrocytes and Muller cells. J Neurosci 2001; 21: 2215-2223.
40. Parpura V, Haydon PG: Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci USA 2000; 97: 8629-8634.
41. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG: Astrocytic purinergic signaling coordinates synaptic networks. Science 2005; 310: 113-116.
42. Santello M, Volterra A: Synaptic modulation by astrocytes via Ca 2+ -dependent glutamate release. Neuroscience 2009; 158: 253-259.
43. Micevych P, Kuo J, Christensen A: Physiology of membrane oestrogen receptor signalling in reproduction. J Neuroendocrinol 2009; 21: 249-256.
44. Mantyh PW, Johnson DJ, Boehmer CG, Catton MD, Vinters HV, Maggio JE, Too HP, Vigna SR: Substance P receptor binding sites are expressed by glia in vivo after neuronal injury. Proc Natl Acad Sci USA 1989; 86: 5193-5197.
45. Mong JA, McCarthy MM: Steroid-induced developmental plasticity in hypothalamic astrocytes: implications for synaptic patterning. J Neurobiol 1999; 40: 602-619.
46. Rozovsky I, Wei M, Stone DJ, Zanjani H, Anderson CP, Morgan TE, Finch CE: Estradiol (E2) enhances neurite outgrowth by repressing glial fibrillary acidic protein expression and reorganizing laminin. Endocrinology 2002; 143: 636-646.
47. Jennes L, Stumpf WE, Sheedy ME: Ultrastructural characterization of gonadotropin- releasing hormone (GnRH)-producing neurons. J Comp Neurol 1985; 232: 534-547.
48. Lehman MN, Karsch FJ, Robinson JE, Silverman AJ: Ultrastructure and synaptic organization of luteinizing hormone-releasing hormone (LHRH) neurons in the anestrous ewe. J Comp Neurol 1988; 273: 447-458.
49. Baroncini M, Allet C, Leroy D, Beauvillain JC, Francke JP, Prevot V: Morphological evidence for direct interaction between gonadotrophin- releasing hormone neurones and astroglial cells in the human hypothalamus. J Neuroendocrinol 2007; 19: 691-702.
50. Kozlowski GP, Coates PW: Ependymoneuronal specializations between LHRH fibers and cells of the cerebroventricular system. Cell Tissue Res 1985; 242: 301-311.
51. King JC, Letourneau RJ: Luteinizing hormone- releasing hormone terminals in the median eminence of rats undergo dramatic changes after gonadectomy, as revealed by electron microscopic image analysis. Endocrinology 1994; 134: 1340-1351.
52. Ojeda SR, Lomniczi A, Sandau US: Glial-gonadotrophin hormone (GnRH) neurone interactions in the median eminence and the control of GnRH secretion. J Neuroendocrinol 2008; 20: 732-742.
53. Rage F, Lee BJ, Ma YJ, Ojeda SR: Estradiol enhances prostaglandin E2 receptor gene expression in luteinizing hormone-releasing hormone (LHRH) neurons and facilitates the LHRH response to PGE2 by activating a glia-to-neuron signaling pathway. J Neurosci 1997; 17: 9145-9156.
54. Ma YJ, Berg-von der Emde K, Rage F, Wetsel WC, Ojeda SR: Hypothalamic astrocytes respond to transforming growth factor-alpha with the secretion of neuroactive substances that stimulate the release of luteinizing hormone- releasing hormone. Endocrinology 1997; 138: 19-25.
55. Sinchak K, Mills RH, Tao L, LaPolt P, Lu JK, Micevych P: Estrogen induces de novo progesterone synthesis in astrocytes. Dev Neurosci 2003; 25: 343-348.
56. Mahesh VB, Dhandapani KM, Brann DW: Role of astrocytes in reproduction and neuroprotection. Mol Cell Endocrinol 2006; 246: 1-9.
57. Chappell PE, Levine JE: Stimulation of gonadotropin- releasing hormone surges by estrogen. I. Role of hypothalamic progesterone receptors. Endocrinology 2000; 141: 1477-1485.
58. MacLusky NJ, McEwen BS: Oestrogen modulates progestin receptor concentrations in some rat brain regions but not in others. Nature 1978; 274: 276-278.
59. Soma KK, Sinchak K, Lakhter A, Schlinger BA, Micevych PE: Neurosteroids and female reproduction: estrogen increases 3beta-HSD mRNA and activity in rat hypothalamus. Endocrinology 2005; 146: 4386-4390.
60. Wintermantel TM, Campbell RE, Porteous R, Bock D, Grone HJ, Todman MG, Korach KS, Greiner E, Perez CA, Schutz G, Herbison AE: Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin- releasing hormone neurons and fertility. Neuron 2006; 52: 271-280.
61. Micevych P, Sinchak K, Mills RH, Tao L, LaPolt P, Lu JK: The luteinizing hormone surge is preceded by an estrogen-induced increase of hypothalamic progesterone in ovariectomized and adrenalectomized rats. Neuroendocrinology 2003; 78: 29-35.
62. Couse JF, Korach KS: Contrasting phenotypes in reproductive tissues of female estrogen receptor null mice. Ann NY Acad Sci 2001; 948: 1-8.
63. Scorticati C, Fernandez-Solari J, De Laurentiis A, Mohn C, Prestifilippo JP, Lasaga M, Seilicovich A, Billi S, Franchi A, McCann SM, Rettori V: The inhibitory effect of anandamide on luteinizing hormone-releasing hormone secretion is reversed by estrogen. Proc Natl Acad Sci USA 2004; 101: 11891-11896.
64. Herbison AE: Physiology of the GnRH neuronal network; in Neill JD (ed): Knobil and Neill's Physiology of Reproduction, 3rd ed. San Diego, Academic Press, 2006, pp 1415- 1482.
65. 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: 8691-8697.
66. Herbison AE: Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 2008; 57: 277-287.
67. Oakley AE, Clifton DK, Steiner RA: Kisspeptin signaling in the brain. Endocr Rev 2009; 30: 713-743.
68. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A: Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006; 401: 225-230.
69. Richard N, Galmiche G, Corvaisier S, Caraty A, Kottler ML: KiSS-1 and GPR54 genes are co-expressed in rat gonadotrophs and differentially regulated in vivo by oestradiol and gonadotrophin-releasing hormone. J Neuroendocrinol 2008; 20: 381-393.
70. Mann DR, Korowitz CD, Barraclough CA: Adrenal gland involvement in synchronizing the preovulatory release of LH in rats. Proc Soc Exp Biol Med 1975; 150: 115-120.
71. Hibbert ML, Stouffer RL, Wolf DP, Zelinski- Wooten MB: Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc Natl Acad Sci USA 1996; 93: 1897-1901.
72. Remohi J, Balmaceda JP, Rojas FJ, Asch RH: The role of pre-ovulatory progesterone in the midcycle gonadotrophin surge, ovulation and subsequent luteal phase: studies with RU486 in rhesus monkeys. Hum Reprod 1988; 3: 431-435.
73. DePaolo LV: Attenuation of preovulatory gonadotrophin surges by epostane: a new inhibitor of 3beta-hydroxysteroid dehydrogenase. J Endocrinol 1988; 118: 59-68.
74. DePaolo LV, Barraclough CA: Dose dependent effects of progesterone on the facili tation and inhibition of spontaneous go nadotropin surges in estrogen treated ovariectomized rats. Biol Reprod 1979; 21: 1015-1023.
75. Micevych PE, Mermelstein PG: Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in brain. Mol Neurobiol 2008; 38: 66-77.
76. Schumacher M, Robert F: Progesterone synthesis, metabolism, mechanisms of action, and effects in the nervous system; in Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds): Hormones, Brain and Behavior. Amsterdam, Academic Press, 2002, pp 683-745.
77. Zwain IH, Yen SS: Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 1999; 140: 3843-3852.
78. Micevych P, Sinchak K: Estradiol regulation of progesterone synthesis in the brain. Mol Cell Endocrinol 2008; 290: 44-50.
79. Mermelstein PG, Micevych PE: Nervous system physiology regulated by membrane estrogen receptors. Rev Neurosci 2008; 19: 413-424.
80. Micevych P, Sinchak K: Synthesis and function of hypothalamic neuroprogesterone in reproduction. Endocrinology 2008; 149: 2739-2742.
81. Clarkson J, Herbison AE: Oestrogen, kisspeptin, GPR54 and the pre-ovulatory luteinising hormone surge. J Neuroendocrinol 2009; 21: 305-311.
82. Aparicio SA: Kisspeptins and GPR54 - the new biology of the mammalian GnRH axis. Cell Metab 2005; 1: 293-296.
83. Micevych P, Soma KK, Sinchak K: Neuroprogesterone: key to estrogen positive feedback? Brain Res Rev 2008; 57: 470-480.
84. Micevych P, Dominguez R: Membrane estradiol signaling in the brain. Front Neuroendocrinol 2009; 30: 315-327.
85. Razandi M, Pedram A, Greene GL, Levin ER: Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol Endocrinol 1999; 13: 307-319.
86. Dominguez R, Micevych P: Estradiol rapidly regulates membrane ER- levels in hypothalamic neurons. J Neurosci. In review.
87. Bondar G, Kuo J, Hamid N, Micevych P: Estradiol-induced estrogen receptor-alpha trafficking. J Neurosci 2009; 29: 15323-15330.
88. Deecher DC, Swiggard P, Frail DE, O'Connor LT: Characterization of a membrane-associated estrogen receptor in a rat hypothalamic cell line (D12). Endocrine 2003; 22: 211-223.
89. Boulware MI, Kordasiewicz H, Mermelstein PG: Caveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons. J Neurosci 2007; 27: 9941-9950.
90. Grove-Strawser D, Mermelstein PG: Estrogen receptors activate different mGluRs across distinct brain regions. Soc Neuroscience Ann Meet, San Diego, 2007.
91. Pedram A, Razandi M, Sainson RC, Kim JK, Hughes CC, Levin ER: A conserved mechanism for steroid receptor translocation to the plasma membrane. J Biol Chem 2007; 282: 22278-22288.
92. Acconcia F, Ascenzi P, Bocedi A, Spisni E, Tomasi V, Trentalance A, Visca P, Marino M: Palmitoylation-dependent estrogen receptor alpha membrane localization: regulation by 17beta-estradiol. Mol Biol Cell 2005; 16: 231-237.
93. Razandi M, Alton G, Pedram A, Ghonshani S, Webb P, Levin ER: Identification of a structural determinant necessary for the localization and function of estrogen receptor alpha at the plasma membrane. Mol Cell Biol 2003; 23: 1633-1646.
94. Gu G, Rojo AA, Zee MC, Yu J, Simerly RB: Hormonal regulation of CREB phosphorylation in the anteroventral periventricular nucleus. J Neurosci 1996; 16: 3035-3044.
95. Zhou Y, Watters JJ, Dorsa DM: Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain. Endocrinology 1996; 137: 2163-2166.
96. Carlstrom L, Ke ZJ, Unnerstall JR, Cohen RS, Pandey SC: Estrogen modulation of the cyclic AMP response element-binding protein pathway: effects of long-term and acute treatments. Neuroendocrinology 2001; 74: 227-243.
97. Kelly MJ, Ronnekleiv OK: Membrane-initiated estrogen signaling in hypothalamic neurons. Mol Cell Endocrinol 2008; 290: 14-23.
98. Boulware MI, Weick JP, Becklund BR, Kuo SP, Groth RD, Mermelstein PG: Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response elementbinding protein. J Neurosci 2005; 25: 5066-5078.
99. Dewing P, Boulware MI, Sinchack K, Christensen A, Mermelstein PG, Micevych P: Membrane ER- interacts with mGluR1a to modulate female sexual receptivity. J Neurosci 2007; 27: 9294-9300.
100. Kuo J, Hariri OR, Bondar G, Ogi J, Micevych P: Membrane estrogen receptor-alpha interacts with metabotropic glutamate receptor type 1a to mobilize intracellular calcium in hypothalamic astrocytes. Endocrinology 2009; 150: 1369-1376.
101. Kahlert S, Nuedling S, van Eickels M, Vetter H, Meyer R, Grohe C: Estrogen receptor alpha rapidly activates the IGF-1 receptor pathway. J Biol Chem 2000; 275: 18447-18453.
102. Etgen AM, Ansonoff MA, Quesada A: Mechanisms of ovarian steroid regulation of norepinephrine receptor-mediated signal transduction in the hypothalamus: implications for female reproductive physiology. Horm Behav 2001; 40: 169-177.
103. Quesada A, Micevych PE: Estrogen interacts with the IGF-1 system to protect nigrostriatal dopamine and maintain motoric behavior after 6-hydroxdopamine lesions. J Neurosci Res 2004; 75: 107-116.
104. Stefanova I, Horejsi V, Ansotegui IJ, Knapp W, Stockinger H: GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science 1991; 254: 1016-1019.
105. Dewing P, Christensen A, Bondar G, Micevych P: Protein kinase C signaling in the hypothalamic arcuate nucleus regulates sexual receptivity in female rats. Endocrinology 2008; 149: 5934-5942.
106. Mermelstein PG, Becker JB, Surmeier DJ: Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. J Neurosci 1996; 16: 595-604.
107. Chaban V, Li J, McDonald J, Rapkin A, Micevych P: Estradiol attenuates ATP-induced increase of intracellular calcium through group II metabotropic glutamate receptors in rat DRG neurons. J Neurosci Res. In review.
108. Kuo J, Ham id N, Bondar G, Prossnitz ER, Micevych P: Membrane estrogen receptors stimulate intracellular calcium flux and progesterone synthesis in hypothalamic astrocytes. J Neurosci. In review.
109. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff DW: Roles of estrogen receptor- alpha gene expression in reproduction- related behaviors in female mice. Endocrinology 1998; 139: 5070-5081.
110. Rissman EF, Wersinger SR, Taylor JA, Lubahn DB: Estrogen receptor function as revealed by knockout studies: neuroendocrine and behavioral aspects. Horm Behav 1997; 31: 232-243.
111. 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: 5616-5627.
112. Chaban VV, Micevych PE: Estrogen receptor- alpha mediates estradiol attenuation of ATP-induced Ca 2+ signaling in mouse dorsal root ganglion neurons. J Neurosci Res 2005; 81: 31-37.
113. Ramirez VD, Kipp JL, Joe I: Estradiol, in the CNS, targets several physiologically relevant membrane-associated proteins. Brain Res Brain Res Rev 2001; 37: 141-152.
114. Dominguez R, Hu E, Zhou M, Baudry M: 17Beta-estradiol-mediated neuroprotection and ERK activation require a pertussis toxin- sensitive mechanism involving GRK2 and beta-arrestin-1. J Neurosci 2009; 29: 4228-4238.
115. Razandi M, Pedram A, Levin ER: Estrogen signals to the preservation of endothelial cell form and function. J Biol Chem 2000; 275: 38540-38546.
116. Russell KS, Haynes MP, Sinha D, Clerisme E, Bender JR: Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci USA 2000; 97: 5930-5935.
117. Kow LM, Pfaff DW: The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions. Proc Natl Acad Sci USA 2004; 101: 12354-12357.
118. Morales A, Diaz M, Ropero AB, Nadal A, Alonso R: Estradiol modulates acetylcholine- induced Ca 2+ signals in LHRH-releasing GT1-7 cells through a membrane binding site. Eur J Neurosci 2003; 18: 2505-2514.
119. Lin JW, Ju W, Foster K, Lee SH, Ahmadian G, Wyszynski M, Wang YT, Sheng M: Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 2000; 3: 1282-1290.
120. Gorosito SV, Lorenzo AG, Cambiasso MJ: Estrogen receptor alpha is expressed on the cell-surface of embryonic hypothalamic neurons. Neuroscience 2008; 154: 1173-1177.
121. Friend KE, Ang LW, Shupnik MA: Estrogen regulates the expression of several different estrogen receptor mRNA isoforms in rat pituitary. Proc Natl Acad Sci USA 1995; 92: 4367-4371.
122. Bollig A, Miksicek RJ: An estrogen receptor- alpha splicing variant mediates both positive and negative effects on gene transcription. Mol Endocrinol 2000; 14: 634-649.
123. Poola I, Abraham J, Baldwin K: Identification of ten exon deleted ERbeta mRNAs in human ovary, breast, uterus and bone tissues: alternate splicing pattern of estrogen receptor beta mRNA is distinct from that of estrogen receptor alpha. FEBS Lett 2002; 516: 133-138.
124. Moriarty K, Kim KH, Bender JR: Minireview: estrogen receptor-mediated rapid signaling. Endocrinology 2006; 147: 5557-5563.
125. Al-Bader MD, El-Abdallah AA, Redzic ZB: Ontogenic profile of estrogen receptor alpha and beta mRNA and protein expression in fetal rat brain. Neurosci Lett 2008; 440: 222-226.
126. Ishunina TA, Swaab DF: Estrogen receptoralpha splice variants in the human brain. Gynecol Endocrinol 2008; 24: 93-98.
127. Ishunina TA, Swaab DF: Age-dependent ERalpha MB1 splice variant expression in discrete areas of the human brain. Neurobiol Aging 2008; 29: 1177-1189.
128. Karas RH, Baur WE, van Eickles M, Mendelsohn ME: Human vascular smooth muscle cells express an estrogen receptor isoform. FEBS Lett 1995; 377: 103-108.
129. Fasco MJ, Keyomarsi K, Arcaro KF, Gierthy JF: Expression of an estrogen receptor alpha variant protein in cell lines and tumors. Mol Cell Endocrinol 2000; 166: 156-169.
130. Shupnik MA, Pitt LK, Soh AY, Anderson A, Lopes MB, Laws ER Jr: Selective expression of estrogen receptor alpha and beta isoforms in human pituitary tumors. J Clin Endocrinol Metab 1998; 83: 3965-3972.
131. Fuqua SA, Fitzgerald SD, Allred DC, Elledge RM, Nawaz Z, McDonnell DP, O'Malley BW, Greene GL, McGuire WL: Inhibition of estrogen receptor action by a naturally occurring variant in human breast tumors. Cancer Res 1992; 52: 483-486.
132. Perlman WR, Matsumoto M, Beltaifa S, Hyde TM, Saunders RC, Webster MJ, Rubinow DR, Kleinman JE, Weickert CS: Expression of estrogen receptor alpha exondeleted mRNA variants in the human and non-human primate frontal cortex. Neuroscience 2005; 134: 81-95.
133. Heberden C, Reine F, Grosse B, Henry C, Zagar Y, Chaumaz G, Lieberherr M: Detection of a raft-located estrogen receptor-like protein distinct from ER alpha. Int J Biochem Cell Biol 2006; 38: 376-391.
134. Matsuda K, Sakamoto H, Mori H, Hosokawa K, Kawamura A, Itose M, Nishi M, Prossnitz ER, Kawata M: Expression and intracellular distribution of the G proteincoupled receptor 30 in rat hippocampal formation. Neurosci Lett 2008; 441: 94-99.
135. Otto C, Rohde-Schulz B, Schwarz G, Fuchs I, Klewer M, Brittain D, Langer G, Bader B, Prelle K, Nubbemeyer R, Fritzemeier KH: GPR30 localizes to the endoplasmic reticulum and is not activated by estradiol. Endocrinology 2008; 149: 4846-4856.
136. Sinchak K, Micevych P: Visualizing activation of opioid circuits by internalization of G protein-coupled receptors. Mol Neurobiol 2003; 27: 197-222.
137. Gonzalez M, Reyes R, Damas C, Alonso R, Bello AR: Oestrogen receptor alpha and beta in female rat pituitary cells: an immunochemical study. Gen Comp Endocrinol 2008; 155: 857-868.