Insights into rapid modulation of neuroplasticity by brain estrogens

Pharmacological Reviews

Volumn 65, Issue 4, 2013, Pages 1318-1350

  Srivastava, Deepak P ^a,b   Woolfrey, Kevin M ^b,c,d   Penzes, Peter ^b,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; AROMATASE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLUTAMATE RECEPTOR; METABOTROPIC RECEPTOR; SCAFFOLD PROTEIN;

ASTROCYTE; BIOAVAILABILITY; BIOSYNTHESIS; BRAIN CELL; CELL STRUCTURE; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; COGNITION; DENDRITIC SPINE; DEVELOPMENTAL STAGE; ENZYME LOCALIZATION; HIPPOCAMPUS; HUMAN; INTRACELLULAR SIGNALING; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; SECOND MESSENGER; TAENIOPYGIA GUTTATA; WORKING MEMORY;

EID: 84888155058     PISSN: 00316997     EISSN: 15210081     Source Type: Journal    
DOI: 10.1124/pr.111.005272     Document Type: Review

References (329)

1. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA, McEwen BS, and Morrison JH (2002) Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci 22:3608-3614.
2. Akama KT and McEwen BS (2003) Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J Neurosci 23:2333-2339.
3. Akama KT, Thompson LI, Milner TA, and McEwen BS (2013) Post-synaptic density-95 (PSD-95) binding capacity of G-protein-coupled receptor 30 (GPR30), an estrogen receptor that can be identified in hippocampal dendritic spines. J Biol Chem 288:6438-6450.
4. Alvarez VA and Sabatini BL (2007) Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci 30:79-97.
5. Amateau SK and McCarthy MM (2002) A novel mechanism of dendritic spine plasticity involving estradiol induction of prostaglandin-E2. J Neurosci 22: 8586-8596.
6. Ashby MC and Isaac JT (2011) Maturation of a recurrent excitatory neocortical circuit by experience-dependent unsilencing of newly formed dendritic spines. Neuron 70:510-521.
7. Aubele T, Kaufman R, Montalmant F, and Kritzer MF (2008) Effects of gonadectomy and hormone replacement on a spontaneous novel object recognition task in adult male rats. Horm Behav 54:244-252.
8. Azcoitia I, Santos-Galindo M, Arevalo MA, and Garcia-Segura LM (2010) Role of astroglia in the neuroplastic and neuroprotective actions of estradiol. Eur J Neurosci 32:1995-2002.
9. Azcoitia I, Yague JG, and Garcia-Segura LM (2011) Estradiol synthesis within the human brain. Neuroscience 191:139-147.
10. Balthazart J, Baillien M, and Ball GF (2001) Rapid and reversible inhibition of brain aromatase activity. J Neuroendocrinol 13:63-73.
11. Balthazart J, Baillien M, and Ball GF (2006) Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 147:359-366.
12. Balthazart J and Ball GF (2006) Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29:241-249.
13. Barker GR and Warburton EC (2011) When is the hippocampus involved in recognition memory? J Neurosci 31:10721-10731.
14. Baulieu EE and Robel P (1990) Neurosteroids: a new brain function? J Steroid Biochem Mol Biol 37:395-403.
15. Beato M (1989) Gene regulation by steroid hormones. Cell 56:335-344.
16. Belelli D and Lambert JJ (2005) Neurosteroids: endogenous regulators of the GABA (A) receptor. Nat Rev Neurosci 6:565-575.
17. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407-412.
18. Beyer C, Pawlak J, and Karolczak M (2003) Membrane receptors for oestrogen in the brain. J Neurochem 87:545-550.
19. Bhatt DH, Zhang S, and Gan WB (2009) Dendritic spine dynamics. Annu Rev Physiol 71:261-282.
20. Bi R, Foy MR, Vouimba RM, Thompson RF, and Baudry M (2001) Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc Natl Acad Sci USA 98:13391-13395.
21. Bimonte HA and Denenberg VH (1999) Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 24:161-173.
22. Blaustein JD (2008) An estrogen by any other name. Endocrinology 149:2697-2698.
23. Bonhoeffer T and Yuste R (2002) Spine motility. Phenomenology, mechanisms, and function. Neuron 35:1019-1027.
24. Boon WC, Chow JD, and Simpson ER (2010) The multiple roles of estrogens and the enzyme aromatase. Prog Brain Res 181:209-232.
25. Boonyaratanakornkit V (2011) Scaffolding proteins mediating membrane-initiated extra-nuclear actions of estrogen receptor. Steroids 76:877-884.
26. Boulware MI, Weick JP, Becklund BR, Kuo SP, Groth RD, and Mermelstein PG (2005) Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J Neurosci 25:5066-5078.
27. Bourne JN and Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47-67.
28. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, Oprea TI, Prossnitz ER, and Dun NJ (2007) Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol 193:311-321.
29. Brinton RD (2009) Estrogen-induced plasticity from cells to circuits: predictions for cognitive function. Trends Pharmacol Sci 30:212-222.
30. Brinton RD (2013) Neurosteroids as regenerative agents in the brain: therapeutic implications. Nat Rev Endocrinol 9:241-250.
31. Bueno J and Pfaff DW (1976) Single unit recording in hypothalamus and preoptic area of estrogen-treated and untreated ovariectomized female rats. Brain Res 101:67-78.
32. Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7:477-484.
33. Callard GV, Petro Z, and Ryan KJ (1978) Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology 103:2283-2290.
34. Castets F, Bartoli M, Barnier JV, Baillat G, Salin P, Moqrich A, Bourgeois JP, Denizot F, Rougon G, and Calothy G, et al. (1996) A novel calmodulin-binding protein, belonging to the WD-repeat family, is localized in dendrites of a subset of CNS neurons. J Cell Biol 134:1051-1062.
35. Castrén E and Hen R (2013) Neuronal plasticity and antidepressant actions. Trends Neurosci 36:259-267.
36. Chan C, Beltzner CC, and Pollard TD (2009) Cofilin dissociates Arp2/3 complex and branches from actin filaments. Curr Biol 19:537-545.
37. Charlier TD, Harada N, Balthazart J, and Cornil CA (2011) Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions. Endocrinology 152:4199-4210.
38. Chen JR, Yan YT, Wang TJ, Chen LJ, Wang YJ, and Tseng GF (2009) Gonadal hormones modulate the dendritic spine densities of primary cortical pyramidal neurons in adult female rat. Cereb Cortex 19:2719-2727.
39. Chklovskii DB, Mel BW, and Svoboda K (2004) Cortical rewiring and information storage. Nature 431:782-788.
40. Choleris E, Clipperton-Allen AE, Phan A, Valsecchi P, and Kavaliers M (2012) Estrogenic involvement in social learning, social recognition and pathogen avoidance. Front Neuroendocrinol 33:140-159.
41. Christopoulos A and Kenakin T (2002) G protein-coupled receptor allosterism and complexing. Pharmacol Rev 54:323-374.
42. Chung WC, Pak TR, Suzuki S, Pouliot WA, Andersen ME, and Handa RJ (2007) Detection and localization of an estrogen receptor beta splice variant protein (ERbeta2) in the adult female rat forebrain and midbrain regions. J Comp Neurol 505:249-267.
43. Cohen S and Greenberg ME (2008) Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu Rev Cell Dev Biol 24:183-209.
44. Cooke SF and Bliss TV (2006) Plasticity in the human central nervous system. Brain 129:1659-1673.
45. Cornil CA, Ball GF, and Balthazart J (2006) Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res 1126:2-26.
46. Cornil CA, Dalla C, Papadopoulou-Daifoti Z, Baillien M, Dejace C, Ball GF, and Balthazart J (2005) Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior. Endocrinology 146:3809-3820.
47. Craig MC, Maki PM, and Murphy DG (2005) The Women's Health Initiative Memory Study: findings and implications for treatment. Lancet Neurol 4:190-194.
48. Cyr M, Calon F, Morissette M, Grandbois M, Di Paolo T, and Callier S (2000) Drugs with estrogen-like potency and brain activity: potential therapeutic application for the CNS. Curr Pharm Des 6:1287-1312.
49. Daniel JM, Fader AJ, Spencer AL, and Dohanich GP (1997) Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 32:217-225.
50. Day JJ and Sweatt JD (2010) DNA methylation and memory formation. Nat Neurosci 13:1319-1323.
51. Day JJ and Sweatt JD (2011) Epigenetic mechanisms in cognition. Neuron 70: 813-829.
52. De Bello WM (2008) Micro-rewiring as a substrate for learning. Trends Neurosci 31: 577-584.
53. Do Rego JL, Seong JY, Burel D, Leprince J, Luu-The V, Tsutsui K, Tonon MC, Pelletier G, and Vaudry H (2009) Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front Neuroendocrinol 30:259-301.
54. Dominguez R and Micevych P (2010) Estradiol rapidly regulates membrane estrogen receptor alpha levels in hypothalamic neurons. J Neurosci 30:12589-12596.
55. DSM-IV (2000) Diagnostic and Statistical Manual of Mental Disorders, American Psychiatric Society, Washington, DC.
56. Dumitriu D, Rapp PR, McEwen BS, and Morrison JH (2010) Estrogen and the aging brain: an elixir for the weary cortical network. Ann N Y Acad Sci 1204:104-112.
57. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, and Mark M (2000) Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127:4277-4291.
58. Edwards DC, Sanders LC, Bokoch GM, and Gill GN (1999) Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1:253-259.
59. Egile C, Loisel TP, Laurent V, Li R, Pantaloni D, Sansonetti PJ, and Carlier MF (1999) Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. J Cell Biol 146:1319-1332.
60. Ehlers MD, Heine M, Groc L, Lee MC, and Choquet D (2007) Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54:447-460.
61. Emes RD, Pocklington AJ, Anderson CN, Bayes A, Collins MO, Vickers CA, Croning MD, Malik BR, Choudhary JS, and Armstrong JD, et al. (2008) Evolutionary expansion and anatomical specialization of synapse proteome complexity. Nat Neurosci 11:799-806.
62. Ennaceur A, Neave N, and Aggleton JP (1997) Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113: 509-519.
63. Espeland MA, Rapp SR, Shumaker SA, Brunner R, Manson JE, Sherwin BB, Hsia J, Margolis KL, Hogan PE, and Wallace R, et al.; Women's Health Initiative Memory Study (2004) Conjugated equine estrogens and global cognitive function in postmenopausal women:Women's Health Initiative Memory Study. JAMA 291:2959-2968.
64. Euston DR, Gruber AJ, and McNaughton BL (2012) The role of medial prefrontal cortex in memory and decision making. Neuron 76:1057-1070.
65. Evans PD, Robb S, Cheek TR, Reale V, Hannan FL, Swales LS, Hall LM, and Midgley JM (1995) Agonist-specific coupling of G-protein-coupled receptors to second-messenger systems. Prog Brain Res 106:259-268.
66. Evans PD, Srivastava DP, and Reale V (2009) Rapid, non-genomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein-coupled receptor. Ecdysone: Structures and Functions, p. 425-443.
67. Fan L, Zhao Z, Orr PT, Chambers CH, Lewis MC, and Frick KM (2010) Estradiolinduced object memory consolidation in middle-aged female mice requires dorsal hippocampal extracellular signal-regulated kinase and phosphatidylinositol 3-kinase activation. J Neurosci 30:4390-4400.
68. Fan X, Warner M, and Gustafsson JA (2006) Estrogen receptor beta expression in the embryonic brain regulates development of calretinin-immunoreactive GABAergic interneurons. Proc Natl Acad Sci USA 103:19338-19343.
69. Fernandez SM, Lewis MC, Pechenino AS, Harburger LL, Orr PT, Gresack JE, Schafe GE, and Frick KM (2008) Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J Neurosci 28:8660-8667.
70. Filardo EJ and Thomas P (2012) Minireview: G protein-coupled estrogen receptor-1, GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology. Endocrinology 153:2953-2962.
71. Fischer M, Kaech S, Knutti D, and Matus A (1998) Rapid actin-based plasticity in dendritic spines. Neuron 20:847-854.
72. Fisher CR, Graves KH, Parlow AF, and Simpson ER (1998) Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci USA 95:6965-6970.
73. Fortress AM, Fan L, Orr PT, Zhao Z, and Frick KM (2013) Estradiol-induced object recognition memory consolidation is dependent on activation of mTOR signaling in the dorsal hippocampus. Learn Mem 20:147-155.
74. Foy MR, Xu J, Xie X, Brinton RD, Thompson RF, and Berger TW (1999) 17betaestradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol 81:925-929.
75. Frick KM (2009) Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here? Horm Behav 55:2-23.
76. Frick KM, Zhao Z, and Fan L (2011) The epigenetics of estrogen: epigenetic regulation of hormone-induced memory enhancement. Epigenetics 6:675-680.
77. Frost NA, Shroff H, Kong H, Betzig E, and Blanpied TA (2010) Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron 67:86-99.
78. Frye CA, Rhodes ME, and Dudek B (2005) Estradiol to aged female or male mice improves learning in inhibitory avoidance and water maze tasks. Brain Res 1036: 101-108.
79. Fu M and Zuo Y (2011) Experience-dependent structural plasticity in the cortex. Trends Neurosci 34:177-187.
80. Furukawa A, Miyatake A, Ohnishi T, and Ichikawa Y (1998) Steroidogenic acute regulatory protein (StAR) transcripts constitutively expressed in the adult rat central nervous system: colocalization of StAR, cytochrome P-450SCC (CYP XIA1), and 3beta-hydroxysteroid dehydrogenase in the rat brain. J Neurochem 71: 2231-2238.
81. Gaillard S, Bailly Y, Benoist M, Rakitina T, Kessler JP, Fronzaroli-Molinières L, Dargent B, and Castets F (2006) Targeting of proteins of the striatin family to dendritic spines: role of the coiled-coil domain. Traffic 7:74-84.
82. Galea LA, Uban KA, Epp JR, Brummelte S, Barha CK, Wilson WL, Lieblich SE, and Pawluski JL (2008) Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can J Expl Psych 62:247-260.
83. Garcia-Segura LM (2008) Aromatase in the brain: not just for reproduction anymore. J Neuroendocrinol 20:705-712.
84. Gibbs RB (2007) Estradiol enhances DMP acquisition via a mechanism not mediated by turning strategy but which requires intact basal forebrain cholinergic projections. Horm Behav 52:352-359.
85. Gibbs RB and Johnson DA (2008) Sex-specific effects of gonadectomy and hormone treatment on acquisition of a 12-arm radial maze task by Sprague Dawley rats. Endocrinology 149:3176-3183.
86. Gillies GE and McArthur S (2010) Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol Rev 62:155-198.
87. Gobeil F, Fortier A, Zhu T, Bossolasco M, Leduc M, Grandbois M, Heveker N, Bkaily G, Chemtob S, and Barbaz D (2006) G-protein-coupled receptors signalling at the cell nucleus: an emerging paradigm. Can J Physiol Pharmacol 84:287-297.
88. Goley ED and Welch MD (2006) The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7:713-726.
89. González M, Cabrera-Socorro A, Pérez-García CG, Fraser JD, López FJ, Alonso R, and Meyer G (2007) Distribution patterns of estrogen receptor alpha and beta in the human cortex and hippocampus during development and adulthood. J Comp Neurol 503:790-802.
90. Gould E, Woolley CS, Frankfurt M, and McEwen BS (1990) Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10:1286-1291.
91. Gray JA and Roth BL (2007) Molecular targets for treating cognitive dysfunction in schizophrenia. Schizophr Bull 33:1100-1119.
92. Gresack JE and Frick KM (2006) Post-training estrogen enhances spatial and object memory consolidation in female mice. Pharmacol Biochem Behav 84:112-119.
93. Grove-Strawser D, Boulware MI, and Mermelstein PG (2010) Membrane estrogen receptors activate the metabotropic glutamate receptors mGluR5 and mGluR3 to bidirectionally regulate CREB phosphorylation in female rat striatal neurons. Neuroscience 170:1045-1055.
94. Gu J, Lee CW, Fan Y, Komlos D, Tang X, Sun C, Yu K, Hartzell HC, Chen G, and Bamburg JR, et al. (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci 13:1208-1215.
95. Hajszan T, Szigeti-Buck K, Sallam NL, Bober J, Parducz A, Maclusky NJ, Leranth C, and Duman RS (2010) Effects of estradiol on learned helplessness and associated remodeling of hippocampal spine synapses in female rats. Biol Psychiatry 67: 168-174.
96. Hammond R, Nelson D, and Gibbs RB (2011) GPR30 co-localizes with cholinergic neurons in the basal forebrain and enhances potassium-stimulated acetylcholine release in the hippocampus. Psychoneuroendocrinology 36:182-192.
97. Handa RJ, Ogawa S, Wang JM, and Herbison AE (2012) Roles for oestrogen receptor b in adult brain function. J Neuroendocrinol 24:160-173.
98. Hao J, Rapp PR, Janssen WG, Lou W, Lasley BL, Hof PR, and Morrison JH (2007) Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc Natl Acad Sci USA 104:11465-11470.
99. Hazell GG, Yao ST, Roper JA, Prossnitz ER, O'Carroll AM, and Lolait SJ (2009) Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues. J Endocrinol 202: 223-236.
100. Henderson VW (2009) Estrogens, episodic memory, and Alzheimer's disease: a critical update. Semin Reprod Med 27:283-293.
101. Herrick SP, Waters EM, Drake CT, McEwen BS, and Milner TA (2006) Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus. Brain Res 1121:46-58.
102. Hobkirk R (1985) Steroid sulfotransferases and steroid sulfate sulfatases: characteristics and biological roles. Can J Biochem Cell Biol 63:1127-1144.
103. Hojo Y, Higo S, Ishii H, Ooishi Y, Mukai H, Murakami G, Kominami T, Kimoto T, Honma S, and Poirier D, et al. (2009) Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinology 150: 5106-5112.
104. Holtmaat A and Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647-658.
105. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, and Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279-291.
106. Honda S, Harada N, Ito S, Takagi Y, and Maeda S (1998) Disruption of sexual behavior in male aromatase-deficient mice lacking exons 1 and 2 of the cyp19 gene. Biochem Biophys Res Commun 252:445-449.
107. Hotulainen P and Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189:619-629.
108. Hotulainen P, Llano O, Smirnov S, Tanhuanpää K, Faix J, Rivera C, and Lappalainen P (2009) Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J Cell Biol 185:323-339.
109. Huang GZ and Woolley CS (2012) Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism. Neuron 74:801-808.
110. Hughes ZA, Liu F, Marquis K, Muniz L, Pangalos MN, Ring RH, Whiteside GT, and Brandon NJ (2009) Estrogen receptor neurobiology and its potential for translation into broad spectrum therapeutics for CNS disorders. Curr Mol Pharmacol 2:215-236.
111. Inagaki T, Gautreaux C, and Luine V (2010) Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm Behav 58:415-426.
112. Insel TR (2010) Rethinking schizophrenia. Nature 468:187-193.
113. Isaac JT, Nicoll RA, and Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
114. Ishii H, Shoda Y, Yomogida K, Hamada T, and Sakuma Y (2011) Identification of C-terminally and N-terminally truncated estrogen receptor a variants in the mouse. J Steroid Biochem Mol Biol 124:38-46.
115. Ishii H, Tsurugizawa T, Ogiue-Ikeda M, Asashima M, Mukai H, Murakami G, Hojo Y, Kimoto T, and Kawato S (2007) Local production of sex hormones and their modulation of hippocampal synaptic plasticity. Neuroscientist 13:323-334.
116. Ishunina TA and Swaab DF (2008) Estrogen receptor-alpha splice variants in the human brain. Gynecol Endocrinol 24:93-98.
117. Jones KA, Srivastava DP, Allen JA, Strachan RT, Roth BL, and Penzes P (2009) Rapid modulation of spine morphology by the 5-HT2A serotonin receptor through kalirin-7 signaling. Proc Natl Acad Sci USA 106:19575-19580.
118. Jordan BA and Kreutz MR (2009) Nucleocytoplasmic protein shuttling: the direct route in synapse-to-nucleus signaling. Trends Neurosci 32:392-401.
119. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, and Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33: 121-129.
120. Kelly MJ, Moss RL, and Dudley CA (1976) Differential sensitivity of preoptic-septal neurons to microelectrophoresed estrogen during the estrous cycle. Brain Res 114: 152-157.
121. Kelly MJ, Qiu J, and Rønnekleiv OK (2005) Estrogen signaling in the hypothalamus. Vitam Horm 71:123-145.
122. Kennedy MJ, Davison IG, Robinson CG, and Ehlers MD (2010) Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 141:524-535.
123. Kerchner GA and Nicoll RA (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9:813-825.
124. Kessels HW and Malinow R (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61:340-350.
125. Khan MM, Hadman M, Wakade C, De Sevilla LM, Dhandapani KM, Mahesh VB, Vadlamudi RK, and Brann DW (2005) Cloning, expression, and localization of MNAR/PELP1 in rodent brain: colocalization in estrogen receptor-alpha-but not in gonadotropin-releasing hormone-positive neurons. Endocrinology 146:5215-5227.
126. Kim AS, Kakalis LT, Abdul-Manan N, Liu GA, and Rosen MK (2000) Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404: 151-158.
127. Kim Y, Sung JY, Ceglia I, Lee KW, Ahn JH, Halford JM, Kim AM, Kwak SP, Park JB, and Ho Ryu S, et al. (2006) Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 442:814-817.
128. Klann E, Antion MD, Banko JL, and Hou L (2004) Synaptic plasticity and translation initiation. Learn Mem 11:365-372.
129. Kobayashi M, Ishii H, and Sakuma Y (2011) Identification of novel splicing events and post-transcriptional regulation of human estrogen receptor a F isoforms. Mol Cell Endocrinol 333:55-61.
130. Konkle AT and McCarthy MM (2011) Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology 152:223-235.
131. Konur S and Yuste R (2004) Imaging the motility of dendritic protrusions and axon terminals: roles in axon sampling and synaptic competition. Mol Cell Neurosci 27: 427-440.
132. Kramár EA, Chen LY, Brandon NJ, Rex CS, Liu F, Gall CM, and Lynch G (2009) Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J Neurosci 29:12982-12993.
133. Kretz O, Fester L, Wehrenberg U, Zhou L, Brauckmann S, Zhao S, Prange-Kiel J, Naumann T, Jarry H, and Frotscher M, et al. (2004) Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 24:5913-5921.
134. Kritzer MF (2002) Regional, laminar, and cellular distribution of immunoreactivity for ER alpha and ER beta in the cerebral cortex of hormonally intact, adult male and female rats. Cereb Cortex 12:116-128.
135. Kritzer MF, Brewer A, Montalmant F, Davenport M, and Robinson JK (2007) Effects of gonadectomy on performance in operant tasks measuring prefrontal cortical function in adult male rats. Horm Behav 51:183-194.
136. Kríz L, Bicíková M, and Hampl R (2008) Roles of steroid sulfatase in brain and other tissues. Physiol Res 57:657-668.
137. Kudwa AE and Rissman EF (2003) Double oestrogen receptor alpha and beta knockout mice reveal differences in neural oestrogen-mediated progestin receptor induction and female sexual behaviour. J Neuroendocrinol 15:978-983.
138. Kulkarni J (2009) Oestrogen-a new treatment approach for schizophrenia? Med J Aust 190(4, Suppl):S37-S38.
139. Kulkarni J, de Castella A, Fitzgerald PB, Gurvich CT, Bailey M, Bartholomeusz C, and Burger H (2008) Estrogen in severe mental illness: a potential new treatment approach. Arch Gen Psychiatry 65:955-960.
140. Langer G, Bader B, Meoli L, Isensee J, Delbeck M, Noppinger PR, and Otto C (2010) A critical review of fundamental controversies in the field of GPR30 research. Steroids 75:603-610.
141. Lavaque E, Sierra A, Azcoitia I, and Garcia-Segura LM (2006) Steroidogenic acute regulatory protein in the brain. Neuroscience 138:741-747.
142. Le Bé JV and Markram H (2006) Spontaneous and evoked synaptic rewiring in the neonatal neocortex. Proc Natl Acad Sci USA 103:13214-13219.
143. Le Romancer M, Treilleux I, Leconte N, Robin-Lespinasse Y, Sentis S, Bouchekioua-Bouzaghou K, Goddard S, Gobert-Gosse S, and Corbo L (2008) Regulation of estrogen rapid signaling through arginine methylation by PRMT1. Mol Cell 31: 212-221.
144. Lee AW and Pfaff DW (2008) Hormone effects on specific and global brain functions. J Physiol Sci 58:213-220.
145. Levin ER (2011) Minireview: extranuclear steroid receptors: roles in modulation of cell functions. Mol Endocrinol 25:377-384.
146. Liu F, Day M, Muñiz LC, Bitran D, Arias R, Revilla-Sanchez R, Grauer S, Zhang G, Kelley C, and Pulito V, et al. (2008) Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci 11: 334-343.
147. Logan SM, Sarkar SN, Zhang Z, and Simpkins JW (2011) Estrogen-induced signaling attenuates soluble Ab peptide-mediated dysfunction of pathways in synaptic plasticity. Brain Res 1383:1-12.
148. Lokuge S, Frey BN, Foster JA, Soares CN, and Steiner M (2010) The rapid effects of estrogen: a mini-review. Behav Pharmacol 21:465-472.
149. London SE and Clayton DF (2008) Functional identification of sensory mechanisms required for developmental song learning. Nat Neurosci 11:579-586.
150. Lösel R and Wehling M (2003) Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol 4:46-56.
151. Lu Q, Pallas DC, Surks HK, Baur WE, Mendelsohn ME, and Karas RH (2004) Striatin assembles a membrane signaling complex necessary for rapid, nongenomic activation of endothelial NO synthase by estrogen receptor alpha. Proc Natl Acad Sci USA 101:17126-17131.
152. Luine VN (2007) The prefrontal cortex, gonadal hormones and memory. Horm Behav 51:181-182.
153. Luine VN (2008) Sex steroids and cognitive function. J Neuroendocrinol 20:866-872.
154. Luine VN, Jacome LF, and Maclusky NJ (2003) Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144:2836-2844.
155. MacLusky NJ, Luine VN, Hajszan T, and Leranth C (2005) The 17alpha and 17beta isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 146:287-293.
156. MacLusky NJ, Naftolin F, and Goldman-Rakic PS (1986) Estrogen formation and binding in the cerebral cortex of the developing rhesus monkey. Proc Natl Acad Sci USA 83:513-516.
157. Maggiolini M and Picard D (2010) The unfolding stories of GPR30, a new membranebound estrogen receptor. J Endocrinol 204:105-114.
158. Mak P, Zeen R, and Callard GV(1985) Subcellular distribution and reaction kinetics of aromatase in goldfish brain, in Program of the 67th Annual Meeting of The Endocrine Society; Baltimore, MD:265.
159. Malenka RC and Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
160. Manser E, Leung T, Salihuddin H, Zhao ZS, and Lim L (1994) A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367:40-46.
161. Martin S, Jones M, Simpson E, and van den Buuse M (2003) Impaired spatial reference memory in aromatase-deficient (ArKO) mice. Neuroreport 14:1979-1982.
162. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, and Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092.
163. Maze I, Noh KM, and Allis CD (2013) Histone regulation in the CNS: basic principles of epigenetic plasticity. Neuropsychopharmacology 38:3-22.
164. McDevitt MA, Glidewell-Kenney C, Jimenez MA, Ahearn PC, Weiss J, Jameson JL, and Levine JE (2008) New insights into the classical and non-classical actions of estrogen: evidence from estrogen receptor knock-out and knock-in mice. Mol Cell Endocrinol 290:24-30.
165. McEwen BS and Alves SE (1999) Estrogen actions in the central nervous system. Endocr Rev 20:279-307.
166. Melcangi RC, Panzica G, and Garcia-Segura LM (2011) Neuroactive steroids: focus on human brain. Neuroscience 191:1-5.
167. Mendez P, Azcoitia I, and Garcia-Segura LM (2003) Estrogen receptor alpha forms estrogen-dependent multimolecular complexes with insulin-like growth factor receptor and phosphatidylinositol 3-kinase in the adult rat brain. Brain Res Mol Brain Res 112:170-176.
168. Mendez P, Garcia-Segura LM, and Muller D (2011) Estradiol promotes spine growth and synapse formation without affecting pre-established networks. Hippocampus 21:1263-1267.
169. Mensah-Nyagan AG, Beaujean D, Do-Rego JL, Mathieu M, Vallarino M, Luu-The V, Pelletier G, and Vaudry H (2000) In vivo evidence for the production of sulfated steroids in the frog brain. Comp Biochem Physiol B Biochem Mol Biol 126:213-219.
170. Mermelstein PG, Becker JB, and Surmeier DJ (1996) Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. J Neurosci 16: 595-604.
171. Micevych P, Bondar G, and Kuo J (2010) Estrogen actions on neuroendocrine glia. Neuroendocrinology 91:211-222.
172. Micevych PE and Kelly MJ (2012) Membrane estrogen receptor regulation of hypothalamic function. Neuroendocrinology 96:103-110.
173. Milner TA, Ayoola K, Drake CT, Herrick SP, Tabori NE, McEwen BS, Warrier S, and Alves SE (2005) Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 491:81-95.
174. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, and Alves SE (2001) Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 429:355-371.
175. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, and Schaeffer JM, et al. (2003) Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144:2055-2067.
176. Mitterling KL, Spencer JL, Dziedzic N, Shenoy S, McCarthy K, Waters EM, McEwen BS, and Milner TA (2010) Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J Comp Neurol 518:2729-2743.
177. Mooney R (2009) Neurobiology of song learning. Curr Opin Neurobiol 19:654-660.
178. Mukai H, Tsurugizawa T, Murakami G, Kominami S, Ishii H, Ogiue-Ikeda M, Takata N, Tanabe N, Furukawa A, and Hojo Y, et al. (2007) Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J Neurochem 100:950-967.
179. Murakami G, Tsurugizawa T, Hatanaka Y, Komatsuzaki Y, Tanabe N, Mukai H, Hojo Y, Kominami S, Yamazaki T, and Kimoto T, et al. (2006) Comparison between basal and apical dendritic spines in estrogen-induced rapid spinogenesis of CA1 principal neurons in the adult hippocampus. Biochem Biophys Res Commun 351: 553-558.
180. Murakoshi H and Yasuda R (2012) Postsynaptic signaling during plasticity of dendritic spines. Trends Neurosci 35:135-143.
181. Murphy DD, Cole NB, Greenberger V, and Segal M (1998) Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. J Neurosci 18:2550-2559.
182. Murphy DD and Segal M (1997) Morphological plasticity of dendritic spines in central neurons is mediated by activation of cAMP response element binding protein. Proc Natl Acad Sci USA 94:1482-1487.
183. Nabekura J, Oomura Y, Minami T, Mizuno Y, and Fukuda A (1986) Mechanism of the rapid effect of 17 beta-estradiol on medial amygdala neurons. Science 233:226-228.
184. Nadal A, Alonso-Magdalena P, Soriano S, Ripoll C, Fuentes E, Quesada I, and Ropero AB (2011) Role of estrogen receptors alpha, beta and GPER1/GPR30 in pancreatic beta-cells. Front Biosci (Landmark Ed) 16:251-260.
185. Naftolin F, Horvath TL, Jakab RL, Leranth C, Harada N, and Balthazart J (1996) Aromatase immunoreactivity in axon terminals of the vertebrate brain. An immunocytochemical study on quail, rat, monkey and human tissues. Neuroendocrinology 63:149-155.
186. Naftolin F, Ryan KJ, and Petro Z (1971a) Aromatization of androstenedione by limbic system tissue from human foetuses. J Endocrinol 51:795-796.
187. Naftolin F, Ryan KJ, and Petro Z (1971b) Aromatization of androstenedione by the diencephalon. J Clin Endocrinol Metab 33:368-370.
188. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, and Monteggia LM (2002) Neurobiology of depression. Neuron 34:13-25.
189. Nilsson S, Koehler KF, and Gustafsson JA (2011) Development of subtype-selective oestrogen receptor-based therapeutics. Nat Rev Drug Discov 10:778-792.
190. Nilsson S, Mäkelä S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, and Gustafsson JA (2001) Mechanisms of estrogen action. Physiol Rev 81:1535-1565.
191. O'Neill EE, Blewett AR, Loria PM, and Greene GL (2008) Modulation of alpha-CaMKII signaling by rapid ERalpha action. Brain Res 1222:1-17.
192. Opazo P, Sainlos M, and Choquet D (2012) Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr Opin Neurobiol 22:453-460.
193. Ordóñez-Morán P and Muñoz A (2009) Nuclear receptors: genomic and non-genomic effects converge. Cell Cycle 8:1675-1680.
194. Panatier A, Vallée J, Haber M, Murai KK, Lacaille JC, and Robitaille R (2011) Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146:785-798.
195. Paul SM and Purdy RH (1992) Neuroactive steroids. FASEB J 6:2311-2322.
196. Pedram A, Razandi M, Sainson RC, Kim JK, Hughes CC, and Levin ER (2007) A conserved mechanism for steroid receptor translocation to the plasma membrane. J Biol Chem 282:22278-22288.
197. Pelletier G (2010) Steroidogenic enzymes in the brain: morphological aspects. Prog Brain Res 181:193-207.
198. Penzes P and Cahill ME (2012) Deconstructing signal transduction pathways that regulate the actin cytoskeleton in dendritic spines. Cytoskeleton (Hoboken) 7: 426-441.
199. Penzes P, Cahill ME, Jones KA, and Srivastava DP (2008) Convergent CaMK and RacGEF signals control dendritic structure and function. Trends Cell Biol 18: 405-413.
200. Penzes P, Cahill ME, Jones KA, VanLeeuwen JE, and Woolfrey KM (2011a) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14:285-293.
201. Penzes P, Woolfrey KM, and Srivastava DP (2011b) Epac2-mediated dendritic spine remodeling: implications for disease. Mol Cell Neurosci 46:368-380.
202. Perea G and Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317:1083-1086.
203. Perea G, Navarrete M, and Araque A (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32:421-431.
204. Peterson RS, Yarram L, Schlinger BA, and Saldanha CJ (2005) Aromatase is presynaptic and sexually dimorphic in the adult zebra finch brain. Proc Biol Sci 272: 2089-2096.
205. Pfaff DW and Ribeiro AC (2010) Theoretical consequences of fluctuating versus constant liganding of oestrogen receptor-alpha in neurones. J Neuroendocrinol 22: 486-491.
206. Pfrieger FW and Ungerer N (2011) Cholesterol metabolism in neurons and astrocytes. Prog Lipid Res 50:357-371.
207. Phan A, Gabor CS, Favaro KJ, Kaschack S, Armstrong JN, MacLusky NJ, and Choleris E (2012) Low doses of 17b-estradiol rapidly improve learning and increase hippocampal dendritic spines. Neuropsychopharmacology 37:2299-2309.
208. Phan A, Lancaster KE, Armstrong JN, MacLusky NJ, and Choleris E (2011) Rapid effects of estrogen receptor a and b selective agonists on learning and dendritic spines in female mice. Endocrinology 152:1492-1502.
209. Pierman S, Sica M, Allieri F, Viglietti-Panzica C, Panzica GC, and Bakker J (2008) Activational effects of estradiol and dihydrotestosterone on social recognition and the arginine-vasopressin immunoreactive system in male mice lacking a functional aromatase gene. Horm Behav 54:98-106.
210. Prange-Kiel J, Fester L, Zhou L, Lauke H, Carrétero J, and Rune GM (2006) Inhibition of hippocampal estrogen synthesis causes region-specific downregulation of synaptic protein expression in hippocampal neurons. Hippocampus 16:464-471.
211. Price RH Jr, Butler CA, Webb P, Uht R, Kushner P, and Handa RJ (2001) A splice variant of estrogen receptor beta missing exon 3 displays altered subnuclear localization and capacity for transcriptional activation. Endocrinology 142: 2039-2049.
212. Prossnitz ER and Barton M (2011) The G-protein-coupled estrogen receptor GPER in health and disease. Nat Rev Endocrinol 7:715-726.
213. Prossnitz ER and Maggiolini M (2009) Mechanisms of estrogen signaling and gene expression via GPR30. Mol Cell Endocrinol 308:32-38.
214. Ramón y Cajal S (1911) Histology of the Nervous System of Man and Vertebrates, Oxford University Press, New York.
215. Rasia-Filho AA, Fabian C, Rigoti KM, and Achaval M (2004) Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience 126:839-847.
216. Raz L, Khan MM, Mahesh VB, Vadlamudi RK, and Brann DW (2008) Rapid estrogen signaling in the brain. Neurosignals 16:140-153.
217. Remage-Healey L, Coleman MJ, Oyama RK, and Schlinger BA (2010) Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird. Proc Natl Acad Sci USA 107:3852-3857.
218. Remage-Healey L, Dong S, Maidment NT, and Schlinger BA (2011) Presynaptic control of rapid estrogen fluctuations in the songbird auditory forebrain. J Neurosci 31:10034-10038.
219. Remage-Healey L, Maidment NT, and Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11:1327-1334.
220. Ribeiro AC, Musatov S, Shteyler A, Simanduyev S, Arrieta-Cruz I, Ogawa S, and Pfaff DW (2012) siRNA silencing of estrogen receptor-a expression specifically in medial preoptic area neurons abolishes maternal care in female mice. Proc Natl Acad Sci USA 109:16324-16329.
221. Riccio A (2010) Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways. Nat Neurosci 13:1330-1337.
222. Roberts TF, Tschida KA, Klein ME, and Mooney R (2010) Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature 463: 948-952.
223. Romand S, Wang Y, Toledo-Rodriguez M, and Markram H (2011) Morphological development of thick-tufted layer v pyramidal cells in the rat somatosensory cortex. Front Neuroanat 5:5.
224. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, and Johnson KC, et al.; Writing Group for the Women's Health Initiative Investigators (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 288:321-333.
225. Rune GM and Frotscher M (2005) Neurosteroid synthesis in the hippocampus: role in synaptic plasticity. Neuroscience 136:833-842.
226. Rupprecht R and Holsboer F (1999) Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci 22:410-416.
227. Sakamoto H, Takahashi H, Matsuda K, Nishi M, Takanami K, Ogoshi M, Sakamoto T, and Kawata M (2012) Rapid signaling of steroid hormones in the vertebrate nervous system. Front Biosci (Landmark Ed) 17:996-1019.
228. Saldanha CJ, Remage-Healey L, and Schlinger BA (2011) Synaptocrine signaling: steroid synthesis and action at the synapse. Endocr Rev 32:532-549.
229. Saldanha CJ, Tuerk MJ, Kim YH, Fernandes AO, Arnold AP, and Schlinger BA (2000) Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody. J Comp Neurol 423:619-630.
230. Sánchez-Andrade G and Kendrick KM (2011) Roles of a-and b-estrogen receptors in mouse social recognition memory: effects of gender and the estrous cycle. Horm Behav 59:114-122.
231. Sanchez AM, Flamini MI, Baldacci C, Goglia L, Genazzani AR, and Simoncini T (2010a) Estrogen receptor-alpha promotes breast cancer cell motility and invasion via focal adhesion kinase and N-WASP. Mol Endocrinol 24:2114-2125.
232. Sanchez AM, Flamini MI, Fu XD, Mannella P, Giretti MS, Goglia L, Genazzani AR, and Simoncini T (2009) Rapid signaling of estrogen to WAVE1 and moesin controls neuronal spine formation via the actin cytoskeleton. Mol Endocrinol 23:1193-1202.
233. Sánchez MG, Bourque M, Morissette M, and Di Paolo T (2010b) Steroids-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci Ther 16:e43-e71.
234. Sandén C, Broselid S, Cornmark L, Andersson K, Daszkiewicz-Nilsson J, Mårtensson UE, Olde B, and Leeb-Lundberg LM (2011) G protein-coupled estrogen receptor 1/G protein-coupled receptor 30 localizes in the plasma membrane and traffics intracellularly on cytokeratin intermediate filaments. Mol Pharmacol 79:400-410.
235. Sano K, Tsuda MC, Musatov S, Sakamoto T, and Ogawa S (2013) Differential effects of site-specific knockdown of estrogen receptor a in the medial amygdala, medial pre-optic area, and ventromedial nucleus of the hypothalamus on sexual and aggressive behavior of male mice. Eur J Neurosci 37:1308-1319.
236. Scharfman HE, Hintz TM, Gomez J, Stormes KA, Barouk S, Malthankar-Phatak GH, McCloskey DP, Luine VN, and Maclusky NJ (2007) Changes in hippocampal function of ovariectomized rats after sequential low doses of estradiol to simulate the preovulatory estrogen surge. Eur J Neurosci 26:2595-2612.
237. Schlinger BA and Callard GV (1989) Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology 49:434-441.
238. Scott E, Zhang QG, Wang R, Vadlamudi R, and Brann D (2012) Estrogen neuroprotection and the critical period hypothesis. Front Neuroendocrinol 33:85-104.
239. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev Neurosci 6: 277-284.
240. Segal M (2010) Dendritic spines, synaptic plasticity and neuronal survival: activity shapes dendritic spines to enhance neuronal viability. Eur J Neurosci 31: 2178-2184.
241. Shepherd JD and Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613-643.
242. Sherwin BB and Henry JF (2008) Brain aging modulates the neuroprotective effects of estrogen on selective aspects of cognition in women: a critical review. Front Neuroendocrinol 29:88-113.
243. Shi Y, Pontrello CG, DeFea KA, Reichardt LF, and Ethell IM (2009) Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. J Neurosci 29:8129-8142.
244. Shumaker SA, Legault C, Kuller L, Rapp SR, Thal L, Lane DS, Fillit H, Stefanick ML, Hendrix SL, and Lewis CE, et al.; Women's Health Initiative Memory Study (2004) Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291:2947-2958.
245. Sierra A, Gottfried-Blackmore A, Milner TA, McEwen BS, and Bulloch K (2008) Steroid hormone receptor expression and function in microglia. Glia 56:659-674.
246. Sinopoli KJ, Floresco SB, and Galea LA (2006) Systemic and local administration of estradiol into the prefrontal cortex or hippocampus differentially alters working memory. Neurobiol Learn Mem 86:293-304.
247. Smith CC and McMahon LL (2006) Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 26:8517-8522.
248. Snyder MA, Smejkalova T, Forlano PM, and Woolley CS (2010) Multiple ERbeta antisera label in ERbeta knockout and null mouse tissues. J Neurosci Methods 188: 226-234.
249. Soderling SH, Guire ES, Kaech S, White J, Zhang F, Schutz K, Langeberg LK, Banker G, Raber J, and Scott JD (2007) A WAVE-1 and WRP signaling complex regulates spine density, synaptic plasticity, and memory. J Neurosci 27:355-365.
250. Soderling SH, Langeberg LK, Soderling JA, Davee SM, Simerly R, Raber J, and Scott JD (2003) Loss of WAVE-1 causes sensorimotor retardation and reduced learning and memory in mice. Proc Natl Acad Sci USA 100:1723-1728.
251. Spary EJ, Maqbool A, and Batten TF (2009) Oestrogen receptors in the central nervous system and evidence for their role in the control of cardiovascular function. J Chem Neuroanat 38:185-196.
252. Spence RD, Hamby ME, Umeda E, Itoh N, Du S, Wisdom AJ, Cao Y, Bondar G, Lam J, and Ao Y, et al. (2011) Neuroprotection mediated through estrogen receptoralpha in astrocytes. Proc Natl Acad Sci USA 108:8867-8872.
253. Spencer JL, Waters EM, Milner TA, and McEwen BS (2008) Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 155:1106-1119.
254. Srivastava DP (2012) Two-step wiring plasticity-a mechanism for estrogen-induced rewiring of cortical circuits. J Steroid Biochem Mol Biol 131:17-23.
255. Srivatsava DP and Evans PD (2013) GPER 1: trials and tribulations of a Membrane Oestrogen Receptor. J Neuroendocrinol doi: 10.1111/jne.12071 [published ahead of print].
256. Srivastava DP, Copits BA, Xie Z, Huda R, Jones KA, Mukherji S, Cahill ME, Van-Leeuwen JE, Woolfrey KM, and Rafalovich I, et al. (2012a) Afadin is required for maintenance of dendritic structure and excitatory tone. J Biol Chem 287: 35964-35974.
257. Srivastava DP, Jones KA, Woolfrey KM, Burgdorf J, Russell TA, Kalmbach A, Lee H, Yang C, Bradberry MM, and Wokosin D, et al. (2012b) Social, communication, and cortical structural impairments in Epac2-deficient mice. J Neurosci 32: 11864-11878.
258. Srivastava DP and Penzes P (2011) Rapid estradiol modulation of neuronal connectivity and its implications for disease. Front Endocrinol (Lausanne) 2:77.
259. Srivastava DP, Waters EM, Mermelstein PG, Kramár EA, Shors TJ, and Liu F (2011) Rapid estrogen signaling in the brain: implications for the fine-tuning of neuronal circuitry. J Neurosci 31:16056-16063.
260. Srivastava DP, Woolfrey KM, and Evans PD (2013) Mechanisms underlying the interactions between rapid estrogenic and BDNF control of synaptic connectivity. Neuroscience 239:17-33.
261. Srivastava DP, Woolfrey KM, Jones KA, Anderson CT, Smith KR, Russell TA, Lee H, Yasvoina MV, Wokosin DL, and Ozdinler PH, et al. (2012d) An autism-associated variant of Epac2 reveals a role for Ras/Epac2 signaling in controlling basal dendrite maintenance in mice. PLoS Biol 10:e1001350.
262. Srivastava DP, Woolfrey KM, Jones KA, Shum CY, Lash LL, Swanson GT, and Penzes P (2008) Rapid enhancement of two-step wiring plasticity by estrogen and NMDA receptor activity. Proc Natl Acad Sci USA 105:14650-14655.
263. Srivastava DP, Woolfrey KM, Liu F, Brandon NJ, and Penzes P (2010) Estrogen receptor ß activity modulates synaptic signaling and structure. J Neurosci 30: 13454-13460.
264. Srivastava DP, Yu EJ, Kennedy K, Chatwin H, Reale V, Hamon M, Smith T, and Evans PD (2005) Rapid, nongenomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein-coupled receptor. J Neurosci 25: 6145-6155.
265. Star EN, Kwiatkowski DJ, and Murthy VN (2002) Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5:239-246.
266. Stepanyants A and Chklovskii DB (2005) Neurogeometry and potential synaptic connectivity. Trends Neurosci 28:387-394.
267. Stevis PE, Deecher DC, Suhadolnik L, Mallis LM, and Frail DE (1999) Differential effects of estradiol and estradiol-BSA conjugates. Endocrinology 140:5455-5458.
268. Steward O and Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299-325.
269. Stocco DM (2001) Tracking the role of a star in the sky of the new millennium. Mol Endocrinol 15:1245-1254.
270. Tabatadze N, Smejkalova T, and Woolley CS (2013) Distribution and posttranslational modification of synaptic ERa in the adult female rat hippocampus. Endocrinology 154:819-830.
271. Tada T and ShengM (2006) Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 16:95-101.
272. Takai Y, Sasaki T, and Matozaki T (2001) Small GTP-binding proteins. Physiol Rev 81:153-208.
273. Takenawa T and Suetsugu S (2007) The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8:37-48.
274. Taniguchi Y, Young-Pearse T, Sawa A, and Kamiya A (2012) In utero electroporation as a tool for genetic manipulation in vivo to study psychiatric disorders: from genes to circuits and behaviors. Neuroscientist 18:169-179.
275. Tashiro A and Yuste R (2004) Regulation of dendritic spine motility and stability by Rac1 and Rho kinase: evidence for two forms of spine motility. Mol Cell Neurosci 26:429-440.
276. Tau GZ and Peterson BS (2010) Normal development of brain circuits. Neuropsychopharmacology 35:147-168.
277. Thomas GM and Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5:173-183.
278. Thomas P (2012) Rapid steroid hormone actions initiated at the cell surface and the receptors that mediate them with an emphasis on recent progress in fish models. Gen Comp Endocrinol 175:367-383.
279. Toda K, Saibara T, Okada T, Onishi S, and Shizuta Y (2001) A loss of aggressive behaviour and its reinstatement by oestrogen in mice lacking the aromatase gene (Cyp19). J Endocrinol 168:217-220.
280. Toran-Allerand CD (1976) Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: implications for sexual differentiation. Brain Res 106:407-412.
281. Toran-Allerand CD (2004) Minireview: A plethora of estrogen receptors in the brain: where will it end? Endocrinology 145:1069-1074.
282. Torrey EF and Davis JM (2012) Adjunct treatments for schizophrenia and bipolar disorder: what to try when you are out of ideas. Clin Schizophr Relat Psychoses 5: 208-216.
283. Tremere LA, Jeong JK, and Pinaud R (2009) Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression. J Neurosci 29:5949-5963.
284. Tremere LA and Pinaud R (2011) Brain-generated estradiol drives long-term optimization of auditory coding to enhance the discrimination of communication signals. J Neurosci 31:3271-3289.
285. Tsurugizawa T, Mukai H, Tanabe N, Murakami G, Hojo Y, Kominami S, Mitsuhashi K, Komatsuzaki Y, Morrison JH, and Janssen WG, et al. (2005) Estrogen induces rapid decrease in dendritic thorns of CA3 pyramidal neurons in adult male rat hippocampus. Biochem Biophys Res Commun 337:1345-1352.
286. Uylings HB, Groenewegen HJ, and Kolb B (2003) Do rats have a prefrontal cortex? Behav Brain Res 146:3-17.
287. Vadlamudi RK, Wang RA, Mazumdar A, Kim Y, Shin J, Sahin A, and Kumar R (2001) Molecular cloning and characterization of PELP1, a novel human coregulator of estrogen receptor alpha. J Biol Chem 276:38272-38279.
288. van Spronsen M and Hoogenraad CC (2010) Synapse pathology in psychiatric and neurologic disease. Curr Neurol Neurosci Rep 10:207-214.
289. Vasudevan N and Pfaff DW (2007) Membrane-initiated actions of estrogens in neuroendocrinology: emerging principles. Endocr Rev 28:1-19.
290. Vasudevan N and Pfaff DW (2008) Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol 29: 238-257.
291. Vivacqua A, Lappano R, De Marco P, Sisci D, Aquila S, De Amicis F, Fuqua SA, Andò S, and Maggiolini M (2009) G protein-coupled receptor 30 expression is upregulated by EGF and TGF alpha in estrogen receptor alpha-positive cancer cells. Mol Endocrinol 23:1815-1826.
292. Walf AA and Frye CA (2008) Rapid and estrogen receptor beta mediated actions in the hippocampus mediate some functional effects of estrogen. Steroids 73: 997-1007.
293. Walf AA, Koonce CJ, and Frye CA (2008a) Estradiol or diarylpropionitrile administration to wild type, but not estrogen receptor beta knockout, mice enhances performance in the object recognition and object placement tasks. Neurobiol Learn Mem 89:513-521.
294. Walf AA, Koonce CJ, and Frye CA (2008b) Estradiol or diarylpropionitrile decrease anxiety-like behavior of wildtype, but not estrogen receptor beta knockout, mice. Behav Neurosci 122:974-981.
295. Walf AA, Rhodes ME, and Frye CA (2006) Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol Learn Mem 86:35-46.
296. Wang AC, Hara Y, Janssen WG, Rapp PR, and Morrison JH (2010) Synaptic estrogen receptor-alpha levels in prefrontal cortex in female rhesus monkeys and their correlation with cognitive performance. J Neurosci 30:12770-12776.
297. Warner M and Gustafsson JA (2006) Nongenomic effects of estrogen: why all the uncertainty? Steroids 71:91-95.
298. Waters EM, Yildirim M, Janssen WG, Lou WY, McEwen BS, Morrison JH, and Milner TA (2011) Estrogen and aging affect the synaptic distribution of estrogen receptor b-immunoreactivity in the CA1 region of female rat hippocampus. Brain Res 1379:86-97.
299. Wegner AM, Nebhan CA, Hu L, Majumdar D, Meier KM, Weaver AM, and Webb DJ (2008) N-wasp and the arp2/3 complex are critical regulators of actin in the development of dendritic spines and synapses. J Biol Chem 283:15912-15920.
300. Wehling M and Lösel R (2006) Non-genomic steroid hormone effects: membrane or intracellular receptors? J Steroid Biochem Mol Biol 102:180-183.
301. Wehrenberg U, Prange-Kiel J, and Rune GM (2001) Steroidogenic factor-1 expression in marmoset and rat hippocampus: co-localization with StAR and aromatase. J Neurochem 76:1879-1886.
302. Wójtowicz T and Mozrzymas JW (2010) Estradiol and GABAergic transmission in the hippocampus. Vitam Horm 82:279-300.
303. Wong M and Moss RL (1991) Electrophysiological evidence for a rapid membrane action of the gonadal steroid, 17 beta-estradiol, on CA1 pyramidal neurons of the rat hippocampus. Brain Res 543:148-152.
304. Woolfrey KM, Srivastava DP, Photowala H, Yamashita M, Barbolina MV, Cahill ME, Xie Z, Jones KA, Quilliam LA, and Prakriya M, et al. (2009) Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat Neurosci 12:1275-1284.
305. Woolley CS (2007) Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47:657-680.
306. Woolley CS, Gould E, Frankfurt M, and McEwen BS (1990) Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
307. Woolley CS and McEwen BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12: 2549-2554.
308. Wu TW, Chen S, and Brinton RD (2011) Membrane estrogen receptors mediate calcium signaling and MAP kinase activation in individual hippocampal neurons. Brain Res 1379:34-43.
309. Wu X, Subramaniam M, Negron V, Cicek M, Reynolds C, Lingle WL, Goetz MP, Ingle JN, Spelsberg TC, and Hawse JR (2012) Development, characterization, and applications of a novel estrogen receptor beta monoclonal antibody. J Cell Biochem 113:711-723.
310. Xiao X, Yang Y, Zhang Y, Zhang XM, Zhao ZQ, and Zhang YQ (2013) Estrogen in the anterior cingulate cortex contributes to pain-related aversion. Cereb Cortex 23: 2190-2203.
311. Xie Z, Huganir RL, and Penzes P (2005) Activity-dependent dendritic spine structural plasticity is regulated by small GTPase Rap1 and its target AF-6. Neuron 48: 605-618.
312. Xie Z, Srivastava DP, Photowala H, Kai L, Cahill ME, Woolfrey KM, Shum CY, Surmeier DJ, and Penzes P (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56:640-656.
313. Yague JG, Muñoz A, de Monasterio-Schrader P, Defelipe J, Garcia-Segura LM, and Azcoitia I (2006) Aromatase expression in the human temporal cortex. Neuroscience 138:389-401.
314. Yague JG, Wang AC, Janssen WG, Hof PR, Garcia-Segura LM, Azcoitia I, and Morrison JH (2008) Aromatase distribution in the monkey temporal neocortex and hippocampus. Brain Res 1209:115-127.
315. Yang G, Pan F, and Gan WB (2009) Stably maintained dendritic spines are associated with lifelong memories. Nature 462:920-924.
316. Yang SH, Liu R, Perez EJ, Wen Y, Stevens SM Jr, Valencia T, Brun-Zinkernagel AM, Prokai L, Will Y, and Dykens J, et al. (2004) Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci USA 101:4130-4135.
317. Yasuda R and Murakoshi H (2011) The mechanisms underlying the spatial spreading of signaling activity. Curr Opin Neurobiol 21:313-321.
318. Yildirim M, Janssen WG, Tabori NE, Adams MM, Yuen GS, Akama KT, McEwen BS, Milner TA, and Morrison JH (2008) Estrogen and aging affect synaptic distribution of phosphorylated LIM kinase (pLIMK) in CA1 region of female rat hippocampus. Neuroscience 152:360-370.
319. Yoshihara Y, De Roo M, and Muller D (2009) Dendritic spine formation and stabilization. Curr Opin Neurobiol 19:146-153.
320. Yuen GS, McEwen BS, and Akama KT (2011) LIM kinase mediates estrogen action on the actin depolymerization factor Cofilin. Brain Res 1379:44-52.
321. Zadran S, Qin Q, Bi X, Zadran H, Kim Y, Foy MR, Thompson R, and Baudry M (2009) 17-Beta-estradiol increases neuronal excitability through MAP kinase-induced calpain activation. Proc Natl Acad Sci USA 106:21936-21941.
322. Zhao L, O'Neill K, and Diaz Brinton R (2005) Selective estrogen receptor modulators (SERMs) for the brain: current status and remaining challenges for developing NeuroSERMs. Brain Res Brain Res Rev 49:472-493.
323. Zhao Z, Fan L, Fortress AM, Boulware MI, and Frick KM (2012) Hippocampal histone acetylation regulates object recognition and the estradiol-induced enhancement of object recognition. J Neurosci 32:2344-2351.
324. Zhao Z, Fan L, and Frick KM (2010) Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation. Proc Natl Acad Sci USA 107:5605-5610.
325. Zhou L, Fester L, von Blittersdorff B, Hassu B, Nogens H, Prange-Kiel J, Jarry H, Wegscheider K, and Rune GM (2010) Aromatase inhibitors induce spine synapse loss in the hippocampus of ovariectomized mice. Endocrinology 151:1153-1160.
326. Zhou L, Lehan N, Wehrenberg U, Disteldorf E, von Lossow R, Mares U, Jarry H, and Rune GM (2007) Neuroprotection by estradiol: a role of aromatase against spine synapse loss after blockade of GABA(A) receptors. Exp Neurol 203:72-81.
327. Zhu BT and Conney AH (1998) Functional role of estrogen metabolism in target cells: review and perspectives. Carcinogenesis 19:1-27.
328. Ziv NE and Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102.
329. Zwain IH and Yen SS (1999) Dehydroepiandrosterone: biosynthesis and metabolism in the brain. Endocrinology 140:880-887.