Role of estrogen receptor alpha and beta expression and signaling on cognitive function during aging

Hippocampus

Volumn 22, Issue 4, 2012, Pages 656-669

  Foster, Thomas C ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Estradiol; Hippocampus; Memory; Synaptogenesis; Transcription

Indexed keywords

AMPA RECEPTOR; CALCIUM; CYCLIC AMP; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN KINASE B; SYNAPTOPHYSIN;

AGING; COGNITION; DNA BINDING; GENE EXPRESSION; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMAN; INTRACELLULAR SIGNALING; LEARNING; MEMORY; MEMORY DISORDER; NEUROPROTECTION; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

AGING; ANIMALS; COGNITION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; HUMANS; MEMORY; MEMORY DISORDERS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MODELS, PSYCHOLOGICAL; NEUROGENESIS; RATS; SIGNAL TRANSDUCTION;

EID: 84858727599     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20935     Document Type: Note

References (200)

1. Adams MM, Oung T, Morrison JH, Gore AC. 2001. Length of postovariectomy interval and age, but not estrogen replacement, regulate N-methyl-D-aspartate receptor mRNA levels in the hippocampus of female rats. Exp Neurol 170: 345-356.
2. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA, McEwen BS, 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.
3. Aenlle KK, Foster TC. 2010. Aging alters the expression of genes for neuroprotection and synaptic function following acute estradiol treatment. Hippocampus 20: 1047-1060.
4. Aenlle KK, Kumar A, Cui L, Jackson TC, Foster TC. 2009. Estrogen effects on cognition and hippocampal transcription in middle-aged mice. Neurobiol Aging 30: 932-945.
5. Akama KT, McEwen BS. 2003. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J Neurosci 23: 2333-2339.
6. Akram A, Christoffel D, Rocher AB, Bouras C, Kovari E, Perl DP, Morrison JH, Herrmann FR, Haroutunian V, Giannakopoulos P, Hof PR. 2008. Stereologic estimates of total spinophilin-immunoreactive spine number in area 9 and the CA1 field: Relationship with the progression of Alzheimer's disease. Neurobiol Aging 29: 1296-1307.
7. Barha CK, Dalton GL, Galea LA. 2010a. Low doses of 17alpha-estradiol and 17beta-estradiol facilitate, whereas higher doses of estrone and 17alpha- and 17beta-estradiol impair, contextual fear conditioning in adult female rats. Neuropsychopharmacology 35: 547-559.
8. Barha CK, Brummelte S, Lieblich SE, Galea LA. Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus (in press).
9. Barker JM, Galea LA. 2009. Sex and regional differences in estradiol content in the prefrontal cortex, amygdala and hippocampus of adult male and female rats. Gen Comp Endocrinol 164: 77-84.
10. Barha CK, Galea LA. 2010. Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochim Biophys Acta 1800: 1056-1067.
11. Barkhem T, Carlsson B, Nilsson Y, Enmark E, Gustafsson J, Nilsson S. 1998. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol Pharmacol 54: 105-112.
12. Bi R, Foy MR, Thompson RF, Baudry M. 2003. Effects of estrogen, age, and calpain on MAP kinase and NMDA receptors in female rat brain. Neurobiol Aging 24: 977-983.
13. Bimonte-Nelson HA, Francis KR, Umphlet CD, Granholm AC. 2006. Progesterone reverses the spatial memory enhancements initiated by tonic and cyclic oestrogen therapy in middle-aged ovariectomized female rats. Eur J Neurosci 24: 229-242.
14. Blalock EM, Chen KC, Sharrow K, Herman JP, Porter NM, Foster TC, Landfield PW. 2003. Gene microarrays in hippocampal aging: Statistical profiling identifies novel processes correlated with cognitive impairment. J Neurosci 23: 3807-3819.
15. Bohacek J, Daniel JM. 2009. The ability of oestradiol administration to regulate protein levels of oestrogen receptor alpha in the hippocampus and prefrontal cortex of middle-aged rats is altered following long-term ovarian hormone deprivation. J Neuroendocrinol 21: 640-647.
16. Boulware MI, Weick JP, Becklund BR, Kuo SP, Groth RD, Mermelstein PG. 2005. Estradiol activates group I, II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J Neurosci 25: 5066-5078.
17. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, Oprea TI, Prossnitz ER, 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.
18. Brewer GJ, Reichensperger JD, Brinton RD. 2006. Prevention of age-related dysregulation of calcium dynamics by estrogen in neurons. Neurobiol Aging 27: 306-317.
19. Brewer LD, Dowling AL, Curran-Rauhut MA, Landfield PW, Porter NM, Blalock EM. 2009. Estradiol reverses a calcium-related biomarker of brain aging in female rats. J Neurosci 29: 6058-6067.
20. Brinton RD. 2008. The healthy cell bias of estrogen action: Mitochondrial bioenergetics and neurological implications. Trends Neurosci 31: 529-537.
21. Brinton RD. 2009. Estrogen-induced plasticity from cells to circuits: Predictions for cognitive function. Trends Pharmacol Sci 30: 212-222.
22. Calabrese EJ. 2001. Estrogen and related compounds: Biphasic dose responses. Crit Rev Toxicol 31: 503-515.
23. Carswell HV, Macrae IM, Gallagher L, Harrop E, Horsburgh KJ. 2004. Neuroprotection by a selective estrogen receptor beta agonist in a mouse model of global ischemia. Am J Physiol Heart Circ Physiol 287: H1501-H1504.
24. Chung WC, Pak TR, Suzuki S, Pouliot WA, Andersen ME, 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.
25. Ciana P, Raviscioni M, Mussi P, Vegeto E, Que I, Parker MG, Lowik C, Maggi A. 2003. In vivo imaging of transcriptionally active estrogen receptors. Nat Med 9: 82-86.
26. Coleman KM, Smith CL. 2001. Intracellular signaling pathways: Nongenomic actions of estrogens and ligand-independent activation of estrogen receptors. Front Biosci 6: D1379-D1391.
27. Coleman KM, Dutertre M, El-Gharbawy A, Rowan BG, Weigel NL, Smith CL. 2003. Mechanistic differences in the activation of estrogen receptor-alpha (ER alpha)- and ER beta-dependent gene expression by cAMP signaling pathway(s). J Biol Chem 278: 12834-12845.
28. Colucci-D'Amato L, Perrone-Capano C, di Porzio U. 2003. Chronic activation of ERK, neurodegenerative diseases. Bioessays 25: 1085-1095.
29. Corbo RM, Gambina G, Ruggeri M, Scacchi R. 2006. Association of estrogen receptor alpha (ESR1) PvuII and XbaI polymorphisms with sporadic Alzheimer's disease and their effect on apolipoprotein E concentrations. Dement Geriatr Cogn Disord 22: 67-72.
30. Cowley SM, Parker MG. 1999. A comparison of transcriptional activation by ER alpha and ER beta. J Steroid Biochem Mol Biol 69: 165-175.
31. Dai X, Chen L, Sokabe M. 2007. Neurosteroid estradiol rescues ischemia-induced deficit in the long-term potentiation of rat hippocampal CA1 neurons. Neuropharmacology 52: 1124-1138.
32. Daniel JM, Hulst JL, Berbling JL. 2006. Estradiol replacement enhances working memory in middle-aged rats when initiated immediately after ovariectomy but not after a long-term period of ovarian hormone deprivation. Endocrinology 147: 607-614.
33. Devidze N, Fujimori K, Urade Y, Pfaff DW, Mong JA. 2010. Estradiol regulation of lipocalin-type prostaglandin D synthase promoter activity: Evidence for direct and indirect mechanisms. Neurosci Lett 474: 17-21.
34. Dominguez R, Liu R, Baudry M. 2007. 17-Beta-estradiol-mediated activation of extracellular-signal regulated kinase, phosphatidylinositol 3-kinase/protein kinase B-Akt and N-methyl-D-aspartate receptor phosphorylation in cortical synaptoneurosomes. J Neurochem 101: 232-240.
35. El-Tanani MK, Green CD. 1997. Two separate mechanisms for ligand-independent activation of the estrogen receptor. Mol Endocrinol 11: 928-937.
36. Fan X, Xu H, Warner M, Gustafsson JA. 2010a. ERbeta in CNS: New roles in development and function. Prog Brain Res 181: 233-250.
37. Fan L, Zhao Z, Orr PT, Chambers CH, Lewis MC, Frick KM. 2010b. Estradiol-induced 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.
38. Finch CE. 2009. The neurobiology of middle-age has arrived. Neurobiol Aging 30: 515-520; discussion 530-533.
39. Foster TC. 1999. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res Brain Res Rev 30: 236-249.
40. Foster TC. 2005. Interaction of rapid signal transduction cascades and gene expression in mediating estrogen effects on memory over the life span. Front Neuroendocrinol 26: 51-64.
41. Foster TC, Kumar A. 2007. Susceptibility to induction of long-term depression is associated with impaired memory in aged Fischer 344 rats. Neurobiol Learn Mem 87: 522-535.
42. Foster TC, Rani A, Kumar A, Cui L, Semple-Rowland SL. 2008. Viral vector-mediated delivery of estrogen receptor-alpha to the hippocampus improves spatial learning in estrogen receptor-alpha knockout mice. Mol Ther 16: 1587-1593.
43. Foster TC, Sharrow KM, Kumar A, Masse J. 2003. Interaction of age and chronic estradiol replacement on memory and markers of brain aging. Neurobiol Aging 24: 839-852.
44. Foy MR, Baudry M, Foy JG, Thompson RF. 2008. 17beta-estradiol modifies stress-induced and age-related changes in hippocampal synaptic plasticity. Behav Neurosci 122: 301-309.
45. 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.
46. Frick KM, Fernandez SM, Bulinski SC. 2002. Estrogen replacement improves spatial reference memory and increases hippocampal synaptophysin in aged female mice. Neuroscience 115: 547-558.
47. Fugger HN, Cunningham SG, Rissman EF, Foster TC. 1998. Sex differences in the activational effect of ERalpha on spatial learning. Horm Behav 34: 163-170.
48. Fugger HN, Foster TC, Gustafsson J, Rissman EF. 2000. Novel effects of estradiol and estrogen receptor alpha and beta on cognitive function. Brain Res 883: 258-264.
49. Fugger HN, Kumar A, Lubahn DB, Korach KS, Foster TC. 2001. Examination of estradiol effects on the rapid estradiol mediated increase in hippocampal synaptic transmission in estrogen receptor alpha knockout mice. Neurosci Lett 309: 207-209.
50. Gamerdinger M, Manthey D, Behl C. 2006. Oestrogen receptor subtype-specific repression of calpain expression and calpain enzymatic activity in neuronal cells-Implications for neuroprotection against Ca-mediated excitotoxicity. J Neurochem 97: 57-68.
51. Geinisman Y. 2000. Structural synaptic modifications associated with hippocampal LTP, behavioral learning. Cereb Cortex 10: 952-962.
52. Gerrits M, Westenbroek C, Koch T, Grootkarzijn A, ter Horst GJ. 2006. Increased limbic phosphorylated extracellular-regulated kinase 1 and 2 expression after chronic stress is reduced by cyclic 17beta-estradiol administration. Neuroscience 142: 1293-1302.
53. Gibbs RB. 2000. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging 21: 107-116.
54. Gingerich S, Kim GL, Chalmers JA, Koletar MM, Wang X, Wang Y, Belsham DD. 2010. Estrogen receptor alpha and G-protein coupled receptor 30 mediate the neuroprotective effects of 17beta-estradiol in novel murine hippocampal cell models. Neuroscience 170: 54-66.
55. Gonzalez M, Cabrera-Socorro A, Perez-Garcia CG, Fraser JD, Lopez FJ, Alonso R, 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.
56. Gonzales KL, Tetel MJ, Wagner CK. 2008. Estrogen receptor (ER) beta modulates ERalpha responses to estrogens in the developing rat ventromedial nucleus of the hypothalamus. Endocrinology 149: 4615-4621.
57. Gottfried-Blackmore A, Croft G, McEwen BS, Bulloch K. 2007. Transcriptional activity of estrogen receptors ERalpha and ERbeta in the EtC.1 cerebellar granule cell line. Brain Res 1186: 41-47.
58. Gould E, Woolley CS, Frankfurt M, McEwen BS. 1990. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10: 1286-1291.
59. Gresack JE, Frick KM. 2006. Post-training estrogen enhances spatial and object memory consolidation in female mice. Pharmacol Biochem Behav 84: 112-119.
60. Gundlah C, Kohama SG, Mirkes SJ, Garyfallou VT, Urbanski HF, Bethea CL. 2000. Distribution of estrogen receptor beta (ERbeta) mRNA in hypothalamus, midbrain and temporal lobe of spayed macaque: Continued expression with hormone replacement. Brain Res Mol Brain Res 76: 191-204.
61. Hall JM, McDonnell DP. 1999. The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140: 5566-5578.
62. Hazell GG, Yao ST, Roper JA, Prossnitz ER, O'Carroll AM, 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.
63. Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT, Mukai H, Morrison JH, Janssen WG, Kominami S, Harada N, Kimoto T, Kawato S. 2004. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc Natl Acad Sci USA 101: 865-870.
64. Holmes MM, Wide JK, Galea LA. 2002. Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. Behav Neurosci 116: 928-934.
65. Hu S, Lu SF, Kaplan JR, Adams MR, Simon NG. 2005. ERbeta protein expression in female cynomolgus monkey and CF-1 mouse brain: Western analysis. J Neurobiol 64: 298-309.
66. Huang J, Li X, Maguire CA, Hilf R, Bambara RA, Muyan M. 2005. Binding of estrogen receptor beta to estrogen response element in situ is independent of estradiol and impaired by its amino terminus. Mol Endocrinol 19: 2696-712.
67. Iivonen S, Heikkinen T, Puolivali J, Helisalmi S, Hiltunen M, Soininen H, Tanila H. 2006. Effects of estradiol on spatial learning, hippocampal cytochrome P450 19, and estrogen alpha and beta mRNA levels in ovariectomized female mice. Neuroscience 137: 1143-1152.
68. Inagaki T, Gautreaux C, Luine V. 2010. Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm Behav 58: 415-426.
69. Ishunina TA, Fischer DF, Swaab DF. 2007. Estrogen receptor alpha and its splice variants in the hippocampus in aging and Alzheimer's disease. Neurobiol Aging 28: 1670-1681.
70. Ishunina TA, Swaab DF. 2008. Estrogen receptor-alpha splice variants in the human brain. Gynecol Endocrinol 24: 93-98.
71. Ishunina TA, Swaab DF. 2009. Hippocampal estrogen receptor-alpha splice variant TADDI in the human brain in aging and Alzheimer's disease. Neuroendocrinology 89: 187-199.
72. Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, Baylin SB. 1994. Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet 7: 536-540.
73. Jelks KB, Wylie R, Floyd CL, McAllister AK, Wise P. 2007. Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: Critical role of estrogen receptor-alpha. J Neurosci 27: 6903-6913.
74. Jezierski MK, Sohrabji F. 2001. Neurotrophin expression in the reproductively senescent forebrain is refractory to estrogen stimulation. Neurobiol Aging 22: 309-319.
75. Ji Y, Urakami K, Wada-Isoe K, Adachi Y, Nakashima K. 2000. Estrogen receptor gene polymorphisms in patients with Alzheimer's disease, vascular dementia and alcohol-associated dementia. Dement Geriatr Cogn Disord 11: 119-122.
76. Jiang MJ, Peng MT. 1981. Cytoplasmic and nuclear binding of estradiol in the brain and pituitary of old female rats. Gerontology 27): 51-57.
77. Kawai H, Li H, Avraham S, Jiang S, Avraham HK. 2003. Overexpression of histone deacetylase HDAC1 modulates breast cancer progression by negative regulation of estrogen receptor alpha. Int J Cancer 107: 353-358.
78. Kramar EA, Chen LY, Brandon NJ, Rex CS, Liu F, Gall CM, Lynch G. 2009. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J Neurosci 29: 12982-12993.
79. Kretz O, Fester L, Wehrenberg U, Zhou L, Brauckmann S, Zhao S, Prange-Kiel J, Naumann T, Jarry H, Frotscher M, Rune GM. 2004. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 24: 5913-5921.
80. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. 1997. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138: 863-870.
81. Kumar A, Foster TC. 2002. 17beta-estradiol benzoate decreases the AHP amplitude in CA1 pyramidal neurons. J Neurophysiol 88: 621-626.
82. Kumar A, Rani A, Bodhinathan K, Foster TC. 2009. Selective estrogen receptor agonists PPT, DPN differentially regulate hippocampal synaptic transmission in estrogen receptor alpha and beta KO mice. Soc Neurosci Abstr (719.3).
83. Kuroki Y, Fukushima K, Kanda Y, Mizuno K, Watanabe Y. 2000. Putative membrane-bound estrogen receptors possibly stimulate mitogen-activated protein kinase in the rat hippocampus. Eur J Pharmacol 400: 205-209.
84. Lazennec G, Thomas JA, Katzenellenbogen BS. 2001. Involvement of cyclic AMP response element binding protein (CREB) and estrogen receptor phosphorylation in the synergistic activation of the estrogen receptor by estradiol and protein kinase activators. J Steroid Biochem Mol Biol 77: 193-203.
85. Leuner B, Falduto J, Shors TJ. 2003. Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci 23: 659-665.
86. Lewis DK, Johnson AB, Stohlgren S, Harms A, Sohrabji F. 2008. Effects of estrogen receptor agonists on regulation of the inflammatory response in astrocytes from young adult and middle-aged female rats. J Neuroimmunol 195: 47-59.
87. Li C, Brake WG, Romeo RD, Dunlop JC, Gordon M, Buzescu R, Magarinos AM, Allen PB, Greengard P, Luine V, McEwen BS. 2004. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc Natl Acad Sci USA 101: 2185-2190.
88. Lindberg MK, Moverare S, Skrtic S, Gao H, Dahlman-Wright K, Gustafsson JA, Ohlsson C. 2003. Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "ying yang" relationship between ERalpha and ERbeta in mice. Mol Endocrinol 17: 203-208.
89. Liu F, Day M, Muniz LC, Bitran D, Arias R, Revilla-Sanchez R, Grauer S, Zhang G, Kelley C, Pulito V, Sung A, Mervis RF, Navarra R, Hirst WD, Reinhart PH, Marquis KL, Moss SJ, Pangalos MN, Brandon NJ. 2008. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci 11: 334-343.
90. Liu L, van Groen T, Kadish I, Tollefsbol TO. 2009. DNA methylation impacts on learning and memory in aging. Neurobiol Aging 30: 549-560.
91. Mannella P, Brinton RD. 2006. Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: A unified mechanism of estrogen action. J Neurosci 26: 9439-9447.
92. Markham JA, Pych JC, Juraska JM. 2002. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm Behav 42: 284-293.
93. Markowska AL, Savonenko AV. 2002. Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J Neurosci 22: 10985-10995.
94. Matthews J, Gustafsson JA. 2003. Estrogen signaling: A subtle balance between ER alpha and ER beta. Mol Interv 3: 281-292.
95. Mazzucco CA, Lieblich SE, Bingham BI, Williamson MA, Viau V, Galea LA. 2006. Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience 141: 1793-1800.
96. McInerney EM, Weis KE, Sun J, Mosselman S, Katzenellenbogen BS. 1998. Transcription activation by the human estrogen receptor subtype beta (ER beta) studied with ER beta and ER alpha receptor chimeras. Endocrinology 139: 4513-4522.
97. Mehra RD, Sharma K, Nyakas C, Vij U. 2005. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: A qualitative and quantitative study. Brain Res 1056: 22-35.
98. Miller NR, Jover T, Cohen HW, Zukin RS, Etgen AM. 2005. Estrogen can act via estrogen receptor alpha and beta to protect hippocampal neurons against global ischemia-induced cell death. Endocrinology 146: 3070-3079.
99. Miller CA, Campbell SL, Sweatt JD. 2008. DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiol Learn Mem 89: 599-603.
100. Milner TA, Ayoola K, Drake CT, Herrick SP, Tabori NE, McEwen BS, Warrier S, Alves SE. 2005. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 491: 81-95.
101. Miranda P, Williams CL, Einstein G. 1999. Granule cells in aging rats are sexually dimorphic in their response to estradiol. J Neurosci 19: 3316-3325.
102. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE. 2003. Immunolocalization of estrogen receptor beta in the mouse brain: Comparison with estrogen receptor alpha. Endocrinology 144: 2055-2067.
103. Morissette M, Le Saux M, D'Astous M, Jourdain S, Al Sweidi S, Morin N, Estrada-Camarena E, Mendez P, Garcia-Segura LM, Di Paolo T. 2008a. Contribution of estrogen receptors alpha and beta to the effects of estradiol in the brain. J Steroid Biochem Mol Biol 108: 327-338.
104. Morissette M, Le Saux M, Di Paolo T. 2008b. Effect of oestrogen receptor alpha and beta agonists on brain N-methyl-D-aspartate receptors. J Neuroendocrinol 20: 1006-1014.
105. Mosselman S, Polman J, Dijkema R. 1996. ER beta: Identification and characterization of a novel human estrogen receptor. FEBS Lett 392: 49-53.
106. Murakami G, Tsurugizawa T, Hatanaka Y, Komatsuzaki Y, Tanabe N, Mukai H, Hojo Y, Kominami S, Yamazaki T, Kimoto T, Kawato S. 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.
107. Murphy DD, Segal M. 1996. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16: 4059-4068.
108. Nicholson DA, Yoshida R, Berry RW, Gallagher M, Geinisman Y. 2004. Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J Neurosci 24: 7648-7653.
109. Nilsson S, Makela S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson JA. 2001. Mechanisms of estrogen action. Physiol Rev 81: 1535-1565.
110. Norris CM, Halpain S, Foster TC. 1998. Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. J Neurophysiol 80: 1567-1570.
111. Nyborg H. 1990. Sex hormones, brain development, and spatio-perceptual strategies in Turner syndrome. In: Berch D, Bender B, editors. Sex Chromosome Abnormalities and Human Behavior. Washington, DC: American Association for the Advancement of Science.
112. O'Lone R, Knorr K, Jaffe IZ, Schaffer ME, Martini PG, Karas RH, Bienkowska J, Mendelsohn ME, Hansen U. 2007. Estrogen receptors alpha and beta mediate distinct pathways of vascular gene expression, including genes involved in mitochondrial electron transport and generation of reactive oxygen species. Mol Endocrinol 21: 1281-1296.
113. O'Neill EE, Blewett AR, Loria PM, Greene GL. 2008. Modulation of alphaCaMKII signaling by rapid ERalpha action. Brain Res 1222: 1-17.
114. Olsen L, Rasmussen HB, Hansen T, Bagger YZ, Tanko LB, Qin G, Christiansen C, Werge T. 2006. Estrogen receptor alpha and risk for cognitive impairment in postmenopausal women. Psychiatr Genet 16: 85-88.
115. Osterlund MK, Gustafsson JA, Keller E, Hurd YL. 2000. Estrogen receptor beta (ERbeta) messenger ribonucleic acid (mRNA) expression within the human forebrain: Distinct distribution pattern to ERalpha mRNA. J Clin Endocrinol Metab 85: 3840-3846.
116. Ottaviano YL, Issa JP, Parl FF, Smith HS, Baylin SB, Davidson NE. 1994. Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res 54: 2552-2555.
117. Packard MG, Teather LA. 1997a. Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. Neuroreport 8: 3009-3013.
118. Packard MG, Teather LA. 1997b. Posttraining estradiol injections enhance memory in ovariectomized rats: Cholinergic blockade and synergism. Neurobiol Learn Mem 68: 172-188.
119. Patrone C, Gianazza E, Santagati S, Agrati P, Maggi A. 1998. Divergent pathways regulate ligand-independent activation of ER alpha in SK-N-BE neuroblastoma and COS-1 renal carcinoma cells. Mol Endocrinol 12: 835-841.
120. Patrone C, Pollio G, Vegeto E, Enmark E, de Curtis I, Gustafsson JA, Maggi A. 2000. Estradiol induces differential neuronal phenotypes by activating estrogen receptor alpha or beta. Endocrinology 141: 1839-1845.
121. Pau CY, Pau KY, Spies HG. 1998. Putative estrogen receptor beta and alpha mRNA expression in male and female rhesus macaques. Mol Cell Endocrinol 146: 59-68.
122. Pawluski JL, Barakauskas VE, Galea LA. 2010. Pregnancy decreases oestrogen receptor alpha expression and pyknosis, but not cell proliferation or survival, in the hippocampus. J Neuroendocrinol 22: 248-257.
123. Perez SE, Chen EY, Mufson EJ. 2003. Distribution of estrogen receptor alpha and beta immunoreactive profiles in the postnatal rat brain. Brain Res Dev Brain Res 145: 117-139.
124. Perlman WR, Tomaskovic-Crook E, Montague DM, Webster MJ, Rubinow DR, Kleinman JE, Weickert CS. 2005. Alteration in estrogen receptor alpha mRNA levels in frontal cortex and hippocampus of patients with major mental illness. Biol Psychiatry 58: 812-824.
125. Petersen DN, Tkalcevic GT, Koza-Taylor PH, Turi TG, Brown TA. 1998. Identification of estrogen receptor beta2, a functional variant of estrogen receptor beta expressed in normal rat tissues. Endocrinology 139: 1082-1092.
126. Pettersson K, Delaunay F, Gustafsson JA. 2000. Estrogen receptor beta acts as a dominant regulator of estrogen signaling. Oncogene 19: 4970-4978.
127. Platano D, Fattoretti P, Balietti M, Giorgetti B, Casoli T, Di Stefano G, Bertoni-Freddari C, Aicardi G. 2008. Synaptic remodeling in hippocampal CA1 region of aged rats correlates with better memory performance in passive avoidance test. Rejuvenation Res 11: 341-348.
128. Post WS, Goldschmidt-Clermont PJ, Wilhide CC, Heldman AW, Sussman MS, Ouyang P, Milliken EE, Issa JP. 1999. Methylation of the estrogen receptor gene is associated with aging and atherosclerosis in the cardiovascular system. Cardiovasc Res 43: 985-991.
129. Prange-Kiel J, Wehrenberg U, Jarry H, Rune GM. 2003. Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus 13: 226-234.
130. Putz O, Schwartz CB, Kim S, LeBlanc GA, Cooper RL, Prins GS. 2001a. Neonatal low- and high-dose exposure to estradiol benzoate in the male rat: I. Effects on the prostate gland. Biol Reprod 65: 1496-1505.
131. Putz O, Schwartz CB, LeBlanc GA, Cooper RL, Prins GS. 2001b. Neonatal low- and high-dose exposure to estradiol benzoate in the male rat: II. Effects on male puberty and the reproductive tract. Biol Reprod 65: 1506-1517.
132. Rapp PR, Morrison JH, Roberts JA. 2003. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci 23: 5708-5714.
133. Register TC, Shively CA, Lewis CE. 1998. Expression of estrogen receptor alpha and beta transcripts in female monkey hippocampus and hypothalamus. Brain Res 788: 320-322.
134. Remage-Healey L, Maidment NT, Schlinger BA. 2008. Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11: 1327-1334.
135. Reul JM, de Kloet ER. 1985. Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology 117: 2505-2511.
136. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER. 2005. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307: 1625-1630.
137. Rissman EF. 2008. Roles of oestrogen receptors alpha and beta in behavioural neuroendocrinology: Beyond Yin/Yang. J Neuroendocrinol 20: 873-879.
138. Rissman EF, Heck AL, Leonard JE, Shupnik MA, Gustafsson JA. 2002. Disruption of estrogen receptor beta gene impairs spatial learning in female mice. Proc Natl Acad Sci USA 99: 3996-4001.
139. Rodgers SP, Bohacek J, Daniel JM. 2010. Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology 151: 1194-1203.
140. Rose'Meyer RB, Mellick AS, Garnham BG, Harrison GJ, Massa HM, Griffiths LR. 2003. The measurement of adenosine and estrogen receptor expression in rat brains following ovariectomy using quantitative PCR analysis. Brain Res Brain Res Protoc 11: 9-18.
141. Rozovsky I, Wei M, Morgan TE, Finch CE. 2005. Reversible age impairments in neurite outgrowth by manipulations of astrocytic GFAP. Neurobiol Aging 26: 705-715.
142. Rubin BS, Fox TO, Bridges RS. 1986. Estrogen binding in nuclear and cytosolic extracts from brain and pituitary of middle-aged female rats. Brain Res 383: 60-67.
143. Rune GM, Wehrenberg U, Prange-Kiel J, Zhou L, Adelmann G, Frotscher M. 2002. Estrogen up-regulates estrogen receptor alpha and synaptophysin in slice cultures of rat hippocampus. Neuroscience 113: 167-175.
144. Sandstrom NJ, Williams CL. 2001. Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115: 384-393.
145. Sandstrom NJ, Williams CL. 2004. Spatial memory retention is enhanced by acute and continuous estradiol replacement. Horm Behav 45: 128-135.
146. Savaskan E, Olivieri G, Meier F, Ravid R, Muller-Spahn F. 2001. Hippocampal estrogen beta-receptor immunoreactivity is increased in Alzheimer's disease. Brain Res 908: 113-119.
147. Sharma PK, Thakur MK. 2006. Expression of estrogen receptor (ER) alpha and beta in mouse cerebral cortex: Effect of age, sex and gonadal steroids. Neurobiol Aging 27: 880-887.
148. Sharrow KM, Kumar A, Foster TC. 2002. Calcineurin as a potential contributor in estradiol regulation of hippocampal synaptic function. Neuroscience 113: 89-97.
149. Sherwin BB. 2006. Estrogen and cognitive aging in women. Neuroscience 138: 1021-1026.
150. Shughrue PJ, Bushnell CD, Dorsa DM. 1992. Estrogen receptor messenger ribonucleic acid in female rat brain during the estrous cycle: A comparison with ovariectomized females and intact males. Endocrinology 131: 381-388.
151. Shughrue PJ, Lane MV, Merchenthaler I. 1997. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388: 507-525.
152. Simpkins JW, Singh M. 2004. Consortium for the Assessment of Research on Progestins and Estrogens (CARPE) Fort Worth, Texas August 1-3, 2003 J Womens Health (Larchmt) 13: 1165-1168.
153. Sinopoli KJ, Floresco SB, 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.
154. Smejkalova T, Woolley CS. 2010. Estradiol acutely potentiates hippocampal excitatory synaptic transmission through a presynaptic mechanism. J Neurosci 30: 16137-16148.
155. Smith CC, McMahon LL. 2005. Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J Neurosci 25: 7780-7791.
156. Smith CC, Vedder LC, McMahon LL. 2009. Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses. Psychoneuroendocrinology 34: S130-S142.
157. Snyder MA, Smejkalova T, Forlano PM, Woolley CS. 2010. Multiple ERbeta antisera label in ERbeta knockout and null mouse tissues. J Neurosci Methods 188: 226-234.
158. Spencer JL, Waters EM, Romeo RD, Wood GE, Milner TA, McEwen BS. 2008. Uncovering the mechanisms of estrogen effects on hippocampal function. Front Neuroendocrinol 29: 219-237.
159. Strom A, Hartman J, Foster JS, Kietz S, Wimalasena J, Gustafsson JA. 2004. Estrogen receptor beta inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proc Natl Acad Sci USA 101: 1566-1571.
160. Su J, Sripanidkulchai B, Sripanidkulchai K, Piyachaturawat P, Wara-Aswapati N. 2010. Effect of Curcuma comosa and estradiol on the spatial memory and hippocampal estrogen receptor in the post-training ovariectomized rats. J Nat Med 65: 57-62.
161. Szymczak S, Kalita K, Jaworski J, Mioduszewska B, Savonenko A, Markowska A, Merchenthaler I, Kaczmarek L. 2006. Increased estrogen receptor beta expression correlates with decreased spine formation in the rat hippocampus. Hippocampus 16: 453-463.
162. Talboom JS, Williams BJ, Baxley ER, West SG, Bimonte-Nelson HA. 2008. Higher levels of estradiol replacement correlate with better spatial memory in surgically menopausal young and middle-aged rats. Neurobiol Learn Mem 90: 155-163.
163. Tanapat P, Hastings NB, Gould E. 2005. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J Comp Neurol 481: 252-265.
164. Thakur MK, Sharma PK. 2007. Transcription of estrogen receptor alpha and beta in mouse cerebral cortex: Effect of age, sex, 17beta-estradiol and testosterone. Neurochem Int 50: 314-321.
165. Thomas P, Pang Y, Filardo EJ, Dong J. 2005. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146: 624-632.
166. Tohgi H, Utsugisawa K, Yamagata M, Yoshimura M. 1995. Effects of age on messenger RNA expression of glucocorticoid, thyroid hormone, androgen, and estrogen receptors in postmortem human hippocampus. Brain Res 700: 245-253.
167. Tomihara K, Soga T, Nomura M, Korach KS, Gustafsson JA, Pfaff DW, Ogawa S. 2009. Effect of ER-beta gene disruption on estrogenic regulation of anxiety in female mice. Physiol Behav 96: 300-306.
168. Tremblay GB, Tremblay A, Copeland NG, Gilbert DJ, Jenkins NA, Labrie F, Giguere V. 1997. Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta. Mol Endocrinol 11: 353-365.
169. vom Saal FS, Timms BG, Montano MM, Palanza P, Thayer KA, Nagel SC, Dhar MD, Ganjam VK, Parmigiani S, Welshons WV. 1997. Prostate enlargement in mice because of fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses. Proc Natl Acad Sci USA 94: 2056-2061.
170. Wade CB, Dorsa DM. 2003. Estrogen activation of cyclic adenosine 5'-monophosphate response element-mediated transcription requires the extracellularly regulated kinase/mitogen-activated protein kinase pathway. Endocrinology 144: 832-838.
171. Walf AA, Koonce C, Manley K, Frye CA. 2009. Proestrous compared to diestrous wildtype, but not estrogen receptor beta knockout, mice have better performance in the spontaneous alternation and object recognition tasks and reduced anxiety-like behavior in the elevated plus and mirror maze. Behav Brain Res 196: 254-260.
172. Wang JM, Irwin RW, Brinton RD. 2006. Activation of estrogen receptor alpha increases and estrogen receptor beta decreases apolipoprotein E expression in hippocampus in vitro and in vivo. Proc Natl Acad Sci USA 103: 16983-16988.
173. Wang AC, Hara Y, Janssen WG, Rapp PR, Morrison JH. 2010. Synaptic estrogen receptor-alpha levels in prefrontal cortex in female rhesus monkeys and their correlation with cognitive performance. JNeurosci 30: 12770-12776.
174. Waters EM, Mitterling K, Spencer JL, Mazid S, McEwen BS, Milner TA. 2009. Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res 1290: 1-11.
175. Waters EM, Yildirim M, Janssen WG, Lou WY, McEwen BS, Morrison JH, Milner TA. Estrogen and aging affect the synaptic distribution of estrogen receptor beta-immunoreactivity in the ca1 region of female rat hippocampus. Brain Res (in press).
176. Webb P, Valentine C, Nguyen P, Price RHJr., Marimuthu A, West BL, Baxter JD, Kushner PJ. 2003. ERbeta Binds N-CoR in the Presence of Estrogens via an LXXLL-like Motif in the N-CoR C-terminus. Nucl Recept 1: 4.
177. Welshons WV, Thayer KA, Judy BM, Taylor JA, Curran EM, vom Saal FS. 2003. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ Health Perspect 111: 994-1006.
178. Wide JK, Hanratty K, Ting J, Galea LA. 2004. High level estradiol impairs and low level estradiol facilitates non-spatial working memory. Behav Brain Res 155: 45-53.
179. Wilson ME, Westberry JM, Prewitt AK. 2008. Dynamic regulation of estrogen receptor-alpha gene expression in the brain: A role for promoter methylation? Front Neuroendocrinol 29: 375-385.
180. Windahl SH, Hollberg K, Vidal O, Gustafsson JA, Ohlsson C, Andersson G. 2001. Female estrogen receptor beta-/- mice are partially protected against age-related trabecular bone loss. J Bone Miner Res 16: 1388-1398.
181. Wong M, Moss RL. 1992. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J Neurosci 12: 3217-3225.
182. Woolley CS, McEwen BS. 1992. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12: 2549-2554.
183. Wu TW, Wang JM, Chen S, Brinton RD. 2005. 17Beta-estradiol induced Ca2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: A potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 135: 59-72.
184. Xu X, Zhang Z. 2006. Effects of estradiol benzoate on learning-memory behavior and synaptic structure in ovariectomized mice. Life Sci 79: 1553-1560.
185. Yaffe K, Lui LY, Grady D, Stone K, Morin P. 2002. Estrogen receptor 1 polymorphisms and risk of cognitive impairment in older women. Biol Psychiatry 51: 677-682.
186. Yaffe K, Lindquist K, Sen S, Cauley J, Ferrell R, Penninx B, Harris T, Li R, Cummings SR. 2009. Estrogen receptor genotype and risk of cognitive impairment in elders: Findings from the Health ABC study. Neurobiol Aging 30: 607-614.
187. Yang X, Ferguson AT, Nass SJ, Phillips DL, Butash KA, Wang SM, Herman JG, Davidson NE. 2000. Transcriptional activation of estrogen receptor alpha in human breast cancer cells by histone deacetylase inhibition. Cancer Res 60: 6890-6894.
188. Yang SH, Sarkar SN, Liu R, Perez EJ, Wang X, Wen Y, Yan LJ, Simpkins JW. 2009. Estrogen receptor beta as a mitochondrial vulnerability factor. J Biol Chem 284: 9540-9548.
189. Yi P, Bhagat S, Hilf R, Bambara RA, Muyan M. 2002a. Differences in the abilities of estrogen receptors to integrate activation functions are critical for subtype-specific transcriptional responses. Mol Endocrinol 16: 1810-1827.
190. Yi P, Driscoll MD, Huang J, Bhagat S, Hilf R, Bambara RA, Muyan M. 2002b. The effects of estrogen-responsive element- and ligand-induced structural changes on the recruitment of cofactors and transcriptional responses by ER alpha and ER beta. Mol Endocrinol 16: 674-693.
191. Yildirim M, Janssen WG, Tabori NE, Adams MM, Yuen GS, Akama KT, McEwen BS, Milner TA, 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.
192. Yun SH, Park KA, Kwon S, Woolley CS, Sullivan PM, Pasternak JF, Trommer BL. 2007. Estradiol enhances long term potentiation in hippocampal slices from aged apoE4-TR mice. Hippocampus 17: 1153-1157.
193. Zadran S, Qin Q, Bi X, Zadran H, Kim Y, Foy MR, Thompson R, Baudry M. 2009. 17-Beta-estradiol increases neuronal excitability through MAP kinase-induced calpain activation. Proc Natl Acad Sci USA 106: 21936-21941.
194. Zeier Z, Madorsky I, Xu Y, Ogle WO, Notterpek L, Foster TC. 2011. Gene expression in the hippocampus: Regionally specific effects of aging and caloric restriction. Mech Ageing Dev 132: 8-19.
195. Zhang QG, Raz L, Wang R, Han D, De Sevilla L, Yang F, Vadlamudi RK, Brann DW. 2009. Estrogen attenuates ischemic oxidative damage via an estrogen receptor alpha-mediated inhibition of NADPH oxidase activation. J Neurosci 29: 13823-13836.
196. Zhao L, Wu TW, Brinton RD. 2004. Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Res 1010: 22-34.
197. Zhao L, Brinton RD. 2007. Estrogen receptor alpha and beta differentially regulate intracellular Ca(2+) dynamics leading to ERK phosphorylation and estrogen neuroprotection in hippocampal neurons. Brain Res 1172: 48-59.
198. Zhao C, Matthews J, Tujague M, Wan J, Strom A, Toresson G, Lam EW, Cheng G, Gustafsson JA, Dahlman-Wright K. 2007. Estrogen receptor beta2 negatively regulates the transactivation of estrogen receptor alpha in human breast cancer cells. Cancer Res 67: 3955-3962.
199. Zhou L, Fester L, von Blittersdorff B, Hassu B, Nogens H, Prange-Kiel J, Jarry H, Wegscheider K, Rune GM. 2010. Aromatase inhibitors induce spine synapse loss in the hippocampus of ovariectomized mice. Endocrinology 151: 1153-1160.
200. Zurkovsky L, Brown SL, Boyd SE, Fell JA, Korol DL. 2007. Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscience 144: 26-37.