Molecular mechanisms underlying the memory-enhancing effects of estradiol

Hormones and Behavior

Volumn 74, Issue , 2015, Pages 4-18

  Frick, Karyn M ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Cell signaling; DNA methylation; Epigenetic; ERK; Estrogen; Estrogen receptor; GPER; Hippocampus; Histone acetylation; MTOR

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; ESTRADIOL; ESTROGEN RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; PERFORMANCE ENHANCING SUBSTANCE;

ARTICLE; EPIGENETICS; GENETIC MANIPULATION; HIPPOCAMPUS; HORMONE SYNTHESIS; HUMAN; LONG TERM POTENTIATION; MEMORY; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; FEMALE; GENETIC EPIGENESIS; GENETICS; METABOLISM;

ANIMALS; EPIGENESIS, GENETIC; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; HIPPOCAMPUS; HUMANS; MEMORY; PERFORMANCE-ENHANCING SUBSTANCES; SIGNAL TRANSDUCTION;

EID: 84941747846     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.05.001     Document Type: Article

References (188)

1. Adams J.P., Sweatt J.D. Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu. Rev. Pharmacol. Toxicol. 2002, 42:135-163.
2. Aenlle K.K., Foster T.C. Aging alters the expression of genes for neuroprotection and synaptic function following acute estradiol treatment. Hippocampus 2010, 20:1047-1060.
3. Aenlle K.K., Kumar A., Cui L., Jackson T.C., Foster T.C. Estrogen effects on cognition and hippocampal transcription in middle-aged mice. Neurobiol. Aging 2009, 30:932-945.
4. Akama K.T., McEwen B.S. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J. Neurosci. 2003, 23:2333-2339.
5. Akama K.T., Thompson L.I., Milner T.A., McEwen B.S. 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. 2013, 288:6438-6450.
6. Atkins C.M., Selcher J.C., Petraitis J.J., Trzaskos J.M., Sweatt J.D. The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1998, 1:602-609.
7. Azcoitia I., Sierra A., Veiga S., Garcia-Segura L.M. Aromatase expression by reactive astroglia is neuroprotective. Ann. N. Y. Acad. Sci. 2003, 1007:298-305.
8. Bailey D.J., Ma C., Soma K.K., Saldanha C.J. Inhibition of hippocampal aromatization impairs spatial memory performance in a male songbird. Endocrinology 2013, 154:4707-4714.
9. Bean L.A., Ianov L., Foster T.C. Estrogen receptors, the hippocampus, and memory. Neuroscientist 2014, 20:534-545.
10. Bekinschtein P., Katche C., Slipczuk L.N., Igaz L.M., Cammarota M., Izquierdo I., Medina J.H. mTOR signaling in the hippocampus is necessary for memory formation. Neurobiol. Learn. Mem. 2007, 87:303-307.
11. Bekinschtein P., Cammarota M., Medina J.H. BDNF and memory processing. Neuropharmacology 2014, 76(Pt C):677-683.
12. Bi R., Broutman G., Foy M.R., Thompson R.F., Baudry M. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:3602-3607.
13. Bi R., Foy M.R., Vouimba R.-M., Thompson R.F., Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13391-13395.
14. Blum S., Moore A.N., Adams F., Dash P.K. A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory. J. Neurosci. 1999, 19:3535-3544.
15. Bologa C.G., Revankar C.M., Young S.M., Edwards B.S., Arterburn J.B., Kiselyov A.S., Parker M.A., Tkachenko S.E., Savchuck N.P., Sklar L.A., Oprea T.I., Prossnitz E.R. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol. 2006, 2:207-212.
16. Boulware M.I., Weick J.P., Becklund B.R., Kuo S.P., Groth R.D., Mermelstein P.G. Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J. Neurosci. 2005, 25:5066-5078.
17. Boulware M.I., Heisler J.D., Frick K.M. The memory-enhancing effects of hippocampal estrogen receptor activation involve metabotropic glutamate receptor signaling. J. Neurosci. 2013, 33:15184-15194.
18. Bozon B., Kelly A., Josselyn S.A., Silva A.J., Davis S., Laroche S. MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:805-814.
19. Brailoiu E., Dun S.L., Brailoiu G.C., Mizuo K., Sklar L.A., Oprea T.I., Prossnitz E.R., Dun N.J. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 2007, 311-321.
20. Brinton R.D. Cellular and molecular mechanisms of estrogen regulation of memory function and neuroprotection against Alzheimer's disease: recent insights and remaining challenges. Learn. Mem. 2001, 8:121-133.
21. Cammalleri M., Lütjens R., Berton F., King A.R., Simpson C., Francesconi W., Sanna P.P. Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:14368-14373.
22. Carrer H.F., Araque A., Buño W. Estradiol regulates the slow Ca2+-activated K+ current in hippocampal pyramidal neurons. J. Neurosci. 2003, 23:6338-6344.
23. Chahrour M., Jung S.Y., Shaw C., Zhao X., Wong S.T.C., Qin J., Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and repressed transcription. Science 2008, 320:1224-1229.
24. Chan M., Chow C., Hamson D.K., Lieblich S.E., Galea L.A. Effects of chronic oestradiol, progesterone and medroxyprogesterone acetate on hippocampal neurogenesis and adrenal mass in adult female rats. J. Neuroendocrinol. 2014, 26:386-399.
25. Choleris E., Clipperton-Allen A.E., Phan A., Valsecchi P., Kavaliers M. Estrogenic involvement in social learning, social recognition and pathogen avoidance. Front. Neuroendocrinol. 2012, 33:140-159.
26. Conrad C.D., Bimonte-Nelson H.A. Impact of the hypothalamic-pituitary-adrenal/ gonadal axes on trajectory of age-related cognitive decline. Prog. Brain Res. 2010, 182:31-76.
27. Daniel J.M. Effects of oestrogen on cognition: what have we learned from basic research?. J. Neuroendocrinol. 2006, 18:787-795.
28. Dash P.K., Orsi S.A., Moore A.N. Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-mammalian target of rapamycin pathway. J. Neurosci. 2006, 26:8048-8056.
29. Day J.J., Sweatt J.D. DNA methylation and memory formation. Nat. Neurosci. 2010, 11:1319-1323.
30. Day J.J., Sweatt J.D. Cognitive neuroepigenetics: a role for epigenetic mechanisms in learning and memory. Neurobiol. Learn. Mem. 2011, 96:2-12.
31. de Castilhos J., Forti C.D., Achaval M., Rasia-Filho A.A. Dendritic spine density of posterodorsal medial amygdala neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: a Golgi study. Brain Res. 2008, 1240:73-81.
32. Dennis M.K., Burai R., Ramesh C., Petrie W.K., Alcon S.N., Nayak T.K., Bologa C.G., Leitao A., Brailoiu E., Deliu E., Dun N.J., Sklar L.A., Hathaway H.J., Arterburn J.B., Oprea T.I., Prossnitz E.R. In vivo effects of a GPR30 antagonist. Nat. Chem. Biol. 2009, 5:421-427.
33. Dennis M.K., Field A.S., Burai R., Ramesh C., Petrie W.K., Bologa C.G., Oprea T.I., Yamaguchi Y., Hayashi S.-I., Sklar L.A., Hathaway H.J., Arterburn J.B., Prossnitz E.R. Identification of a GPER/GPR30 antagonist with improved estrogen receptor counterselectivity. J. Steroid Biochem. Mol. Biol. 2011, 127:358-366.
34. Ervin K.S., Phan A., Gabor C.S., Choleris E. Rapid oestrogenic regulation of social and nonsocial learning. J. Neuroendocrinol. 2013, 25:1116-1132.
35. Fan L., Zhao Z., Orr P.T., Chambers C.H., Lewis M.C., Frick K.M. Estradiol-induced object memory consolidation in middle-aged female mice requires dorsal hippocampal extracellular signal-regulated kinase and phosphatidylinositol 3-kinase activation. J. Neurosci. 2010, 30:4390-4400.
36. Fernandez S.M., Lewis M.C., Pechenino A.S., Harburger L.L., Orr P.T., Gresack J.E., Schafe G.E., Frick K.M. Estradiol-induced enhancement of object memory consolidation involves hippocampal ERK activation and membrane-bound estrogen receptors. J. Neurosci. 2008, 28:8660-8667.
37. Filardo E.J., Quinn J.A., Bland K.I., Frackelton A.R. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 2000, 14:1649-1660.
38. Fischer A., Sananbenesi F., Mungenast A., Tsai L.H. Targeting the correct HDAC(s) to treat cognitive disorders. Trends Pharmacol. Sci. 2010, 31:605-617.
39. Fortress A.M., Frick K.M. Epigenetic regulation of estrogen-dependent memory. Front. Neuroendocrinol. 2014, 35:530-549.
40. Fortress A.M., Fan L., Orr P.T., Zhao Z., Frick K.M. Estradiol-induced object recognition memory consolidation is dependent on activation on mTOR signaling in the dorsal hippocampus. Learn. Mem. 2013, 20:147-155.
41. Fortress A.M., Kim J., Poole R.L., Gould T.J., Frick K.M. 17β-Estradiol regulates histone alterations associated with memory consolidation and increases Bdnf promoter acetylation in middle-aged female mice. Learn. Mem. 2014, 21:457-467.
42. Foster T.C., Rani A., Kumar A., Cui L., Semple-Rowland S.L. Viral vector-mediated delivery of estrogen receptor-alpha to the hippocampus improves spatial learning in estrogen receptor-alpha knockout mice. Mol. Ther. 2008, 16:1587-1593.
43. Foy M.R., Xu J., Xie X., Brinton R.D., Thompson R.F., Berger T.W. 17ß-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J. Neurophysiol. 1999, 81:925-929.
44. Frick K.M. Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here?. Horm. Behav. 2009, 55:2-23.
45. Frick K.M. Building a better hormone therapy?: How understanding the rapid effects of sex steroid hormones could lead to novel therapeutics for age-related memory decline. Behav. Neurosci. 2012, 126:29-53.
46. Frick K.M. Epigenetics, oestradiol and hippocampal memory consolidation. J. Neuroendocrinol. 2013, 25:1151-1162.
47. Frick K.M., Fernandez S.M., Bennett J.C., Prange-Kiel J., MacLusky N.J., Leranth C. Behavioral training interferes with the ability of gonadal hormones to increase CA1 spine synapse density in ovariectomized female rats. Eur. J. Neurosci. 2004, 19:3026-3032.
48. Frick K.M., Fernandez S.M., Harburger L.L. A new approach to understanding the molecular mechanisms through which estrogens affect cognition. Biochim. Biophys. Acta Gen. Subj. 2010, 1800:1045-1055.
49. Frye C.A., Duffy C.K., Walf A.A. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol. Learn. Mem. 2007, 88:208-216.
50. Fuchikami M., Yamamoto S., Morinobu S., Takei S., Yamawaki S. Epigenetic regulation of BDNF gene in response to stress. Psychiatry Investig. 2010, 7:251-256.
51. Fugger H.N., Foster T.C., Gustafsson J.-A., Rissman E.F. Novel effects of estradiol and estrogen receptor α and β on cognitive function. Brain Res. 2000, 883:258-264.
52. Fukata Y., Fukata M. Protein palmitoylation in neuronal development and synaptic plasticity. Nat. Rev. Neurosci. 2010, 11:161-175.
53. Galea L.A.M., Wide J.K., Paine T.A., Holmes M.M., Ormerod B.K., Floresco S.B. High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory. Behav. Brain Res. 2001, 126:115-126.
54. Galea L.A., Wainwright S.R., Roes M.M., Duarte-Guterman P., Chow C., Hamson D.K. Sex, hormones, and neurogenesis in the hippocampus: hormonal modulation of neurogenesis and potential functional implications. J. Neuroendocrinol. 2013, 25:1039-1061.
55. Garcia-Segura L.M., Wozniak A., Azcoitia I., Rodriguez J.R., Hutchison R.E., Hutchison J.B. Aromatase expression by astrocytes after brain injury: implications for local estrogen formation in brain repair. Neuroscience 1999, 89:567-578.
56. Garcia-Segura L.M., Azcoitia I., DonCarlos L.L. Neuroprotection by estradiol. Prog. Neurobiol. 2001, 63.
57. Gibbs R.B. Estrogen therapy and cognition: a review of the cholinergic hypothesis. Endocr. Rev. 2010, 31:224-253.
58. Glasper E.R., Gould E. Sexual experience restores age-related decline in adult neurogenesis and hippocampal function. Hippocampus 2013, 23:303-312.
59. Gould E., Woolley C.S., Frankfurt M., McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 1990, 10:1286-1291.
60. Gräff J., Tsai L.H. Histone acetylation: molecular mnemonics on the chromatin. Nat. Rev. Neurosci. 2013, 14:97-111.
61. Graham B.M., Milad M.R. Blockade of estrogen by hormonal contraceptives impairs fear extinction in female rats and women. Biol. Psychiatry 2013, 73:371-378.
62. Graham B.M., Milad M.R. Inhibition of estradiol synthesis impairs fear extinction in male rats. Learn. Mem. 2014, 21:347-350.
63. Gresack J.E., Frick K.M. Post-training estrogen enhances spatial and object memory consolidation in female mice. Pharmacol. Biochem. Behav. 2006, 84:112-119.
64. Gresack J.E., Kerr K.M., Frick K.M. Life-long environmental enrichment differentially affects the mnemonic response to estrogen in young, middle-aged, and aged female mice. Neurobiol. Learn. Mem. 2007, 88:393-408.
65. Gu Q., Moss R.L. Novel mechanism for non-genomic action of 17 beta-oestradiol on kainate-induced currents in isolated rat CA1 hippocampal neurones. J. Physiol. 1998, 506:745-754.
66. Guan J.S., Haggarty S.J., Giacometti E., Dannenberg J.H., Joseph N., Gao J., Nieland T.J., Zhou Y., Wang X., Mazitschek R., Bradner J.E., DePinho R.A., Jaenisch R., Tsai L.H. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009, 459:55-60.
67. Hammond R., Mauk R., Ninaci D., Nelson D., Gibbs R.B. Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm. Behav. 2009, 56:309-314.
68. Hammond R., Nelson D., Kline E., Gibbs R.B. Chronic treatment with a GPR30 antagonist impairs acquisition of a spatial learning task in young female rats. Horm. Behav. 2012, 62:367-374.
69. Han X., Aenlle K.K., Bean L.A., Rani A., Semple-Rowland S.L., Kumar A., Foster T.C. Role of estrogen receptor α and β in preserving hippocampal function during aging. J. Neurosci. 2013, 33:2671-2683.
70. Hao J., Rapp P.R., Leffler A.E., Leffler S.R., Janssen W.G., Lou W., McKay H., Roberts J.A., Wearne S.L., Hof P.R., Morrison J.H. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J. Neurosci. 2006, 26:2571-2578.
71. Hasegawa Y., Hojo Y., Kojima H., Ikeda M., Hotta K., Sato R., Ooishi Y., Yoshiya M., Chung B.-C., Yamazaki T., Kawato S. Estradiol rapidly modulates synaptic plasticity of hippocampal neurons: involvement of kinase networks. Brain Res. 2015, (in press). 10.1016/j.brainres.2014.1012.1056.
72. Heldt S.A., Stanek L., Chhatwal J.P., Ressler K.J. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol. Psychiatry 2007, 12:656-670.
73. Hoeffer C.A., Klann E. mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci. 2010, 33:67-75.
74. Hojo Y., Hattori T.A., Enami T., Furukawa A., Suzuki K., Ishii H.T., Mukai H., Morrison J.H., Janssen W.G., Kominami S., Harada N., Kimoto T., Kawato S. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:865-870.
75. Hojo Y., Higo S., Ishii H., Ooishi Y., Mukai H., Murakami G., Kominami T., Kimoto T., Honma S., Poirer D., Kawato S. Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinology 2009, 150:5106-5112.
76. Horwood J.M., Dufour F., Laroche S., Davis S. Signaling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur. J. Neurosci. 2006, 23:3375-3384.
77. Huang Y., Huang Y.L., Zhang S., Zhu Y.C., Yao T. Estradiol acutely attenuates glutamate-induced calcium overload in primarily cultured rat hippocampal neurons through a membrane receptor-dependent mechanism. Brain Res. 2004, 1026:254-260.
78. Ikeda T., Makino Y., Yamada K. 17α-estradiol is generated locally in the male rat brain and can regulate GAD65 expression and anxiety. Neuropharmacology 2015, 90:9-14.
79. Inagaki T., Frankfurt M., Luine V. Estrogen-induced memory enhancements are blocked by acute bisphenol A in adult female rats: role of dendritic spines. Endocrinology 2012, 1534:3357-3367.
80. Jacome L.F., Gautreaux C., Inagaki T., Mohan G., Alves S., Lubbers L.S., Luine V. Estradiol and ERβ agonists enhance recognition memory, and DPN, an ERβ agonist, alters brain monoamines. Neurobiol. Learn. Mem. 2010, 94:488-498.
81. Jarome T.J., Lubin F.D. Epigenetic mechanisms of memory formation and reconsolidation. Neurobiol. Learn. Mem. 2014, 115:116-127.
82. Kajta M., Rzemieniec J., Litwa E., Lason W., Lenartowicz M., Krzeptowski W., Wojtowicz A.K. The key involvement of estrogen receptor β and G-protein-coupled receptor 30 in the neuroprotective action of daidzein. Neuroscience 2013, 238:345-360.
83. Kato A., Hojo Y., Higo S., Komatsuzaki Y., Murakami G., Yoshino H., Uebayashi M., Kawato S. Female hippocampal estrogens have a significant correlation with cyclic fluctuation of hippocampal spines. Front. Neural Circuits 2013, 7:149.
84. Kelly A., Lynch M.A. Long-term potentiation in dentate gyrus of the rat is inhibited by the phosphoinositide 3-kinase inhibitor, wortmannin. Neuropharmacology 2000, 39:643-651.
85. Kelly A., Laroche S., Davis S. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J. Neurosci. 2003, 12:5354-5360.
86. Kessler R.C., Chiu W.T., Demler O., Merikangas K.R., Walters E.E. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 2005, 62:617-627.
87. Khan M.M., Dhandapani K.M., Zhang Q.G., Brann D.W. Estrogen regulation of spine density and excitatory synapses in rat prefrontal and somatosensory cerebral cortex. Steroids 2013, 78:614-623.
88. Kim J., Boulware M.I., Frick K.M. Role of G-protein-coupled estrogen receptor (GPER/GPR30) in hippocampal memory and cell signaling in female mice. Soc Neurosci Abstr, Poster 376.305 2013.
89. Kim J., Szinte J.S., Frick K.M. Distinct effects of estrogen receptor inhibition on novel object recognition and spatial memory consolidation in ovariectomized mice. Soc Neurosci Abstr Poster 451.11 2014.
90. Klann E., Dever T.E. Biochemical mechanisms for translational regulation in synaptic plasticity. Nat. Rev. Neurosci. 2004, 5:931-942.
91. Kramár E.A., Chen L.Y., Brandon N.J., Rex C.S., Liu F., Gall C.M., Lynch G. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J. Neurosci. 2009, 29:12982-12993.
92. Kretz O., Fester L., Wehrenberg U., Zhou L., Brauckmann S., Zhao S., Prange-Kiel J., Naumann T., Jarry H., Frotscher M., Rune G.M. Hippocampal synapses depend on hippocampal estrogen synthesis. J. Neurosci. 2004, 24:5913-5921.
93. Kumar A., Foster T.C. 17β-estradiol benzoate decreases the AHP amplitude in CA1 pyramidal neurons. J. Neurophysiol. 2002, 88:621-626.
94. Kuroki Y., Fukushima K., Kanda Y., Mizuno K., Watanabe Y. Putative membrane-bound estrogen receptors possibly stimulate mitogen-activated protein kinase in the rat hippocampus. Eur. J. Pharmacol. 2000, 400:205-209.
95. Langer G., Bader B., Meoli L., Isensee J., Delbeck M., Noppinger P.R., Otto C. A critical review of fundamental controversies in the field of GPR30 research. Steroids 2010, 75:603-610.
96. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
97. Levenson J.M., O'Riordan K.J., Brown K.D., Trinh M.A., Molfese D.L., Sweatt J.D. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 2004, 279:40545-40559.
98. Levin E.R. Cellular functions of the plasma membrane estrogen receptor. Trends Endocrinol. Metab. 1999, 10:374-377.
99. Levin E.R. G protein-coupled receptor 30: estrogen receptor or collaborator?. Endocrinology 2009, 150:1563-1565.
100. Lewis M.C., Kerr K.M., Orr P.T., Frick K.M. Estradiol-induced enhancement of object memory consolidation involves NMDA receptors and protein kinase A in the dorsal hippocampus of female C57BL/6 mice. Behav. Neurosci. 2008, 122:716-721.
101. Lin C.H., Yeh S.H., Lin C.H., Lu K.T., Leu T.H., Chang W.C., Gean P.W. A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 2001, 31:841-851.
102. Liu F., Day M., Muniz L.C., Bitran D., Arias R., Revilla-Sanchez R., Grauer S., Zhang G., Kelley C., Pulito V., Sung A., Mervis R.F., Navarra R., Hirst W.D., Reinhart P.H., Marquis K.L., Moss S.J., Pangalos M.N., Brandon N.J. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat. Neurosci. 2008, 11:334-343.
103. Lubin F.D., Roth T.L., Sweatt J.D. Epigenetic regulation of bdnf gene transcription in the consolidation of fear memory. J. Neurosci. 2008, 28:10576-10586.
104. Luine V. Estradiol and cognitive function: past, present and future. Horm. Behav. 2014, 66:602-618.
105. Luine V. Recognition memory tasks in neuroendocrine research. Behav. Brain Res. 2015, 285:158-164.
106. Luine V.N., Frankfurt M. Estrogens facilitate memory processing through membrane mediated mechanisms and alterations in spine density. Front. Neuroendocrinol. 2012, 33:388-402.
107. Luine V., Rodriguez M. Effects of estradiol on radial arm maze performance of young and aged rats. Behav. Neural Biol. 1994, 62:230-236.
108. Luine V.N., Jacome L.F., MacLusky N.J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 2003, 144:2836-2844.
109. MacLusky N.J., Luine V.N., Hajszan T., Leranth C. The 17alpha and 17beta isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 2005, 146:287-293.
110. Manella P., Brinton R.D. 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. 2006, 26:9437-9447.
111. Marriott L.K., Hauss-Wegrzyniak B., Benton R.S., Vraniak P.D., Wenk G.L. Long-term estrogen therapy worsens the behavioral and neuropathological consequences of chronic brain inflammation. Behav. Neurosci. 2002, 116:902-911.
112. McClure R., Barha C.K., Galea L.A. 17β-Estradiol, but not estrone, increases hippocampal neurogenesis and activation of new granule neurons in response to spatial memory in adult female rats. Horm. Behav. 2013, 63:144-157.
113. McQuown S.C., Barrett R.M., Matheos D.P., Post R.J., Rogge G.A., Alenghat T., Mullican S.E., Jones S., Rusche J.R., Lazar M.A., Wood M.A. HDAC3 is a critical negative regulator of long-term memory formation. J. Neurosci. 2011, 31:764-774.
114. Meinhard N., Kessing L.V., Vinberg M. The role of estrogen in bipolar disorder, a review. Nord. J. Psychiatry 2014, 68:81-87.
115. Meitzen J., Luoma J.I., Boulware M.I., Hedges V.L., Peterson B.M., Tuomela K., Britson K.A., Mermelstein P.G. Palmitoylation of estrogen receptors is essential for neuronal membrane signaling. Neuroendocrinology 2013, 154:4293-4304.
116. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., Katzenellenbogen J.A. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J. Med. Chem. 2001, 44:4230-4251.
117. Milad M.R., Zeidan M.A., Contero A., Pitman R.K., Klibanski A., Rauch S.L., Goldstein J.M. The influence of gonadal hormones on conditioned fear extinction in healthy humans. Neuroscience 2010, 168:652-658.
118. Miller C.A., Sweatt J.D. Covalent modification of DNA regulates memory formation. Neuron 2007, 53:857-869.
119. Miller C.A., Campbell S.L., Sweatt J.D. DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiol. Learn. Mem. 2008, 89:599-603.
120. Milner T.A., McEwen B.S., Hayashi S., Li C.J., Reagan L.P., Alves S.E. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J. Comp. Neurol. 2001, 429:355-371.
121. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 2005, 491:81-95.
122. Mitra S.W., Hoskin E., Yudkovitz J., Pear L., Wilkinson H.A., Hayashi S., Pfaff D.W., Ogawa S., Rohrer S.P., Schaeffer J.M., McEwen B.S., Alves S.E. Immunolocalization of estrogen receptor β in the mouse brain: comparison with estrogen receptor α. Endocrinology 2003, 144:2055-2067.
123. Mitterling K.L., Spencer J.L., Shenoy S., McCarthy K., Waters E.M., McEwen B.S., Milner T.A. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J. Comp. Neurol. 2010, 518:2729-2743.
124. Murphy D.D., Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J. Neurosci. 1996, 16:4059-4068.
125. Myskiw J.C., Rossato J.I., Bevilaqua L.R., Medina J.H., Izquierdo I., Cammarota M. On the participation of mTOR in recognition memory. Neurobiol. Learn. Mem. 2008, 89:338-351.
126. Nguyen P.V., Woo N.H. Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog. Neurobiol. 2003, 71:401-437.
127. Nilsen J., Brinton R.D. Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10506-10511.
128. Noriega N.C., Eghlidi D.H., Garyfallou V.F., Kohama S.G., Kryger S.G., Urbanski H.F. Influence of 17beta-estradiol and progesterone on GABAergic gene expression in the arcuate nucleus, amygdala and hippocampus of the rhesus macaque. Brain Res. 2010, 1307:28-42.
129. Ormerod B.K., Lee T.T., Galea L.A. Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rat. J. Neurobiol. 2003, 55:247-260.
130. Packard M.G., Teather L.A. Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. NeuroReport 1997, 8:3009-3013.
131. Packard M.G., Teather L.A. Posttraining estradiol injections enhance memory in ovariectomized rats: Cholinergic blockade and synergism. Neurobiol. Learn. Mem. 1997, 68:172-188.
132. Packard M.G., Kohlmaier J.R., Alexander G.M. Posttraining intrahippocampal estradiol injections enhance spatial memory in male rats: interaction with cholinergic systems. Behav. Neurosci. 1996, 110:626-632.
133. Parsons R.G., Gafford G.M., Helmstetter F.J. Translational control via the mammalian target of rapamycin pathway is critical for the formation and stability of long-term fear memory in amygdala neurons. J. Neurosci. 2006, 26:12977-12983.
134. Pechenino A.S., Frick K.M. The effects of acute 17β-estradiol treatment on gene expression in the young female mouse hippocampus. Neurobiol. Learn. Mem. 2009, 91:315-322.
135. Peixoto L., Abel T. The role of histone acetylation in memory formation and cognitive impairments. Neuropsychopharmacology 2013, 38:62-76.
136. Pereira L.M., Bastos C.P., de Souza J.M., Ribeiro F.M., Pereira G.S. Estradiol enhances object recognition memory in Swiss female mice by activating hippocampal estrogen receptor α. Neurobiol. Learn. Mem. 2014, 114:1-9.
137. Perovic M., Tesic V., Mladenovic Djordjevic A., Smiljanic K., Loncarevic-Vasiljkovic N., Ruzdijic S., Kanazir S. BDNF transcripts, proBDNF and proNGF, in the cortex and hippocampus throughout the life span of the rat. Age (Dordr.) 2013, 35:2057-2070.
138. Phan A., Lancaster K.E., Armstrong J.N., MacLusky N.J., Choleris E. Rapid effects of estrogen receptor α and β selective agonists on learning and dendritic spines in female mice. Endocrinology 2011, 152:1492-1502.
139. Prange-Kiel J., Fester L., Zhou L., Lauke H., Carrétero J., Rune G.M. Inhibition of hippocampal estrogen synthesis causes region-specific downregulation of synaptic protein expression in hippocampal neurons. Hippocampus 2006, 16:464-471.
140. Qiu J., Bosch M.A., Tobias S.C., Grandy D.K., Scanlan T.S., Ronnekleiv O.K., Kelly M.J. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J. Neurosci. 2003, 23:9529-9540.
141. Remage-Healey L., Maidment N.T., Schlinger B.A. Forebrain steroid levels fluctuate rapidly during social interactions. Nat. Neurosci. 2008, 11:1327-1334.
142. Richter J.D., Klann E. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev. 2009, 23:1-11.
143. Rossouw J.E., Anderson G.L., Prentice R.L., LaCroix A.Z., Kooperbert C., Stefanick M.L., Jackson R.D., Beresford S.A., Howard B.V., Johnson K.C., Kotchen J.M., Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women. JAMA 2002, 288:321-333.
144. Ruiz-Palmero I., Hernando M., Garcia-Segura L.M., Arevalo M.-A. G protein-coupled estrogen receptor is required for the neuritogenic mechanism of 17β-estradiol in developing hippocampal neurons. Mol. Cell. Endocrinol. 2013, 372:105-115.
145. Saenz C., Dominguez R., de Lacalle S. Estrogen contributes to structural recovery after a lesion. Neurosci. Lett. 2006, 392:198-201.
146. Segal M., Murphy D. Estradiol induces formation of dendritic spines in hippocampal neurons: functional correlates. Horm. Behav. 2001, 40:156-159.
147. Sheldahl L.C., Shapiro R.A., Bryant D.N., Koerner I.P., Dorsa D.M. Estrogen induced rapid translocation of estrogen receptor β, but not estrogen receptor α, to the neuronal plasma membrane. Neuroscience 2008, 153:751-761.
148. Shingo A.S., Kito S. Estradiol induces PKA activation through the putative membrane receptor in the living hippocampal neuron. J. Neural Transm. 2005, 112:1469-1473.
149. Shughrue P.J., Merchenthaler I. Evidence for novel estrogen binding sites in the rat hippocampus. Neuroscience 2000, 99:605-612.
150. Shughrue P., Scrimo P., Lane M., Askew R., Merchenthaler I. The distribution of estrogen receptor-ß mRNA in forebrain regions of the estrogen receptor-α knockout mouse. Endocrinology 1997, 138:5649-5652.
151. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-α and -ß mRNA in the rat central nervous system. J. Comp. Neurol. 1997, 388:507-525.
152. Smith C.C., McMahon L.L. 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. 2005, 26:8517-8522.
153. Srivastava D.P., Woolfrey K.M., Jones K.A., Shum C.Y., Lash L.L., Swanson G.T., Penzes P. Rapid enhancement of two-step wiring plasticity by estrogen and NMDA receptor activity. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14650-14655.
154. Stauffer S.R., Coletta C.J., Tedesco R., Nishiguchi G., Carlson K., Sun J., Katzenellenbogen B.S., Katzenellenbogen J.A. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J. Med. Chem. 2000, 43:4934-4947.
155. Sweatt J.D. Experience-dependent epigenetic modifications in the central nervous system. Biol. Psychiatry 2009, 65:191-197.
156. Tanapat P., Hastings N.B., Reeves A.J., Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 1999, 19:5792-5801.
157. Tang H., Zhang Q., Yang L., Dong Y., Khan M., Yang F., Brann D.W., Wang R. GPR30 mediates estrogen rapid signaling and neuroprotection. Mol. Cell. Endocrinol. 2014, 387:52-58.
158. Thomas P., Pang Y., Filardo E.J., Dong J. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 2005, 146:624-632.
159. Toran-Allerand C.D., Guan X., MacLusky N.J., Horvath T.L., Diano S., Singh M., Connolly E.S.J., Nethrapalli I.S., Tinnikov A.A. ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J. Neurosci. 2002, 22:8391-8401.
160. Tsokas P., Grace E.A., Chan P., Ma T., Sealfon S.C., Iyengar R., Landau E.M., Blitzer R.D. Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J. Neurosci. 2005, 25:5833-5843.
161. Tuscher J.J., Szinte J.S., Starrett J.R., Krentzel A.A., Remage-Healey L., Frick K.M. Hippocampally-synthesized estrogens are essential for spatial memory consolidation in female mice. Soc Neurosci Abstr, Poster 376.307 2013.
162. Tuscher J.J., Fortress A.M., Kim J., Frick K.M. Regulation of object recognition and object placement by ovarian sex steroid hormones. Behav. Brain Res. 2015, 285:140-157.
163. Vedder L.C., Smith C.C., Flannigan A.E., McMahon L.L. Estradiol-induced increase in novel object recognition requires hippocampal NR2B-containing NMDA receptors. Hippocampus 2013, 23:108-115.
164. Vierk R., Glassmeier G., Zhou L., Brandt N., Fester L., Dudzinski D., Wilkars W., Bender R.A., Lewerenz M., Gloger S., Graser L., Schwarz J., Rune G.M. Aromatase inhibition abolishes LTP generation in female but not in male mice. J. Neurosci. 2012, 32:8116-8126.
165. Wade C.B., Dorsa D.M. Estrogen activation of cyclic adenosine 5'-monophosphate response element-mediated transcription requires the extracellularly regulated kinase/mitogen-activated protein kinase pathway. Endocrinology 2003, 144:832-838.
166. Wade C.B., Robinson S., Shapiro R.A., Dorsa D.M. Estrogen receptor (ER)α and ERß exhibit unique pharmacologic properties when coupled to activation of the mitogen-activated protein kinase pathway. Endocrinology 2001, 142:2336-2342.
167. Wakeling A.E., Bowler J. ICI 182,780, a new antioestrogen with clinical potential. J. Steroid Biochem. Mol. Biol. 1992, 43:173-177.
168. Walf A.A., Rhodes M.E., Frye C.A. Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol. Learn. Mem. 2006, 86:35-46.
169. Walf A.A., Koonce C.J., Frye C.A. 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. 2008, 89:513-521.
170. Waters E.M., Yildirim M., Janssen W.G., Lou W.Y., McEwen B.S., Morrison J.H., Milner T.A. Estrogen and aging affect the synaptic distribution of estrogen receptor beta-immunoreactivity in the CA1 region of female rat hippocampus. Brain Res. 2011, 1379:86-97.
171. Waters E.M., Thompson L.I., Patel P., Gonzales A.D., Ye H.Z., Filardo E.J., Clegg D.J., Gorecka J., Akama K.T., McEwen B.S., Milner T.A. G-protein-coupled estrogen receptor 1 is anatomically positioned to modulate synaptic plasticity in the mouse hippocampus. J. Neurosci. 2015, 35:2384-2397.
172. Watters J.J., Campbell J.S., Cunningham M.J., Krebs E.G., Dorsa D.M. Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription. Endocrinology 1997, 138:4030-4033.
173. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Liu Y. Estrogens: trophic and protective factors in the adult brain. Front. Neuroendocrinol. 2001, 22:33-66.
174. Wong M., Moss R.L. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J. Neurosci. 1992, 12:3217-3225.
175. Woolley C.S., McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 1992, 12:2549-2554.
176. Woolley C.S., McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 1993, 336:293-306.
177. Woolley C.S., Gould E., Frankfurt M., McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 1990, 10:4035-4039.
178. Woolley C.S., Weiland N.G., McEwen B.S., Schwartzkroin P.A. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J. Neurosci. 1997, 17:1848-1859.
179. Workman J.L., Barha C.K., Galea L.A. Endocrine substrates of cognitive and affective changes during pregnancy and postpartum. Behav. Neurosci. 2012, 126:54-72.
180. Wu T.W., Chen S., Brinton R.D. Membrane estrogen receptors mediate calcium signaling and MAP kinase activation in individual hippocampal neurons. Brain Res. 2011, 1379:34-43.
181. Yaffe K., Barnes D., Lindquist K., Cauley J., Simonsick E.M., Penninx B., Satterfield S., Harris T., Cummings S.R. Endogenous sex hormone levels and risk of cognitive decline in an older biracial cohort. Neurobiol. Aging 2007, 28:171-178.
182. Yang L.C., Zhang Q.G., Zhao C.F., Yang F., Zhang Y.D., Wang R.M., Brann D.W. Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus. PLoS ONE 2010, 5:e9851.
183. Yokomaku D., Numakawa T., Numakawa Y., Suzuki S., Matsumoto T., Adachi N., Nishio C., Taguchi T., Hatanaka H. Estrogen enhances depolarization-induced glutamate release through activation of phosphatidylinositol 3-kinase and mitogen-activated protein kinase in cultured hippocampal neurons. Mol. Endocrinol. 2003, 17:831-844.
184. Zandi P.P., Carlson M.C., Plassman B.L., Welsh-Bohmer K.A., Mayer L.S., Steffens D.C., Breitner J.C.S. Hormone replacement therapy and incidence of Alzheimer disease in older women. JAMA 2002, 288:2123-2129.
185. 2+ dynamics leading to ERK phosphorylation and estrogen neuroprotection in hippocampal neurons. Brain Res. 2007, 1172:48-59.
186. Zhao Z., Fan L., Frick K.M. Epigenetic alterations regulate the estradiol-induced enhancement of memory consolidation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5605-5610.
187. Zhao Z., Fan L., Fortress A.M., Boulware M.I., Frick K.M. Hippocampal histone acetylation regulates object recognition and the estradiol-induced enhancement of object recognition. J. Neurosci. 2012, 32:2344-2351.
188. Zhou L., Fester L., Haghshenas S., de Vrese X., von Hacht R., Gloger S., Brandt N., Bader M., Vollmer G., Rune G.M. Oestradiol-induced synapse formation in the female hippocampus: roles of oestrogen receptor subtypes. J. Neuroendocrinol. 2014, 26:439-447.