Estradiol rapidly modulates synaptic plasticity of hippocampal neurons: Involvement of kinase networks

Brain Research

Volumn 1621, Issue , 2015, Pages 147-161

  Hasegawa, Yoshitaka ^a   Hojo, Yasushi ^a,c   Kojima, Hiroki ^a   Ikeda, Muneki ^a   Hotta, Keisuke ^a   Sato, Rei ^a   Ooishi, Yuuki ^a   Yoshiya, Miyuki ^a   Chung, Bon Chu ^a,c   Yamazaki, Takeshi ^b   Kawato, Suguru ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

Author keywords

Estradiol; Estrogen; Estrogen receptor; Kinase; LTP; Rapid action; Spine; Synaptic plasticity

Indexed keywords

ANDROSTANOLONE; CALCINEURIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; ESTRADIOL; GLYCOGEN SYNTHASE KINASE 3BETA; LIM KINASE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE C; CYCLIC AMP DEPENDENT PROTEIN KINASE; NR2B NMDA RECEPTOR; PROTEIN KINASE;

ADULT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC SPINE; ENZYME INHIBITION; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SLICE; LONG TERM POTENTIATION; MALE; MOLECULAR IMAGING; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINOGENESIS; SYNAPTIC TRANSMISSION; THETA RHYTHM; YOUNG ADULT; ANIMAL; CYTOLOGY; DRUG EFFECTS; ELECTROSTIMULATION; METABOLISM; PHYSIOLOGY; PYRAMIDAL NERVE CELL; WISTAR RAT;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DENDRITIC SPINES; ELECTRIC STIMULATION; ESTRADIOL; LIM KINASES; LONG-TERM POTENTIATION; MALE; MAP KINASE SIGNALING SYSTEM; PHOSPHATIDYLINOSITOL 3-KINASE; PROTEIN KINASE C; PROTEIN KINASES; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION;

EID: 84941599036     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.12.056     Document Type: Article

References (90)

1. H. Aizawa, S. Wakatsuki, A. Ishii, K. Moriyama, Y. Sasaki, K. Ohashi, Y. Sekine-Aizawa, A. Sehara-Fujisawa, K. Mizuno, Y. Goshima, and I. Yahara Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse Nat. Neurosci. 4 2001 367 373
2. J. Balthazart, and G.F. Ball Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci. 29 2006 241 249
3. E.E. Baulieu Neurosteroids: of the nervous system, by the nervous system, for the nervous system Recent Prog. Horm. Res. 52 1997 1 32
4. E.E. Baulieu, and P. Robel Dehydroepiandrosterone (DHEA) and dehydroepiandrosterone sulfate (DHEAS) as neuroactive neurosteroids Proc. Natl. Acad. Sci. U.S.A. 95 1998 4089 4091
5. C. Beyer, and G. Rune Steroids in the brain: regulators of brain plasticity and protectors against neuronal damage J. Steroid Biochem. Mol. Biol. 131 2012 1
6. R. Bi, G. Broutman, M.R. Foy, R.F. Thompson, and M. Baudry The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus Proc. Natl. Acad. Sci. U.S.A. 97 2000 3602 3607
7. M.I. Boulware, and P.G. Mermelstein Membrane estrogen receptors activate metabotropic glutamate receptors to influence nervous system physiology Steroids 74 2009 608 613
8. M.I. Boulware, J.P. Weick, B.R. Becklund, S.P. Kuo, R.D. Groth, and P.G. Mermelstein Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein J. Neurosci. 25 2005 5066 5078
9. D.H. Campbell, R.L. Sutherland, and R.J. Daly Signaling pathways and structural domains required for phosphorylation of EMS1/cortactin Cancer Res. 59 1999 5376 5385
10. T. Chijiwa, A. Mishima, M. Hagiwara, M. Sano, K. Hayashi, T. Inoue, K. Naito, T. Toshioka, and H. Hidaka Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells J. Biol. Chem. 265 1990 5267 5272
11. A.N. Clancy, R.W. Bonsall, and R.P. Michael Immunohistochemical labeling of androgen receptors in the brain of rat and monkey Life Sci. 50 1992 409 417
12. C. Corpechot, P. Robel, M. Axelson, J. Sjovall, and E.E. Baulieu Characterization and measurement of dehydroepiandrosterone sulfate in rat brain Proc. Natl. Acad. Sci. U.S.A. 78 1981 4704 4707
13. R. Dominguez, R. Liu, and M. Baudry 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 2007 232 240
14. H. Duan, S.L. Wearne, J.H. Morrison, and P.R. Hof Quantitative analysis of the dendritic morphology of corticocortical projection neurons in the macaque monkey association cortex Neuroscience 114 2002 349 359
15. I. Ehrlich, and R. Malinow Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity J. Neurosci. 24 2004 916 927
16. M.F. Favata, K.Y. Horiuchi, E.J. Manos, A.J. Daulerio, D.A. Stradley, W.S. Feeser, D.E. Van Dyk, W.J. Pitts, R.A. Earl, F. Hobbs, R.A. Copeland, R.L. Magolda, P.A. Scherle, and J.M. Trzaskos Identification of a novel inhibitor of mitogen-activated protein kinase kinase J. Biol. Chem. 273 1998 18623 18632
17. G. Fischer, V. Mutel, G. Trube, P. Malherbe, J.N. Kew, E. Mohacsi, M.P. Heitz, and J.A. Kemp Ro 25-6981, a highly potent and selective blocker of N-methyl-d-aspartate receptors containing the NR2B subunit. Characterization in vitro J. Pharmacol. Exp. Ther. 283 1997 1285 1292
18. M.R. Foy, J. Xu, X. Xie, R.D. Brinton, R.F. Thompson, and T.W. Berger 17Beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation J. Neurophysiol. 81 1999 925 929
19. L.M. Garcia-Segura, Y. Diz-Chaves, M. Perez-Martin, and M. Darnaudery Estradiol, insuin-like growth factor-I and brain aging Psychoneuroendocrinology 32 1 2007 S57 S61
20. E. Gould, C.S. Woolley, M. Frankfurt, and B.S. McEwen Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood J. Neurosci. 10 1990 1286 1291
21. Q. Gu, K.S. Korach, and R.L. Moss Rapid action of 17beta-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors Endocrinology 140 1999 660 666
22. Q. Gu, and R.L. Moss 17 Beta-estradiol potentiates kainate-induced currents via activation of the cAMP cascade J. Neurosci. 16 1996 3620 3629
23. C. Guerra-Araiza, O. Villamar-Cruz, A. Gonzalez-Arenas, R. Chavira, and I. Camacho-Arroyo Changes in progesterone receptor isoforms content in the rat brain during the oestrous cycle and after oestradiol and progesterone treatments J. Neuroendocrinol. 15 2003 984 990
24. Y. Hasegawa, H. Mukai, M. Asashima, Y. Hojo, M. Ikeda, Y. Komatsuzaki, Y. Ooishi, and S. Kawato Acute modulation of synaptic plasticity of pyramidal neurons by activin in adult hippocampus Front. Neural. Circuits 8 2014 56
25. J.M. Herbert, J.M. Augereau, J. Gleye, and J.P. Maffrand Chelerythrine is a potent and specific inhibitor of protein kinase C Biochem. Biophys. Res. Commun. 172 1990 993 999
26. H. Hering, and M. Sheng Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis J. Neurosci. 23 2003 11759 11769
27. S.P. Herrick, E.M. Waters, C.T. Drake, B.S. McEwen, and T.A. Milner Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus Brain Res. 1121 2006 46 58
28. S. Higo, Y. Hojo, H. Ishii, T. Kominami, K. Nakajima, D. Poirier, T. Kimoto, and S. Kawato Comparison of sex-steroid synthesis between neonatal and adult rat hippocampus Biochem. Biophys. Res. Commun. 385 2009 62 66
29. Y. Hojo, T.A. Hattori, T. Enami, A. Furukawa, K. Suzuki, H.T. Ishii, H. Mukai, J.H. Morrison, W.G. Janssen, S. Kominami, N. Harada, T. Kimoto, and S. Kawato Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons Proc. Natl. Acad. Sci. U.S.A. 101 2004 865 870
30. Y. Hojo, S. Higo, H. Ishii, Y. Ooishi, H. Mukai, G. Murakami, T. Kominami, T. Kimoto, S. Honma, D. Poirier, and S. Kawato Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus Endocrinology 150 2009 5106 5112
31. Y. Hojo, S. Higo, S. Kawato, Y. Hatanaka, Y. Ooishi, G. Murakami, H. Ishii, Y. Komatsuzaki, M. Ogiue-Ikeda, H. Mukai, and T. Kimoto Hippocampal synthesis of sex steroids and corticosteroids: essential for modulation of synaptic plasticity Front. Endocrinol. (Lausanne) 2 2011 43
32. Y. Hojo, G. Murakami, H. Mukai, S. Higo, Y. Hatanaka, M. Ogiue-Ikeda, H. Ishii, T. Kimoto, and S. Kawato Estrogen synthesis in the brain - role in synaptic plasticity and memory Mol. Cell Endocrinol. 290 2008 31 43
33. J. Iki, A. Inoue, H. Bito, and S. Okabe Bi-directional regulation of postsynaptic cortactin distribution by BDNF and NMDA receptor activity Eur. J. Neurosci. 22 2005 2985 2994
34. K. Ito, K.L. Skinkle, and T.P. Hicks Age-dependent, steroid-specific effects of oestrogen on long-term potentiation in rat hippocampal slices J. Physiol. 515 1999 209 220 (Pt 1)
35. T. Jover-Mengual, T. Miyawaki, A. Latuszek, E. Alborch, R.S. Zukin, and A.M. Etgen Acute estradiol protects CA1 neurons from ischemia-induced apoptotic cell death via the PI3K/Akt pathway Brain Res. 1321 2010 1 12
36. A. Kato, Y. Hojo, S. Higo, Y. Komatsuzaki, G. Murakami, H. Yoshino, M. Uebayashi, and S. Kawato Female hippocampal estrogens have a significant correlation with cyclic fluctuation of hippocampal spines Front. Neural. Circuits 7 2013 149
37. S. Kawato Endocrine disrupters as disrupters of brain function: a neurosteroid viewpoint Environ. Sci. 11 2004 1 14
38. S. Kawato, Y. Hojo, and T. Kimoto Histological and metabolism analysis of P450 expression in the brain Methods Enzymol. 357 2002 241 249
39. S. Kawato, M. Yamada, and T. Kimoto Brain neurosteroids are 4th generation neuromessengers in the brain: cell biophysical analysis of steroid signal transduction Adv. Biophys. 37 2003 1 48
40. J.S. Kim, H.Y. Kim, J.H. Kim, H.K. Shin, S.H. Lee, Y.S. Lee, and H. Son Enhancement of rat hippocampal long-term potentiation by 17 beta-estradiol involves mitogen-activated protein kinase-dependent and -independent components Neurosci. Lett. 332 2002 65 69
41. T. Kimoto, T. Tsurugizawa, Y. Ohta, J. Makino, H. Tamura, Y. Hojo, N. Takata, and S. Kawato Neurosteroid synthesis by cytochrome p450-containing systems localized in the rat brain hippocampal neurons: N-methyl-D-aspartate and calcium-dependent synthesis Endocrinology 142 2001 3578 3589
42. M. Kobayashi, M. Nishita, T. Mishima, K. Ohashi, and K. Mizuno MAPKAPK-2-mediated LIM-kinase activation is critical for VEGF-induced actin remodeling and cell migration Embo J. 25 2006 713 726
43. A.T. Konkle, and M.M. McCarthy Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain Endocrinology 152 2011 223 235
44. E.A. Kramar, L.Y. Chen, N.J. Brandon, C.S. Rex, F. Liu, C.M. Gall, and G. Lynch Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity J. Neurosci. 29 2009 12982 12993
45. O. Kretz, L. Fester, U. Wehrenberg, L. Zhou, S. Brauckmann, S. Zhao, J. Prange-Kiel, T. Naumann, H. Jarry, M. Frotscher, and G.M. Rune Hippocampal synapses depend on hippocampal estrogen synthesis J. Neurosci. 24 2004 5913 5921
46. J.J. Krupp, B. Vissel, C.G. Thomas, S.F. Heinemann, and G.L. Westbrook Calcineurin acts via the C-terminus of NR2A to modulate desensitization of NMDA receptors Neuropharmacology 42 2002 593 602
47. C. Leranth, M. Shanabrough, and T.L. Horvath Hormonal regulation of hippocampal spine synapse density involves subcortical mediation Neuroscience 101 2000 349 356
48. C. Leranth, M. Shanabrough, and D.E. Redmond Jr. Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates J. Comp. Neurol. 447 2002 34 42
49. C. Liston, J.M. Cichon, F. Jeanneteau, Z. Jia, M.V. Chao, and W.B. Gan Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance Nat. Neurosci. 16 2013 698 705
50. G. Lynch, E.A. Kramar, C.S. Rex, Y. Jia, D. Chappas, C.M. Gall, and D.A. Simmons Brain-derived neurotrophic factor restores synaptic plasticity in a knock-in mouse model of Huntington's disease J. Neurosci. 27 2007 4424 4434
51. G.M. MacQueen, S. Campbell, B.S. McEwen, K. Macdonald, S. Amano, R.T. Joffe, C. Nahmias, and L.T. Young Course of illness, hippocampal function, and hippocampal volume in major depression Proc. Natl. Acad. Sci. U.S.A. 100 2003 1387 1392
52. B.S. McEwen, and S.E. Alves Estrogen actions in the central nervous system Endocr. Rev. 20 1999 279 307
53. T.A. Milner, K. Ayoola, C.T. Drake, S.P. Herrick, N.E. Tabori, B.S. McEwen, S. Warrier, and S.E. Alves Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation J. Comp. Neurol. 491 2005 81 95
54. M.S. Mo, H.B. Li, B.Y. Wang, S.L. Wang, Z.L. Zhu, and X.R. Yu PI3K/Akt and NF-kappaB activation following intravitreal administration of 17beta-estradiol: neuroprotection of the rat retina from light-induced apoptosis Neuroscience 228 2013 1 12
55. H. Mukai, Y. Hatanaka, K. Mitsuhashi, Y. Hojo, Y. Komatsuzaki, R. Sato, G. Murakami, T. Kimoto, and S. Kawato Automated analysis of spines from confocal laser microscopy images: application to the discrimination of androgen and estrogen effects on spinogenesis Cereb Cortex 21 2011 2704 2711
56. H. Mukai, T. Kimoto, Y. Hojo, S. Kawato, G. Murakami, S. Higo, Y. Hatanaka, and M. Ogiue-Ikeda Modulation of synaptic plasticity by brain estrogen in the hippocampus Biochim. Biophys. Acta 1800 2010 1030 1044
57. H. Mukai, N. Takata, H.T. Ishii, N. Tanabe, Y. Hojo, A. Furukawa, T. Kimoto, and S. Kawato Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology Neuroscience 138 2006 757 764
58. H. Mukai, T. Tsurugizawa, G. Murakami, S. Kominami, H. Ishii, M. Ogiue-Ikeda, N. Takata, N. Tanabe, A. Furukawa, Y. Hojo, Y. Ooishi, J.H. Morrison, W.G. Janssen, J.A. Rose, P. Chambon, S. Kato, S. Izumi, T. Yamazaki, T. Kimoto, and S. Kawato Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons J. Neurochem. 100 2007 950 967
59. E. Munetsuna, Y. Hojo, M. Hattori, H. Ishii, S. Kawato, A. Ishida, S.A. Kominami, and T. Yamazaki Retinoic acid stimulates 17beta-estradiol and testosterone synthesis in rat hippocampal slice cultures Endocrinology 150 2009 4260 4269
60. D.D. Murphy, and M. Segal Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones J. Neurosci. 16 1996 4059 4068
61. N. Nebieridze, X.L. Zhang, T. Chachua, L. Velisek, P.K. Stanton, and J. Veliskova Beta-estradiol unmasks metabotropic receptor-mediated metaplasticity of NMDA receptor transmission in the female rat dentate gyrus Psychoneuroendocrinology 37 2012 1845 1854
62. M. Ogiue-Ikeda, N. Tanabe, H. Mukai, Y. Hojo, G. Murakami, T. Tsurugizawa, N. Takata, T. Kimoto, and S. Kawato Rapid modulation of synaptic plasticity by estrogens as well as endocrine disrupters in hippocampal neurons Brain Res. Rev. 57 2008 363 375
63. M. Okamoto, Y. Hojo, K. Inoue, T. Matsui, S. Kawato, B.S. McEwen, and H. Soya Mild exercise increases dihydrotestosterone in hippocampus providing evidence for androgenic mediation of neurogenesis Proc. Natl. Acad. Sci. U.S.A. 109 2012 13100 13105
64. Y. Ooishi, S. Kawato, Y. Hojo, Y. Hatanaka, S. Higo, G. Murakami, Y. Komatsuzaki, M. Ogiue-Ikeda, T. Kimoto, and H. Mukai Modulation of synaptic plasticity in the hippocampus by hippocampus-derived estrogen and androgen J. Steroid Biochem. Mol. Biol. 131 2012a 37 51
65. Y. Ooishi, H. Mukai, Y. Hojo, G. Murakami, Y. Hasegawa, T. Shindo, J.H. Morrison, T. Kimoto, and S. Kawato Estradiol rapidly rescues synaptic transmission from corticosterone-induced suppression via synaptic/extranuclear steroid receptors in the hippocampus Cereb. Cortex 22 2012b 926 936
66. V.E. Pettorossi, M. Di Mauro, M. Scarduzio, R. Panichi, A. Tozzi, P. Calabresi, and S. Grassi Modulatory role of androgenic and estrogenic neurosteroids in determining the direction of synaptic plasticity in the CA1 hippocampal region of male rats Physiol. Rep. 1 2013 e00185
67. Y. Pilpel, and M. Segal Activation of PKC induces rapid morphological plasticity in dendrites of hippocampal neurons via Rac and Rho-dependent mechanisms Eur. J. Neurosci. 19 2004 3151 3164
68. L.D. Pozzo-Miller, T. Inoue, and D.D. Murphy Estradiol increases spine density and NMDA-dependent Ca2+ transients in spines of CA1 pyramidal neurons from hippocampal slices J. Neurophysiol. 81 1999 1404 1411
69. M. Razandi, A. Pedram, G.L. Greene, and E.R. Levin Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells Mol. Endocrinol. 13 1999 307 319
70. E.D. Roberson, J.D. English, J.P. Adams, J.C. Selcher, C. Kondratick, and J.D. Sweatt The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus J. Neurosci. 19 1999 4337 4348
71. P. Ross-Macdonald, H. de Silva, Q. Guo, H. Xiao, C.Y. Hung, B. Penhallow, J. Markwalder, L. He, R.M. Attar, T.A. Lin, S. Seitz, C. Tilford, J. Wardwell-Swanson, and D. Jackson Identification of a nonkinase target mediating cytotoxicity of novel kinase inhibitors Mol. Cancer Ther. 7 2008 3490 3498
72. Y. Shi, C.G. Pontrello, K.A. DeFea, L.F. Reichardt, and I.M. Ethell Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity J. Neurosci. 29 2009 8129 8142
73. Y. Shinohara, H. Hirase, M. Watanabe, M. Itakura, M. Takahashi, and R. Shigemoto Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors Proc. Natl. Acad. Sci. U.S.A. 105 2008 19498 19503
74. T. Simoncini, A. Hafezi-Moghadam, D.P. Brazil, K. Ley, W.W. Chin, and J.K. Liao Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase Nature 407 2000 538 541
75. V.A. Skucas, A.M. Duffy, L.C. Harte-Hargrove, A. Magagna-Poveda, T. Radman, G. Chakraborty, C.E. Schroeder, N.J. MacLusky, and H.E. Scharfman Testosterone depletion in adult male rats increases mossy fiber transmission, LTP, and sprouting in area CA3 of hippocampus J. Neurosci. 33 2013 2338 2355
76. C.C. Smith, and L.L. McMahon Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors J. Neurosci. 26 2006 8517 8522
77. M.D. Smith, L.S. Jones, and M.A. Wilson Sex differences in hippocampal slice excitability: role of testosterone Neuroscience 109 2002 517 530
78. M.A. Snyder, B.M. Cooke, and C.S. Woolley Estradiol potentiation of NR2B-dependent EPSCs is not due to changes in NR2B protein expression or phosphorylation Hippocampus 21 2011 398 408
79. C.D. Toran-Allerand, X. Guan, N.J. MacLusky, T.L. Horvath, S. Diano, M. Singh, E.S. Connolly Jr., I.S. Nethrapalli, and A.A. Tinnikov ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury J. Neurosci. 22 2002 8391 8401
80. T. Tsurugizawa, H. Mukai, N. Tanabe, G. Murakami, Y. Hojo, S. Kominami, K. Mitsuhashi, Y. Komatsuzaki, J.H. Morrison, W.G. Janssen, T. Kimoto, and S. Kawato Estrogen induces rapid decrease in dendritic thorns of CA3 pyramidal neurons in adult male rat hippocampus Biochem. Biophys. Res. Commun. 337 2005 1345 1352
81. R. Vierk, G. Glassmeier, L. Zhou, N. Brandt, L. Fester, D. Dudzinski, W. Wilkars, R.A. Bender, M. Lewerenz, S. Gloger, L. Graser, J. Schwarz, and G.M. Rune Aromatase inhibition abolishes LTP generation in female but not in male mice J. Neurosci. 32 2012 8116 8126
82. R.M. Vouimba, M.R. Foy, J.G. Foy, and R.F. Thompson 17Beta-estradiol suppresses expression of long-term depression in aged rats Brain Res. Bull. 53 2000 783 787
83. S.A. Weed, Y. Du, and J.T. Parsons Translocation of cortactin to the cell periphery is mediated by the small GTPase Rac1 J. Cell Sci. 111 1998 2433 2443 (Pt 16)
84. G. Wiederrecht, E. Lam, S. Hung, M. Martin, and N. Sigal The mechanism of action of FK-506 and cyclosporin A Ann. N. Y. Acad. Sci. 696 1993 9 19
85. C.S. Woolley, E. Gould, M. Frankfurt, and B.S. McEwen Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons J. Neurosci. 10 1990 4035 4039
86. C.S. Woolley, and B.S. McEwen Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat J. Neurosci. 12 1992 2549 2554
87. C.S. Woolley, and B.S. McEwen Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat J. Comp. Neurol. 336 1993 293 306
88. C.S. Woolley, and B.S. McEwen Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism J. Neurosci. 14 1994 7680 7687
89. C.S. Woolley, N.G. Weiland, B.S. McEwen, and P.A. Schwartzkroin Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density J. Neurosci. 17 1997 1848 1859
90. L.C. Yang, Q.G. Zhang, C.F. Zhou, F. Yang, Y.D. Zhang, R.M. Wang, and D.W. Brann Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus PLoS One 5 2010 e9851