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Genomics, Proteomics, and the Nervous System pp 161–176Cite as

Gene Expression and Signal Transduction Cascades Mediating Estrogen Effects on Memory

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Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 2))

Abstract

Estrogen treatment has been shown to influence memory function and protect against age-related cognitive decline. However, the mechanism through which estrogen acts to regulate these processes is not well understood. Research in this area has focused on the hippocampus and other limbic structures, due to their well-established role in memory processes. In particular, the impact of estrogen on Ca2+-dependent synaptic plasticity is of interest, since synaptic plasticity provides a potential memory mechanism. Estrogen acts through rapid Ca2+ signaling cascades to modify induction of synaptic plasticity and control translational mechanisms via the phosphorylation state of transcription factors, leading to structural modifications. Estrogen can also influence transcription through estrogen receptor (e.g., ERα and ERβ) interactions with estrogen response elements located on DNA. Thus, in addition to rapid effects on synaptic function, transcriptional mechanisms lead to longer term trophic and neuroprotective benefits that may maintain hippocampal health in the face of aging.

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References

  • Adams, M. M., Fink, S. E., Janssen, W. G., Shah, R. A., & Morrison, J. H. (2004). Estrogen modulates synaptic N-methyl-D-aspartate receptor subunit distribution in the aged hippocampus. The Journal of Comparative Neurology, 474, 419–426.

    Article  PubMed  CAS  Google Scholar 

  • Adams, M. M., Fink, S. E., Shah, R. A., Janssen, W. G., Hayashi, S., Milner, T. A., et al. (2002). Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the ­hippocampus of female rats. The Journal of Neuroscience, 22, 3608–3614.

    PubMed  CAS  Google Scholar 

  • Aronica, S. M., Kraus, W. L., & Katzenellenbogen, B. S. (1994). Estrogen action via the cAMP signaling pathway: Stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proceedings of the National Academy of Sciences of the United States of America, 91, 8517–8521.

    Article  PubMed  CAS  Google Scholar 

  • Azcoitia, I., Sierra, A., & Garcia-Segura, L. M. (1999). Localization of estrogen receptor beta-immunoreactivity in astrocytes of the adult rat brain. Glia, 26, 260–267.

    Article  PubMed  CAS  Google Scholar 

  • 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. Molecular Pharmacology, 54, 105–112.

    PubMed  CAS  Google Scholar 

  • Benvenuti, S., Luciani, P., Vannelli, G. B., Gelmini, S., Franceschi, E., Serio, M., et al. (2005). Estrogen and selective estrogen receptor modulators exert neuroprotective effects and ­stimulate the expression of selective Alzheimer’s disease indicator-1, a recently discovered antiapoptotic gene, in human neuroblast long-term cell cultures. The Journal of Clinical Endocrinology and Metabolism, 90, 1775–1782.

    Article  PubMed  CAS  Google Scholar 

  • Bi, R., Foy, M. R., Vouimba, R. M., Thompson, R. F., & Baudry, M. (2001). Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proceedings of the National Academy of Sciences of the United States of America, 98, 13391–13395.

    Article  PubMed  CAS  Google Scholar 

  • Bjornstrom, L., & Sjoberg, M. (2005). Mechanisms of estrogen receptor signaling: Convergence of genomic and nongenomic actions on target genes. Molecular Endocrinology, 19, 833–842.

    Article  PubMed  CAS  Google Scholar 

  • Blalock, E. M., Chen, K. C., Sharrow, K., Herman, J. P., Porter, N. M., Foster, T. C., et al. (2003). Gene microarrays in hippocampal aging: Statistical profiling identifies novel processes ­correlated with cognitive impairment. The Journal of Neuroscience, 23, 3807–3819.

    PubMed  CAS  Google Scholar 

  • Blum, S., Moore, A. N., Adams, F., & Dash, P. K. (1999). A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory. The Journal of Neuroscience, 19, 3535–3544.

    PubMed  CAS  Google Scholar 

  • Blutstein, T., Devidze, N., Choleris, E., Jasnow, A. M., Pfaff, D. W., & Mong, J. A. (2006). Oestradiol up-regulates glutamine synthetase mRNA and protein expression in the hypothalamus and hippocampus: implications for a role of hormonally responsive glia in amino acid neurotransmission. Journal of Neuroendocrinology, 18, 692–702.

    Article  PubMed  CAS  Google Scholar 

  • Boulware, M. I., Weick, J. P., Becklund, B. R., Kuo, S. P., Groth, R. D., & Mermelstein, P. G. (2005). Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. The Journal of Neuroscience, 25, 5066–5078.

    Article  PubMed  CAS  Google Scholar 

  • Bowman, R. E., Ferguson, D., & Luine, V. N. (2002). Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience, 113, 401–410.

    Article  PubMed  CAS  Google Scholar 

  • Brake, W. G., Alves, S. E., Dunlop, J. C., Lee, S. J., Bulloch, K., Allen, P. B., et al. (2001). Novel target sites for estrogen action in the dorsal hippocampus: An examination of synaptic ­proteins. Endocrinology, 142, 1284–1289.

    Article  PubMed  CAS  Google Scholar 

  • Brewer, G. J., Reichensperger, J. D., & Brinton, R. D. (2006). Prevention of age-related dysregulation of calcium dynamics by estrogen in neurons. Neurobiology of Aging, 27, 306–317.

    Article  PubMed  CAS  Google Scholar 

  • Cardona-Gomez, G. P., Trejo, J. L., Fernandez, A. M., & Garcia-Segura, L. M. (2000). Estrogen receptors and insulin-like growth factor-I receptors mediate estrogen-dependent synaptic plasticity. Neuroreport, 11, 1735–1738.

    Article  PubMed  CAS  Google Scholar 

  • Carrer, H. F., Araque, A., & Buno, W. (2003). Estradiol regulates the slow Ca2+-activated K+ current in hippocampal pyramidal neurons. The Journal of Neuroscience, 23, 6338–6344.

    PubMed  CAS  Google Scholar 

  • Carswell, H. V., Dominiczak, A. F., Garcia-Segura, L. M., Harada, N., Hutchison, J. B., & Macrae, I. M. (2005). Brain aromatase expression after experimental stroke: topography and time course. The Journal of Steroid Biochemistry and Molecular Biology, 96, 89–91.

    Article  PubMed  CAS  Google Scholar 

  • Cattaneo, E., & Maggi, A. (1990). c-fos Induction by estrogen in specific rat brain areas. European Journal of Pharmacology, 188, 153–159.

    Article  PubMed  CAS  Google Scholar 

  • Cavus, I., & Duman, R. S. (2003). Influence of estradiol, stress, and 5-HT2A agonist treatment on brain-derived neurotrophic factor expression in female rats. Biological Psychiatry, 54, 59–69.

    Article  PubMed  CAS  Google Scholar 

  • Chan, S. L., Tammariello, S. P., Estus, S., & Mattson, M. P. (1999). Prostate apoptosis response-4 mediates trophic factor withdrawal-induced apoptosis of hippocampal neurons: Actions prior to mitochondrial dysfunction and caspase activation. Journal of Neurochemistry, 73, 502–512.

    Article  PubMed  CAS  Google Scholar 

  • Chang, L., & Karin, M. (2001). Mammalian MAP kinase signalling cascades. Nature, 410, 37–40.

    Article  PubMed  CAS  Google Scholar 

  • Chen, J. Q., Delannoy, M., Cooke, C., & Yager, J. D. (2004). Mitochondrial localization of ERalpha and ERbeta in human MCF7 cells. American Journal of Physiology. Endocrinology and Metabolism, 286, E1011–E1022.

    Article  PubMed  CAS  Google Scholar 

  • Cyr, M., Thibault, C., Morissette, M., Landry, M., & Di Paolo, T. (2001). Estrogen-like activity of tamoxifen and raloxifene on NMDA receptor binding and expression of its subunits in rat brain. Neuropsychopharmacology, 25, 242–257.

    Article  PubMed  CAS  Google Scholar 

  • Day, J. R, Laping, N. J, Lampert-Etchells, M., Brown, S. A, O’Callaghan, J. P, McNeill, T.H., & Finch, C. E. (1993) Gonadal steroids regulate the expression of glial fibrillary acidic protein in the adult male rat hippocampus. Neuroscience, 55, 435–443.

    Google Scholar 

  • Del Cerro, S., Garcia-Estrada, J., & Garcia-Segura, L. M. (1995) Neuroactive steroids regulate astroglia morphology in hippocampal cultures from adult rats. Glia, 14, 65–71.

    Google Scholar 

  • Dominguez-Salazar, E., Shetty, S., & Rissman, E. F. (2006). Rapid neural Fos responses to oestradiol in oestrogen receptor alphabeta double knockout mice. Journal of Neuroendocrinology, 18, 195–202.

    Article  PubMed  CAS  Google Scholar 

  • Dykens, J. A., Simpkins, J. W., Wang, J., & Gordon, K. (2003). Polycyclic phenols, estrogens and neuroprotection: A proposed mitochondrial mechanism. Experimental Gerontology, 38, 101–107.

    Article  PubMed  CAS  Google Scholar 

  • Eberling, J. L., Wu, C., Tong-Turnbeaugh, R., & Jagust, W. J. (2004). Estrogen- and tamoxifen-associated effects on brain structure and function. Neuroimage, 21, 364–371.

    Article  PubMed  Google Scholar 

  • Espeland, M. A., Rapp, S. R., Shumaker, S. A., Brunner, R., Manson, J. E., Sherwin, B. B., et al. (2004). Conjugated equine estrogens and global cognitive function in postmenopausal women: Women’s Health Initiative Memory Study. JAMA, 291, 2959–2968.

    Article  PubMed  CAS  Google Scholar 

  • Favit, A., Fiore, L., Nicoletti, F., & Canonico, P. L. (1991). Estrogen modulates stimulation of inositol phospholipid hydrolysis by norepinephrine in rat brain slices. Brain Research, 555, 65–69.

    Article  PubMed  CAS  Google Scholar 

  • Ferrini, M., Bisagno, V., Piroli, G., Grillo, C., Deniselle, M. C., & De Nicola, A. F. (2002). Effects of estrogens on choline-acetyltransferase immunoreactivity and GAP-43 mRNA in the forebrain of young and aging male rats. Cellular and Molecular Neurobiology, 22, 289–301.

    Article  PubMed  CAS  Google Scholar 

  • Foster, T. C. (2005). Interaction of rapid signal transduction cascades and gene expression in mediating estrogen effects on memory over the life span. Frontiers in Neuroendocrinology, 26, 51–64.

    Article  PubMed  CAS  Google Scholar 

  • Foy, M. R., Chiaia, N. L., & Teyler, T. J. (1984). Reversal of hippocampal sexual dimorphism by gonadal steroid manipulation. Brain Research, 321, 311–314.

    Article  PubMed  CAS  Google Scholar 

  • Foy, M. R., Xu, J., Xie, X., Brinton, R. D., Thompson, R. F., & Berger, T. W. (1999). 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. Journal of Neurophysiology, 81, 925–929.

    PubMed  CAS  Google Scholar 

  • Fugger, H. N., Kumar, A., Lubahn, D. B., Korach, K. S., & Foster, T. C. (2001). Examination of estradiol effects on the rapid estradiol mediated increase in hippocampal synaptic transmission in estrogen receptor alpha knockout mice. Neuroscience Letters, 309, 207–209.

    Article  PubMed  CAS  Google Scholar 

  • Galea, L. A., Spritzer, M. D., Barker, J. M., & Pawluski, J. L. (2006). Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus, 16, 225–232.

    Article  PubMed  CAS  Google Scholar 

  • Gibbs, R. B. (1998). Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Research, 787, 259–268.

    Article  PubMed  CAS  Google Scholar 

  • Gibbs, R. B. (1999). Treatment with estrogen and progesterone affects relative levels of brain-derived neurotrophic factor mRNA and protein in different regions of the adult rat brain. Brain Research, 844, 20–27.

    Article  PubMed  CAS  Google Scholar 

  • Gibbs, R. B., & Aggarwal, P. (1998). Estrogen and basal forebrain cholinergic neurons: ­implications for brain aging and Alzheimer’s disease-related cognitive decline. Hormones and Behavior, 34, 98–111.

    Article  PubMed  CAS  Google Scholar 

  • Gould, E., Woolley, C. S., Frankfurt, M., & McEwen, B. S. (1990). Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. The Journal of Neuroscience, 10, 1286–1291.

    PubMed  CAS  Google Scholar 

  • Gu, Q., & Moss, R. L. (1996). 17 beta-Estradiol potentiates kainate-induced currents via activation of the cAMP cascade. The Journal of Neuroscience, 16, 3620–3629.

    PubMed  CAS  Google Scholar 

  • Guzowski, J. F. (2002). Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonucleotide and fluorescent imaging approaches. Hippocampus, 12, 86–104.

    Article  PubMed  CAS  Google Scholar 

  • Hayashi, S., Ueyama, T., Kajimoto, T., Yagi, K., Kohmura, E., & Saito, N. (2005). Involvement of gamma protein kinase C in estrogen-induced neuroprotection against focal brain ischemia through G protein-coupled estrogen receptor. Journal of Neurochemistry, 93, 883–891.

    Article  PubMed  CAS  Google Scholar 

  • Heikkinen, T., Puolivali, J., Liu, L., Rissanen, A., & Tanila, H. (2002). Effects of ovariectomy and estrogen treatment on learning and hippocampal neurotransmitters in mice. Hormones and Behavior, 41, 22–32.

    Article  PubMed  CAS  Google Scholar 

  • Hruska, R. E., & Pitman, K. T. (1982). Distribution and localization of estrogen-sensitive dopamine receptors in the rat brain. Journal of Neurochemistry, 39, 1418–1423.

    Article  PubMed  CAS  Google Scholar 

  • Improta-Brears, T., Whorton, A. R., Codazzi, F., York, J. D., Meyer, T., & McDonnell, D. P. (1999). Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium. Proceedings of the National Academy of Sciences of the United States of America, 96, 4686–4691.

    Article  PubMed  CAS  Google Scholar 

  • Jezierski, M. K., & Sohrabji, F. (2001). Neurotrophin expression in the reproductively senescent forebrain is refractory to estrogen stimulation. Neurobiology of Aging, 22, 309–319.

    Article  PubMed  CAS  Google Scholar 

  • Kalita, K., Szymczak, S., & Kaczmarek, L. (2005). Non-nuclear estrogen receptor beta and alpha in the hippocampus of male and female rats. Hippocampus, 15, 404–412.

    Article  PubMed  CAS  Google Scholar 

  • Kurata, K., Takebayashi, M., Kagaya, A., Morinobu, S., & Yamawaki, S. (2001). Effect of beta-estradiol on voltage-gated Ca(2+) channels in rat hippocampal neurons: A comparison with dehydroepiandrosterone. European Journal of Pharmacology, 416, 203–212.

    Article  PubMed  CAS  Google Scholar 

  • 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. European Journal of Pharmacology, 400, 205–209.

    Article  PubMed  CAS  Google Scholar 

  • Lee, S. J., Campomanes, C. R., Sikat, P. T., Greenfield, A. T., Allen, P. B., & McEwen, B. S. (2004). Estrogen induces phosphorylation of cyclic AMP response element binding (pCREB) in primary hippocampal cells in a time-dependent manner. Neuroscience, 124, 549–560.

    Article  PubMed  CAS  Google Scholar 

  • Leranth, C., Shanabrough, M., & Redmond, D. E., Jr. (2002). Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. The Journal of Comparative Neurology, 447, 34–42.

    Article  PubMed  CAS  Google Scholar 

  • Lin, B., Kramar, E. A., Bi, X., Brucher, F. A., Gall, C. M., & Lynch, G. (2005). Theta stimulation polymerizes actin in dendritic spines of hippocampus. The Journal of Neuroscience, 25, 2062–2069.

    Article  PubMed  CAS  Google Scholar 

  • Luine, V. N. (1985). Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Experimental Neurology, 89, 484–490.

    Article  PubMed  CAS  Google Scholar 

  • Mattson, M. P., Robinson, N., & Guo, Q. (1997). Estrogens stabilize mitochondrial function and protect neural cells against the pro-apoptotic action of mutant presenilin-1. Neuroreport, 8, 3817–3821.

    Article  PubMed  CAS  Google Scholar 

  • McCarthy, J. B., Barker-Gibb, A. L., Alves, S. E., & Milner, T. A. (2002). TrkA immunoreactive astrocytes in dendritic fields of the hippocampal formation across estrous. Glia, 38, 36–44.

    Article  PubMed  CAS  Google Scholar 

  • McCullough, L. D., Blizzard, K., Simpson, E. R., Oz, O. K., & Hurn, P. D. (2003). Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection. The Journal of Neuroscience, 23, 8701–8705.

    PubMed  CAS  Google Scholar 

  • McEwen, B. (2002). Estrogen actions throughout the brain. Recent Progress in Hormone Research, 57, 357–384.

    Article  PubMed  CAS  Google Scholar 

  • McEwen, B. S., Tanapat, P., & Weiland, N. G. (1999). Inhibition of dendritic spine induction on hippocampal CA1 pyramidal neurons by a nonsteroidal estrogen antagonist in female rats. Endocrinology, 140, 1044–1047.

    Article  PubMed  CAS  Google Scholar 

  • McQueen, J. K., Dow, R. C., & Fink, G. (1992) Gonadal steroids regulate number of astrocytes immunostained for glial fibrillary acidic protein in mouse hippocampus. Molecular and Cellular Neurosciences, 3, 482–486.

    Google Scholar 

  • Mendez, P., Wandosell, F., & Garcia-Segura, L. M. (2006). Cross-talk between estrogen receptors and insulin-like growth factor-I receptor in the brain: Cellular and molecular mechanisms. Frontiers in Neuroendocrinology, 27, 391–403.

    Article  PubMed  CAS  Google Scholar 

  • Mermelstein, P. G., Becker, J. B., & Surmeier, D. J. (1996). Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. The Journal of Neuroscience, 16, 595–604.

    PubMed  CAS  Google Scholar 

  • Milner, T. A., Ayoola, K., Drake, C. T., Herrick, S. P., Tabori, N. E., McEwen, B. S., et al. (2005). Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. The Journal of Comparative Neurology, 491, 81–95.

    Article  PubMed  CAS  Google Scholar 

  • Milner, T. A., McEwen, B. S., Hayashi, S., Li, C. J., Reagan, L. P., & Alves, S. E. (2001). Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. The Journal of Comparative Neurology, 429, 355–371.

    Article  PubMed  CAS  Google Scholar 

  • Mitra, S. W., Hoskin, E., Yudkovitz, J., Pear, L., Wilkinson, H. A., Hayashi, S., et al. (2003). Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology, 144, 2055–2067.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, D. D., & Segal, M. (1997). Morphological plasticity of dendritic spines in central neurons is mediated by activation of cAMP response element binding protein. Proceedings of the National Academy of Sciences of the United States of America, 94, 1482–1487.

    Article  PubMed  CAS  Google Scholar 

  • Nguyen, P. V., & Woo, N. H. (2003). Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Progress in Neurobiology, 71, 401–437.

    Article  PubMed  CAS  Google Scholar 

  • Nishio, M., Kuroki, Y., & Watanabe, Y. (2004). Subcellular localization of estrogen receptor beta in mouse hippocampus. Neuroscience Letters, 355, 109–112.

    Article  PubMed  CAS  Google Scholar 

  • Nishizuka, M., & Arai, Y. (1982). Synapse formation in response to estrogen in the medial amygdala developing in the eye. Proceedings of the National Academy of Sciences of the United States of America, 79, 7024–7026.

    Article  PubMed  CAS  Google Scholar 

  • Osterlund, M. K., & Hurd, Y. L. (2001). Estrogen receptors in the human forebrain and the relation to neuropsychiatric disorders. Progress in Neurobiology, 64, 251–267.

    Article  PubMed  CAS  Google Scholar 

  • Paech, K., Webb, P., Kuiper, G. G., Nilsson, S., Gustafsson, J., Kushner, P. J., et al. (1997). Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science, 277, 1508–1510.

    Article  PubMed  CAS  Google Scholar 

  • Pang, P. T., & Lu, B. (2004). Regulation of late-phase LTP and long-term memory in normal and aging hippocampus: Role of secreted proteins tPA and BDNF. Ageing Research Reviews, 3, 407–430.

    Article  PubMed  CAS  Google Scholar 

  • Parducz, A., Hajszan, T., Maclusky, N. J., Hoyk, Z., Csakvari, E., Kurunczi, A., et al. (2006). Synaptic remodeling induced by gonadal hormones: Neuronal plasticity as a mediator of neuroendocrine and behavioral responses to steroids. Neuroscience, 138, 977–985.

    Article  PubMed  CAS  Google Scholar 

  • Patrone, C., Pollio, G., Vegeto, E., Enmark, E., de Curtis, I., Gustafsson, J. A., et al. (2000). Estradiol induces differential neuronal phenotypes by activating estrogen receptor alpha or beta. Endocrinology, 141, 1839–1845.

    Article  PubMed  CAS  Google Scholar 

  • Pfaff, D., & Keiner, M. (1973). Atlas of estradiol-concentrating cells in the central nervous system of the female rat. The Journal of Comparative Neurology, 151, 121–158.

    Article  PubMed  CAS  Google Scholar 

  • Prange-Kiel, J., & Rune, G. M. (2006). Direct and indirect effects of estrogen on rat hippocampus. Neuroscience, 138, 765–772.

    Article  PubMed  CAS  Google Scholar 

  • Prolla, T. A. (2002). DNA microarray analysis of the aging brain. Chemical Senses, 27, 299–306.

    Article  PubMed  CAS  Google Scholar 

  • Ramirez, V. D., & Zheng, J. (1996). Membrane sex-steroid receptors in the brain. Frontiers in Neuroendocrinology, 17, 402–439.

    Article  PubMed  CAS  Google Scholar 

  • Revankar, C. M., Cimino, D. F., Sklar, L. A., Arterburn, J. B., & Prossnitz, E. R. (2005). A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science, 307, 1625–1630.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Calvo, R., Jove, M., Coll, T., Camins, A., Sanchez, R. M., Alegret, M., et al. (2006). PGC-1beta down-regulation is associated with reduced ERRalpha activity and MCAD expression in skeletal muscle of senescence-accelerated mice. The Journals of Gerontology. Series A: Biological Sciences and Medical Sciences, 61, 773–780.

    Article  Google Scholar 

  • Romeo, R. D., McCarthy, J. B., Wang, A., Milner, T. A., & McEwen, B. S. (2005). Sex differences in hippocampal estradiol-induced N-methyl-D-aspartic acid binding and ultrastructural localization of estrogen receptor-alpha. Neuroendocrinology, 81, 391–399.

    Article  PubMed  CAS  Google Scholar 

  • Rudick, C. N., & Woolley, C. S. (2003). Selective estrogen receptor modulators regulate ­phasic activation of hippocampal CA1 pyramidal cells by estrogen. Endocrinology, 144, 179–187.

    Article  PubMed  CAS  Google Scholar 

  • Sasano, H., Takashashi, K., Satoh, F., Nagura, H., & Harada, N. (1998). Aromatase in the human central nervous system. Clinical Endocrinology, 48, 325–329.

    Article  PubMed  CAS  Google Scholar 

  • Sawai, T., Bernier, F., Fukushima, T., Hashimoto, T., Ogura, H., & Nishizawa, Y. (2002). Estrogen induces a rapid increase of calcium-calmodulin-dependent protein kinase II activity in the hippocampus. Brain Research, 950, 308–311.

    Article  PubMed  CAS  Google Scholar 

  • Scharfman, H. E., & Maclusky, N. J. (2006). Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: Complexity of steroid hormone-growth factor interactions in the adult CNS. Frontiers in Neuroendocrinology, 27, 415–435.

    Article  PubMed  CAS  Google Scholar 

  • Segal, M., & Murphy, D. (2001). Estradiol induces formation of dendritic spines in hippocampal neurons: Functional correlates. Hormones and Behavior, 40, 156–159.

    Article  PubMed  CAS  Google Scholar 

  • Selcher, J. C., Atkins, C. M., Trzaskos, J. M., Paylor, R., & Sweatt, J. D. (1999). A necessity for MAP kinase activation in mammalian spatial learning. Learning & Memory, 6, 478–490.

    Article  CAS  Google Scholar 

  • Selcher, J. C., Weeber, E. J., Varga, A. W., Sweatt, J. D., & Swank, M. (2002). Protein kinase signal transduction cascades in mammalian associative conditioning. The Neuroscientist, 8, 122–131.

    Article  PubMed  CAS  Google Scholar 

  • Setalo, G., Jr., Singh, M., Guan, X., & Toran-Allerand, C. D. (2002). Estradiol-induced phosphorylation of ERK1/2 in explants of the mouse cerebral cortex: the roles of heat shock protein 90 (Hsp90) and MEK2. Journal of Neurobiology, 50, 1–12.

    Article  PubMed  CAS  Google Scholar 

  • Shah, R. D., Anderson, K. L., Rapoport, M., & Ferreira, A. (2003). Estrogen-induced changes in the microtubular system correlate with a decreased susceptibility of aging neurons to beta amyloid neurotoxicity. Molecular and Cellular Neurosciences, 24, 503–516.

    Article  PubMed  CAS  Google Scholar 

  • Sharrow, K. M., Kumar, A., & Foster, T. C. (2002). Calcineurin as a potential contributor in estradiol regulation of hippocampal synaptic function. Neuroscience, 113, 89–97.

    Article  PubMed  CAS  Google Scholar 

  • Sherwin, B. B. (2005). Estrogen and memory in women: How can we reconcile the findings? Hormones and Behavior, 47, 371–375.

    Article  PubMed  CAS  Google Scholar 

  • Shingo, A. S., & Kito, S. (2005). Estradiol induces PKA activation through the putative membrane receptor in the living hippocampal neuron. Journal of Neural Transmission, 112, 1469–1473.

    Article  PubMed  CAS  Google Scholar 

  • Shingo, A. S., & Kito, S. (2002). Estrogen induces elevation of cAMP-dependent protein kinase activity in immortalized hippocampal neurons: imaging in living cells. Journal of Neural Transmission, 109, 171–174.

    Article  PubMed  CAS  Google Scholar 

  • Shors, T. J., Chua, C., & Falduto, J. (2001). Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. The Journal of Neuroscience, 21, 6292–6297.

    PubMed  CAS  Google Scholar 

  • Shughrue, P. J., Lane, M. V., & Merchenthaler, I. (1997). Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. The Journal of Comparative Neurology, 388, 507–525.

    Article  PubMed  CAS  Google Scholar 

  • Singh, M., Meyer, E. M., & Simpkins, J. W. (1995). The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology, 136, 2320–2324.

    Article  PubMed  CAS  Google Scholar 

  • Singh, M., Setalo, G., Jr., Guan, X., Warren, M., & Toran-Allerand, C. D. (1999). Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. The Journal of Neuroscience, 19, 1179–1188.

    PubMed  CAS  Google Scholar 

  • Sohrabji, F., Miranda, R. C., & Toran-Allerand, C. D. (1995). Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proceedings of the National Academy of Sciences of the United States of America, 92, 11110–11114.

    Article  PubMed  CAS  Google Scholar 

  • Stoltzner, S. E., Berchtold, N. C., Cotman, C. W., & Pike, C. J. (2001). Estrogen regulates bcl-x expression in rat hippocampus. Neuroreport, 12, 2797–2800.

    Article  PubMed  CAS  Google Scholar 

  • Szymczak, S., Kalita, K., Jaworski, J., Mioduszewska, B., Savonenko, A., Markowska, A., et al. (2006). Increased estrogen receptor beta expression correlates with decreased spine formation in the rat hippocampus. Hippocampus, 16, 453–463.

    Article  PubMed  CAS  Google Scholar 

  • Tanabe, N., Kimoto, T., & Kawato, S. (2006). Rapid Ca2+ signaling induced by Bisphenol A in cultured rat hippocampal neurons. Neuro Endocrinology Letters, 27, 97–104.

    PubMed  CAS  Google Scholar 

  • Tanapat, P., Hastings, N. B., Reeves, A. J., & Gould, E. (1999). Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. The Journal of Neuroscience, 19, 5792–5801.

    PubMed  CAS  Google Scholar 

  • Vanacker, J. M., Pettersson, K., Gustafsson, J. A., & Laudet, V. (1999). Transcriptional targets shared by estrogen receptor- related receptors (ERRs) and estrogen receptor (ER) alpha, but not by ERbeta. The EMBO Journal, 18, 4270–4279.

    Article  PubMed  CAS  Google Scholar 

  • Veiga, S., Azcoitia, I., & Garcia-Segura, L. M. (2005). Extragonadal synthesis of estradiol is protective against kainic acid excitotoxic damage to the hippocampus. Neuroreport, 16, 1599–1603.

    Article  PubMed  CAS  Google Scholar 

  • Wade, C. B., & Dorsa, D. M. (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.

    Article  PubMed  CAS  Google Scholar 

  • Watters, J. J., Campbell, J. S., Cunningham, M. J., Krebs, E. G., & Dorsa, D. M. (1997). 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, 138, 4030–4033.

    Article  PubMed  CAS  Google Scholar 

  • Weiland, N. G. (1992). Estradiol selectively regulates agonist binding sites on the N-methyl-D-aspartate receptor complex in the CA1 region of the hippocampus. Endocrinology, 131, 662–668.

    Article  PubMed  CAS  Google Scholar 

  • Weiland, N. G., Orikasa, C., Hayashi, S., & McEwen, B. S. (1997). Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. The Journal of Comparative Neurology, 388, 603–612.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, M. E., Rosewell, K. L., Kashon, M. L., Shughrue, P. J., Merchenthaler, I., & Wise, P. M. (2002). Age differentially influences estrogen receptor-alpha (ERalpha) and estrogen receptor-beta (ERbeta) gene expression in specific regions of the rat brain. Mechanisms of Ageing and Development, 123, 593–601.

    Article  PubMed  CAS  Google Scholar 

  • Winder, D. G., & Sweatt, J. D. (2001). Roles of serine/threonine phosphatases in hippocampal synaptic plasticity. Nature Reviews. Neuroscience, 2, 461–474.

    Article  PubMed  CAS  Google Scholar 

  • Wise, P. M., Dubal, D. B., Rau, S. W., Brown, C. M., & Suzuki, S. (2005). Are estrogens protective or risk factors in brain injury and neurodegeneration? Reevaluation after the Women’s health initiative. Endocrine Reviews, 26, 308–312.

    Article  PubMed  CAS  Google Scholar 

  • Wong, M., & Moss, R. L. (1992). Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. The Journal of Neuroscience, 12, 3217–3225.

    PubMed  CAS  Google Scholar 

  • Woolley, C. S., Gould, E., Frankfurt, M., & McEwen, B. S. (1990). Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. The Journal of Neuroscience, 10, 4035–4039.

    PubMed  CAS  Google Scholar 

  • Woolley, C. S., & McEwen, B. S. (1994). Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. The Journal of Neuroscience, 14, 7680–7687.

    PubMed  CAS  Google Scholar 

  • Wu, T. W., Wang, J. M., Chen, S., & Brinton, R. D. (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.

    Article  PubMed  CAS  Google Scholar 

  • Xu, X., & Zhang, Z. (2006). Effects of estradiol benzoate on learning-memory behavior and synaptic structure in ovariectomized mice. Life Sciences, 79, 1553–1560.

    Article  PubMed  CAS  Google Scholar 

  • Yalcin, A., Kanit, L., Durmaz, G., Sargin, S., Terek, C. H., & Tanyolac, B. (2005) Altered level of apurinic/apyrimidinic endonuclease/redox factor-1 (APE/REF-1) mRNA in the hippocampus of ovariectomized rats treated by raloxifene against kainic acid. Cilinical and Experimental Pharmacology and Physiology, 32, 611–614.

    Google Scholar 

  • Zhao, L., Chen, S., Ming Wang, J., & Brinton, R. D. (2005). 17beta-estradiol induces Ca2+ influx, dendritic and nuclear Ca2+ rise and subsequent cyclic AMP response element-binding protein activation in hippocampal neurons: a potential initiation mechanism for estrogen neurotrophism. Neuroscience, 132, 299–311.

    Article  PubMed  CAS  Google Scholar 

  • Zhao, L., O’Neill, K., & Diaz Brinton, R. (2005). Selective estrogen receptor modulators (SERMs) for the brain: current status and remaining challenges for developing NeuroSERMs. Brain Research. Brain Research Reviews, 49, 472–493.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, J., Zhang, H., Cohen, R. S., & Pandey, S. C. (2005). Effects of estrogen treatment on expression of brain-derived neurotrophic factor and cAMP response element-binding protein expression and phosphorylation in rat amygdaloid and hippocampal structures. Neuroendocrinology, 81, 294–310.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Neuroscience, McKnight Brain Institute, University of Florida, 100244, Gainesville, FL, 32610-0244, USA

    Thomas C. Foster

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  1. Kristina K. Aenlle
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  1. Nathan S. Kline Institute for, Psychiatric Research, New York University, Old Orangeburg Road 140, Orangeburg, 10962, New York, USA

    James D Clelland

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Aenlle, K.K., Foster, T.C. (2011). Gene Expression and Signal Transduction Cascades Mediating Estrogen Effects on Memory. In: Clelland, J. (eds) Genomics, Proteomics, and the Nervous System. Advances in Neurobiology, vol 2. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7197-5_6

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