Abstract
The rat adrenal hormone corticosterone reaches the brain and binds to intracellular receptors. These receptors comprise high-affinity mineralocorticoid and lower-affinity glucocorticoid receptors that, upon activation, affect the transcription rate of specific genes. The two receptor types are discretely localized in the brain, with particularly high expression levels in the hippocampus. Here we review recent studies showing that electrical properties and structural aspects of hippocampal principal neurons are specifically regulated by mineralocorticoid- or glucocorticoid-receptor activation. The molecular mechanisms by which these cellular effects could be accomplished are discussed.
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Ahima R. S. and Harlan R. E. (1990) Charting of Type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system.Neuroscience 39, 579–604.
Ahima R., Krozowski Z., and Harlan, R. (1991) Type I corticosteroid receptor-like immunoreactivity in the rat CNS: distribution and regulation by corticosteroids.J. Comp. Neurol. 313, 522–538.
Andrade R. and Nicoll R. A. (1997) Pharmacologically distinct actions of serotonin on single pyramidal neurones of the rat hippocampus recorded in vitro.J. Physiol. 394, 99–124.
Aronsson M., Fuxe K., Dong Y., Agnati L. E., Okret S., and Gustafsson J. A. (1988) Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization.Proc. Natl. Acad. Sci. USA 85, 9331–9335.
Arriza J. L., Simerly R. B., Swanson L. W., and Evans R. M. (1988) The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response.Neuron 1, 887–900.
Arriza J. L., Weinberger C., Cerelli G., Glaser T. M., Handelin B. L., Housman D. E., and Evans R. M. (1987) Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptors.Science 237, 268–275.
Auerbach J. M. and Segal M. (1996) Muscarinic receptor mediated depression and LTP in rat hippocampus.J. Physiol. 492, 479–493.
Auphan N., Didonato J. A., Rosette C., Helmberg A., and Karin M. (1995) Immunosuppression by glucocorticoids: inhibition of NF-kappa B activity through induction of I kappa B synthesis.Science 270, 286–90.
Bamberger C. M., Schulte H. M., and Chrousos G. P. (1996) Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids.Endocrinol. Rev. 17, 245–261.
Bamberger C. M., Bamberger A. M., de Castro M., and Chrousos G. P. (1995) Glucocorticoid receptor Β, a potential endogeneous inhibitor of glucocorticoid action in humans.J. Clin. Invest. 95, 2435–2441.
Barbany G. and Perrson H. (1993) Adrenalectomy attenuates kainic acid-elicited increases of messenger RNAs for neurotrophins and their receptors in the rat brain.Neuroscience 54, 909–922.
Beck S. G., Choi K. C., List T. J., Okuhara D. Y. and Birnstiel S. (1996) Corticosterone alters 5-HT1a receptor-mediated hyperpolarization in area CA1 hippocampal pyramidal neurons.Neuropsychopharmacol. 14, 27–33.
Beck S. G., List T. J., and Choi K. C. (1994) Longand short-term administration of corticosterone alters CA1 hippocampal neuronal properties.Neuroendocrinology 60, 261–272.
Birnstiel S. and Beck S. G. (1995) Modulation of the 5-hydroxytryptamine (4) receptor-mediated response by short-term and long-term administration of corticosterone in rat CA1 hippocampal pyramidal neurons.J. Pharmacol. Exp. Ther. 273, 1132–1138.
Bloem L.J., Guo C., and Pratt J. H. (1995) Identification of a splice variant of the rat and human mineralocorticoid receptor genes.J. Steroid Biochem. Molec. Biol. 55, 159–162.
Cameron H. A. and Gould E. (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus.Neuroscience 61, 203–209.
Chalmers D. T., Kwak S. P., Mansour A., and Watson S. J. (1993) Corticosteroids regulate brain hippocampal 5HTla receptor mRNA expression.J. Neurosci. 13, 914–923.
Chan Palay V. and Kohler Ch. (1989)The Hippocampus: New Vistas. Allan R. Liss, New York.
Chao H. M. and McEwen B. S. (1994) Glucocorticoids and the expression of mRNAs for neurotrophins, their receptors and GAP-43 in the rat hippocampus.Mol. Brain Res. 26, 271–276.
Chao H. M., Choo P. H., and McEwen B. S. (1989) Glucocorticoid and mineralocorticoid receptor mRNA expression in rat brain.Neuroendocrinology 50, 365–372.
Chee M., Yang R., Hubbell E., Berno A., Huang X. S., Sern D., Winkler J., Lockhart D. J., Morris M. S., and Fodor S. P. (1996) Accessing genetic information with high-density DNA arrays.Science 274, 610–614.
Coirini H., Magarinos A. M., DeNicola A. F., Rainbow T., and McEwen B. S. (1985). Further studies of brain aldosterone binding sites employing new mineralocorticoid and glucocorticoid receptor markers in vitro.Brain Res. 361, 212–216.
Cole T. J., Blendy J. A., Monaghan A. P., Krieglstein K., Schmid W., Aguzzi A., Fantuzzi G., Hummler E., Unsicker K., and Schütz G. (1995) Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation.Genes Dev. 9, 1608–1621.
Dallman M. F. (1993) Stress update. Adaptation of the hypothalamic-pituitary adrenal axis to chronic stress.Trends Endocrinol. Metab. 4, 62–69.
Defie A., Wu H., Reinke V., and Lozano G. (1993) The tumor suppressor p53 regulates its own transcrition.Mol. Cell Biol 13, 3415–3423.
De Kloet E. R. (1991) Brain corticosteroid receptor balance and homeostatic control.Front. Neuroendocrinol. 12, 95–164.
De Kloet E. R., Vreugdenhil E., Oitzl M. S., and JoËls M. (1997) Glucocorticoid feedback resistance.Trends Endocrinol. Metab. 8, 26–33.
De Kloet E. R., Wallach G., and McEwen B. S. (1975) Differences in corticosterone and dexamethasone binding to rat brain and pituitary.Endocrinology 96, 598–609.
Drouin J., Sun Y. L., Chamberland M., Gauthier Y., De L. A., Nemer M., and Schmidt T. J. (1993) Novel glucocorticoid receptor complex with DNA element of the hormone-repressed POMC gene.EMBO J. 12, 145–156.
Eberwine, J., Spencer, C., Miyashiro, K., Mackler, S. and Finnell, R. (1992) cDNA synthesis in situ: methods and applications, inMethods in Enzymology, Recombinant DNA, vol. 216 (Wu, G. R. ed.), Academic, pp. 80–100.
Elliot E. M. and Sapolsky R. M. (1992) Corticosterone enhances kainic acid induced calcium elevation in cultured hippocampal neurons.J. Neurochem. 59, 1033–1040.
Elliot E. M. and Sapolsky R. M. (1993) Corticosterone impairs hippocampal neuronal calcium regulation-possible mediating mechanisms.Brain Res. 602, 84–90.
Encio I. J. and Detera-Wadleigh S. D. (1991) The genomic structure of the human glucocorticoid receptor.J. Biol. Chem. 266, 7182–7188.
Evans R. M. (1988) The steroid and thyroid hormone receptor superfamily.Science 240, 889–895.
Funder J. W. (1993) Mineralocorticoids, glucocorticoids, receptors and response elements.Science 259, 1132–1133.
Fuxe K., Wikstrom A. C., Okret S., Agnatie L. F., Harfstrand A., Yu Z-Y., Granholm L., Zoli M., Vale W., and Gustafsson, J-A. (1985) Mapping of glucocorticoid receptor immunoreactive neurons in the rat tel- and diencephalon using a monoclonal antibody against rat liver glucocnrticoid receptors.Endocrinology 117, 1803–1812.
Gould E., Cameron H. A., and McEwen B. S. (1994) Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus.J Comp. Neurol. 340, 551–565.
Gould E. and McEwen B. S. (1993) Neuronal birth and death.Curr. Opi. Neurobiol. 3, 676–682.
Guardiola-Diaz H. M., Kolinske J. S., Gates L. H., and Seasholtz A. F. (1996) Negative glucocorticoid regulation of cyclic adenosine 3’,5’-monophosphate-stimulated corticotropin-releasing hormonereporter expression in AtT-20 cells.Mol. Endocr. 10, 317–329.
Hassan A. H., von Rosenstiel P., Patchev V. K., Holsboer F., and Almeida O. F. (1996) Exacerbation of apoptosis in the dentate gyrus of the aged rat by dexamethasone and the protective role of corticosterone.Exp. Neurol. 140, 43–52.
Heck S., Kullmann M., Gast A., Ponta H., Rahmsdorf H. J., Herrlich P., and Cato A. C. B. (1994) A distinct modulating domain in glucocorticoid receptor monomers in the repression of activity of transcription factor AP-1.EMBO J. 13, 4087–4095.
Herman J. P., Patel P. D., Akil H., and Watson S. J. (1989) Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat.Mol. Endocrinol. 3, 1886–1894.
Herman J. P. and Cullivan W. E. (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis.Trends Neurosci. 20, 78–84.
Hesen W., Karst H., Meijer O., Cole T. J., Schmid W., de Kloet E. R., Schütz G., and JoËls M. (1996) Hippocampal cell responses in mice with a targeted glucocorticoid receptor gene disruption.J. Neurosci. 16, 6766–6774.
Hesen W., Karten Y. J. G., van de Witte S. V., and JoËls M. (1998) Serotonin and carbachol induced suppression of synaptic excitability in rat CA1 hippocampal area: effects of corticosteroid receptor activation.J. Neuroendocrinol.,10, 9–19.
Hesen W. and JoËls M. (1993) Modulation of carbachol responsiveness in rat CA1 pyramidal neurons by corticosteroid hormones.Brain Res. 627, 159–167.
Hesen W. and JoËls M. (1996) Modulation of 5HT1A responsiveness in CA1 pyramidal neurons by in vivo activation of corticosteroid receptors.J. Neuroendocrinol. 8, 433–438.
Hesen W. and JoËls M. (1996) Cholinergic responsiveness of rat CA1 hippocampal neurons in vitro: modulation by corticosterone and stress.Stress 1, 65–73.
Hollenberg S. M., Weinberger C., Ong E. S., Cerelli G., Oro A., Lebo R., Thompson E. B., Rosenfeld M. G., and Evans R. M. (1985) Primary structure and expression of a functional human glucocorticoid receptor cDNA.Nature 318, 635–641.
Holmes M. C., Yau J. L., French K. L., and Seckl J. R. (1995) The effect of adrenalectomy on 5-hydroxytryptamine and corticosteroid receptor subtype messenger RNA expression in the rat.Neuroscience 64, 327–337.
Hornsby C. D. and de Kloet E. R. (1994) Dexamethasone does not prevent apoptosis in the hippocampus of the rat, inBrain Corticosteroid receptors, (de Kloet E. R., Azmitia E. C., and Landfield P. W., eds.) New York Acadamy of Sciences, New York, pp. 470–472.
Hornsby C. D., Grootendorst J., and de Kloet E. R. (1996) Dexamethasone does not prevent sevenday ADX-induced apoptosis in the dentate gyrus of the rat hippocampus.Stress 1, 51–64.
Jaarsma D., Postema F., and Korf J. (1992) Time course and distribution of neuronal degeneration in the dentate gyrus of rat after adrenalectomy: a silver impregnation study.Hippocampus 2, 143–150.
JoËls M. and de Kloet E. R. (1992) Control of neuronal excitability by corticosteroid hormones.Trends Neurosci. 15, 25–30.
JoËls M. and de Kloet E. R. (1994) Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems.Progr. Neurobiol. 43, 1–36.
JoËls M. (1997) Steroid hormones and excitability in the mammalian brain.Front. Neuroendocrinol. 18, 2–48.
JoËls M. and de Kloet E. R. (1989) Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus.Science 245, 1502–1505.
JoËls M., Werkman T., Karst H., Juta T., and Wadman W. (1998) Corticosteroids and calcium homeostasis: implication for neuroprotection and neurodegeneration, inNew Frontiers in Stress Research, Modulation of Brain Function, 40th OHOLO Conference, (de Kloet E. R., Ben Nathan D., Grauer E., and Levy D., eds.) Harwood, Chichester, UK, pp. 95–104.
JoËls M. and de Kloet E. R. (1990) Mineralocorticoid receptor-mediated changes in membrane properties of rat CA1 pyramidal neurons in vitro.Proc. Natl. Acad. Sci. USA 87, 4495–4498.
JoËls M., Hesen W., and de Kloet E. R. (1991) Mineralocorticoid hormones suppress serotonininduced hyperpolarization of rat hippocampal CA1 neurons.J. Neurosi. 11, 2288–2294.
JoËls M. and de Kloet E. R. (1992) Coordinative mineralocorticoid and glucocorticoid receptormediated control of responses to serotonin in rat hippocampus.Neuroendocrinology 55, 344–350.
Karst H., Wadman W. J., and JoËls M. (1994) Corticosteroid receptor-dependent modulation of calcium currents in rat hippocampal CA1 neurons.Brain Res. 649, 234–242.
Karst H., Werkman T. R., Struik M., Bosma A., and JoËls M. (1997) Influence of adrenalectomy on Ca2+-currents and Ca2+-channel subunit mRNA expression in hippocampal CA1 neurons of young rats.Synapse 26, 155–164.
Karst H., Wadman W. J., and JoËls M. (1993) Longterm control by corticosteroids of the inward rectifier in rat CA1 pyramidal neurons, in vitro.Brain Res. 612. 172–179.
Karst H., and JoËls M. (1991) The induction of corticosteroid actions on membrane properties of hippocampal CA1 neurons requires protein synthesis.Neurosci. Lett. 130, 27–32.
Kerr D. S., Campbell L. W., Hao S-Y, and Landfield P. W. (1989) Corticosteroid modulation of hippocampal potentials: increased effect with aging.Science 245, 1505–1507.
Kerr D. S., Campbell L. W., Thibault O., and Land-field P. W. (1992) Hippocampal glucocorticoid receptor activation enhances voltage-dependent Ca conductances: relevance to brain aging.Proc. Natl. Acad. Sci. USA 89, 8527–8531.
Knöpfel T., Vranesic I., GÄhwiler B. H., and Brown D. A. (1995) Muscarinic and Β-adrenergic depression of the slow Ca2+-activated potassium conductance in hippocampal CA3 pyramidal cells is not mediated by a reduction of depolarizationinduced cytosolic Ca2+ transients.Proc. Natl. Acad. Sci. USA 87, 4083–4087.
Krozowski Z. K. and Funder, J. W. (1983) Renal mineralocorticoid receptors and hippocampal corticosterone binding species have intrinsic steroid specificity.Proc. Natl. Acad. Sci. USA 80, 6056–6060.
Kwak S. P., Patel P. D., Thompson R. C., Akil H., and Watson S. J. (1993) 5’-Heterogeneity of the mineralocorticoid receptor messenger ribonucleic acid: differential expression and regulation of splice variants within the rat hippocampus.Endocrinology 133, 2344–2350.
Lambert J. J., Belelli D., Hill-Venning C., and Peters J. A. (1995) Neurosteroids and GABAa receptor function.Trends Pharmacol. Sci. 16, 295–303.
Leach Scully J. and Otten U. (1997) Glucocorticoid modulation of neurotrophin expression in immortalized mouse hippocampal neurons.Neurosci. Lett. 155, 11–14.
Lefstin J. A., Thomas J. R., and Yamamoto K. R. (1994) Influence of a steroid receptor DNA-binding domain on transcriptional regulatory functions.Genes Dev. 8, 2842–2856.
Liang P. and Pardee A. B. (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction.Science 257, 967–971.
Liao B., Miesak B., and Azmitia E. C. (1993) Loss of 5-HT1A receptor mRNA in the dentate gyrus of the long-term adrenalectomized rats and rapid reversal by dexamethasone.Mol. Brain Res. 19, 328–332.
Lipton S. A. (1997) Janus faces of NF-kappa B: Neurodestruction versus neuroprotection.Nature Medicine 3, 20–22.
Liu W., Wang J., Sauter N. K., and Pearce D. (1995) Steroid receptor heterodimerization demonstratedin vitro and in vivo.Proc. Natl. Acad. Sci. USA 92, 12480–12484.
Luine V., Martinez C., Villegas M., Magarinos A. M., and McEwen B. S. (1996) Restraint stress reversibly enhances spatial memory performance.Physiol. Behav. 59, 27–32.
Magarinos A. M., McEwen B. S., Flugge G., and Fuchs E. (1996) Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews.J. Neurosci. 16, 3534–3540.
Maiyar A. C., Phu P. T., Huang A. J., and Firestone G. L. (1997) Repression of glucocorticoid receptor transactivation and DNA binding of a glucocorticoid responsive element within the serum/glucocorticoid-inducible protein kiase (SKG) gene promotor by the p53 tumor suppressor protein.Mol. Endocrinol. 11, 312–329.
Majewska M. D. (1992) Neurosteroids: Endogenous bimodal modulators of the GABAa receptor. Mechanism of action and physiological significance.Prog. Neurobiol. 38, 379–395.
McEwen B. S., de Kloet E. R., and Rostene W. (1986) Adrenal steroid receptors and actions in the nervous system.Physiol. Rev. 66, 1121–1188.
McEwen B. S., Weiss J. M., and Schwartz L. S. (1968) Selective retention of corticosterone by limbic structures in rat brain.Nature 220, 911–912.
McEwen B. S. and Sapolsky R. M. (1995) Stress and cognitive function.Curr. Opi. Neurobiol. 5, 205–216.
Meberg P.J., Kinney W. R., Valcourt E. G., and Routtenberg A. (1996) Gene expression of the transcription factor NF-kappa B in hippocampus: regulation by synaptic activity.Mol. Brain Res. 38, 179–190.
Meijer O. C. and de Kloet E. R. (1994) Corticosterone suppresses the expression of 5-HT1a receptor mRNA in rat dentate gyrus.Eur. J. Pharmacol. 266, 255–261.
Meijer O. C. and de Kloet E. R. (1998) Corticosterone and serotonergic neurotransmission in the hippocampus: functional implications of central corticosteroid receptor diversity.Critical Rev. Neurobiol,12, 1–20.
Mendelsohn S. D. and McEwen B. S. (1992) Autoradiographic analyses of the effects of adrenalectomy and corticosterone on 5HT1A and 5HT1B receptors in the dorsal hippocampus and cortex of the rat.Neuroendocrinology 55, 444–451.
Meyer J. S. (1985) Biochemical effects of corticosteroids on neural tissues.Physiol. Rev. 65, 946–1020.
Minichiello L. and Klein R. (1996) TrkB and TrkC neurotrophin receptors cooperatein promoting survival of hippocampal and cerebellar granule neurons.Genes Bevel. 10, 2849–2858.
Miyashiti T., Krajewski S., Krajewski M., Wang H. G., Lin H. K., Liebermann D. A., Hoffman B., and Reed J. C. (1994) Tumor suppressor gene p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo.Oncogene 9, 1799–1805.
Miyashita T. and Reed J. C. (1995) Tumor Suppressor p53 is a direct transcriptional activator of the human bax gene.Cell 80, 293–299.
Nair S. M., Werkman T. R., Craig J., Finnell R., JoËls M., and Eberwine J. H. (1998) Corticosteroid regulation of ion channel conductances and mRNA levels in individual hippocampal CA1 neurons.J. Neurosci. 18, 2685–2696.
Nicoll R. A., Malenka R. C., and Kauer J. A. (1990) functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system.Physiol. Rev. 70, 513–565.
Oakley R. H., Sar M., and Cidlowski J. A. (1996) The human glucocorticoid receptor Β-isoform. Expression, biochemical properties and putative function.J. Biol. Chem. 271, 9550–9559.
Oitzl M. S. and de Kloet E. R. (1992) Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning.Behav. Neuroscience 106, 62–71.
Okuhara D. Y., Beck S. G., and Muma N. A. (1997) Corticosterone alters G protein a-subunit levels in the rat hippocampus.Brain Res 745, 144–151.
O’Neill L. A. J. and Kaltschmidt C. (1997) NF-kappaB: a crucial transcription factor for glial and neuronal cell function.Trends Neurosci. 20, 252–258.
Packan D. R. and Sapolsky R. M. (1990) Glucocorticoid endangerment of the hippocampus: tissue, steroid and receptor specificity.Neuroendocrinology 51, 613–618.
Paul S. M. and Purdy R. H. (1992) Neuroective steroids.FASEB J. 6, 2311–2322.
Pearce D. and Yamamoto K. R. (1993) Mineralocorticoid and glucocorticoid receptor activities distinguished by nonreceptor factors at a composite response element.Science 259, 1161–1165.
Pfaff D. W., Silva M. T. A., and Weiss J. M. (1971) Telemetered recording of hormone effects on hippocampal neurons.Science 171, 394–395.
Pfahl M. (1993) Nuclear receptor / AP-1 interaction.Endocrinol. Rev. 14, 651–658.
Qiao, X. X., Hughes P. E., Venero J. L., Dugichdjevic M. M., Nichols N. R., Hefti F., and Knusel B. (1996) NT 4/5 protects against adrenalectomy induced apoptosis of rat hippocampal granule cells.Neuroreport 7, 682–686.
Ray A. and Prefontaine K. E. (1994) Physical interaction and functional antagonism between the p65 subunit of transcrition factor NF-kappaB and the glucocorticoid receptor.Proc. Natl. Acad. Sci. USA 91, 752–756.
Reul J. M. H. M. and de Kloet E. R. (1985) Two receptor systems for corticosterone in rat brain: microdissection and differential occupation.Endocrinology 117, 2505–2512.
Reul J. M. H. M., Van den Bosch J. R., and de Kloet, E. R. (1987a) Differential response of type 1 and type 2 corticosteroid receptors to changes in plasma steroid levels and circadian rhythmicity.Neuroendocrinology 45, 407–412.
Reul J. M. H. M., Van den Bosch J. R., and de Kloet, E. R. (1987b) Relative occupation of type 1 and type 2 corticosteroid receptors in rat brain following stress and dexamethasone treatment: functional implications.J. Endocrinol. 115, 459–467.
Saito N., Guitart X., Hayward M., Tallman J. F., Duman R. S., and Nestler E.J. 1989 Corticosterone differentially regulates the expression of Gsa and Gia messenger RNA and protein in rat cerebral cortex.Proc. Natl. Acad. Sci. USA 86, 3906–3910.
Sakhi S., Bruce A., Sun N., Tocco G., Baudry M., Schreiber S. S. (1994) p53 induction is associated with neuronal damage in the central nervous system.Proc. Natl. Acad. Sci. USA 91, 7525–7579.
Sapolsky R., Krey L., and McEwen B. (1985) Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging.J. Neurosci. 5, 1221–1227.
Sapolsky R. M. (1996) Stress, glucocorticoids, and damage to the nervous system: the current state of confusion.Stress 1, 1–19.
Schaaf M. J. M., Hoetelmans R. W. M., de Kloet E. R. and Vreugdenhil E. (1997) Corticosterone regulates expression of BDNF and trkB, but not NT-3 and trkC mRNA in the rat hippocampus.J. Neurosci. Res., in press.
Schmitz D., Empson R. M., and Heinemann U. (1995) Serotonin and 8-OH-DPAT reduce excitatory synaptic transmission in rat hippocampal area via reduction in presumed presynaptic Ca2+ entry.Brain Res. 701, 249–254.
Schreiber S. S., Sakhi S., Dugichdjordjevic M. M., and Nichols N. R. (1994) Tumor suppressor p53 induction and DNA damage in hippocampal granule cells after adrenalectomy.Exp. Neurol. 30, 368–376.
Sloviter R. S., Dean E., Sollas A. L., and Goodman J. H. (1996) Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat.J Comp. Neurol. 366, 516–533.
Sloviter R. S., Sollas A. L., Dean E., and Neubort S. (1993) Adrenalectomy-induced granule cell degeneration in the rat hippocampal dentate gyrus: characterization of an in vivo model of controlled neuronal death.J Comp. Neurol. 330, 324–336.
Sloviter R. S., Sollas A. L., and Neubort S. (1995) Hippocampal dentate granule cell degeneration after adrenalectomy in the rat is not reversed by dexamethasone.Brain Res. 682, 227–230.
Sloviter R. S., Valiquette G., Abrams G. M., Ronk E., Sollas A., Paul L. A., and Neubort S. (1989) Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy.Science 243, 535–538.
Smith D. F. and Toft D. O. (1993) Steroid receptors and their associated proteins.Mol. Endocrinol. 7, 4–11.
Smith M. A., Makino S., Kvetnansky R., and Post R. M. (1995) Stress and glucocorticoids affect the expression of Brain Derived Neurotrophic Factor and Neurotrophin 3 mRNAs in the hippocampus.J. Neurosci. 15, 1768–1777.
Storm J. F. (1990) Potassium currents in hippocampal pyramidal cells.Progr. Brain Res. 83, 161–187.
Thibault O., and Landfield P. W. (1996) Increase in single L-type calcium channels in hippocampal neurons during aging.Science 272, 1017–1020.
Trapp T., Rupprecht R., Castren M., Reul J. M., and Holsboer F. (1994) Heterodimerization between mineralocorticoid and glucocorticoid receptor: a new principle of glucocorticoid action in the CNS.Neuron 13, 1457–1462.
Truss M. and Beato M. (1993) Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors.Endocr. Rev. 14, 459–479.
Unlap T. and Jope R. S. (1994) Dexamethasone attenuates kainate-induced AP-1 activation in rat brain.Mol. Brain Res. 24, 275–282.
Unlap T. and Jope R. S. (1995) Diurnal variation in kainate-induced AP-1 activation in rat brain: influence of glucocorticoids.Mol Brain Res. 28, 193–200.
Van Eekelen, J. A. M., Jiang, W., de Kloet, E. R., and Bohn, M. C. (1988) Distribution of the mineralocorticoid and glucocorticoid receptor mRNAs in the rat hippocampus.J. Neurosci. Res. 21, 88–94.
Van Eekelen J. A. M., Kiss J. Z., Westphal H. M., and de Kloet, E. R. (1987) Immunocytochemical study on the intracellular localization of the Type 2 glucocorticoid receptor in the rat brain.Brain Res. 436, 120–128.
Van Steensel B., van Binnendijk E. P., Hornsby C. D., van der Voort H. T. M., de Kloet E. R., and van Driel R. (1995) Partial cocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampal neurons.J.Cell Sci. 109, 787–792.
Velculescu V. U., Zhang L., Vogelstein B., and Kinzler K. W. (1995) Serial analysis of gene expression.Science 270, 484–487.
Vreugdenhil E., de Jong J., Schaaf M. J. M., Meijer O. C., Busscher J., Vuijst C., and de Kloet E. R. (1996) Molecular dissection of corticosteroid action in the rat hippocampus.J. Mol. Neurosci. 7, 135–146.
Werkman T. R., van der Linden S., and JoËls M. (1997) Corticosteroid effects on Na+ and Ca2+ currents in acutely dissociated rat CA1 hippocampal neurons.Neuroscience 78, 663–672.
Woolley C. S., Gould E., and McEwen B. S. (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons.Brain Res. 531, 225–231.
Woolley C. S., Gould E., Sakai R. R., Spencer R. L., and McEwen B. S. (1991) Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat.Brain Res. 554, 312–315.
Yang N. N., Venugopalan M., Hardikar S., and Glasebrook A. (1996) Identification of an estrogen response element activated by metabolites of 17-estradiol amd raloxifene.Science 273, 1222–1225.
Zeise M. L., Teschemacher A., Arriagada J., and ZieglgÄnsberger W. (1992) Corticosterone reduces synaptic inhibition in rat hippocampal and neocortical neurons in vitro.J. Neuroendocrinol. 4, 107–112.
Zennaro M., Keightley C., Kotelevtsev Y., Conway G. S., Soubrier F., and Fuller P. J. (1995) Human mineralocorticoid receptor genomic structure and identification of expressed isoforms.J. Biol. Chem. 270 21016–21020.
Zilliacus J., Wright A. P. H., Carlstedt-Duke J., and Gustafsson J-A. (1995) Structural determinants of DNA-binding specificity by steroid receptors.Mol. Endocrinol. 9, 389–400.
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JoËls, M., Vreugdenhil, E. Corticosteroids in the brain. Mol Neurobiol 17, 87–108 (1998). https://doi.org/10.1007/BF02802026
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DOI: https://doi.org/10.1007/BF02802026