Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons

Journal of Neuroscience

Volumn 18, Issue 7, 1998, Pages 2550-2559

  Murphy, Diane D ^a   Cole, Nelson B ^b   Greenberger, V ^c   Segal, Menahem ^c  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Cultures; Dendritic spines; Estrogen receptors; GABA; Hippocampus; Interneuron

Indexed keywords

4 AMINOBUTYRIC ACID; ESTRADIOL; ESTROGEN RECEPTOR; GLUTAMATE DECARBOXYLASE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DENDRITIC SPINE; EMBRYO; ESTROGEN RELEASE; GABAERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

EID: 0032053426     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-07-02550.1998     Document Type: Article

References (36)

1. Berninger B, Marty S, Zafra F, Berzaghi M, Thoenen H, Lindholm D (1995) GABAergic Stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 121:2327-2335.
2. Brinton RD, Tran J, Proffitt P, Montoya M (1997) 17-Beta-estradiol enhances the outgrowth and survival of neocortical neurons in culture. Neurochem Res 22:1339-1351.
3. Buterbaugh GG, Hudson GM (1991) Estradiol replacement to female rats facilitates dorsal hippocampal but not ventral hippocampal kindled seizure acquisition. Exp Neurol 111:55-64.
4. Cao Y, Wilcox KS, Martin CE, Rachinsky TE, Eberwine J, Dichter MA (1996) Presence of mRNA for glutamic acid decarboxylase in both excitatory and inhibitory neurons. Proc Natl Acad Sci USA 93:9844-9849.
5. Davis AM, Grattan DR, Selmanoff M, McCarthy MM (1996) Sex differences in glutamic acid decarboxylase mRNA in neonatal rat brain: implications for sexual differentiation. Horm Behav 30: 538-552.
6. Deisseroth K, Bito H, Tsien R (1996) Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal plasticity. Neuron 16:89-101.
7. Erecinska M, Nelson D, Daikhin Y, Yudhoff M (1996) Regulation of GABA level in rat brain synaptosomes: fluxes through enzymes of the GABA shunt and effects of glutamate, calcium, and ketone bodies. J Neurochem 67:2325-2334.
8. Feldblum S, Dumoulin A, Anoal M, Sandillon F, Privat A (1995) Comparative distribution of GAD65 and GAD67 mRNAs and proteins in the rat spinal cord supports a differential regulation of these two glutamate decarboxylases in vivo. J Neurosci Res 42:742-757.
9. Harris KM, Kater SB (1994) Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17:341-371.
10. Henderson VW (1997) The epidemiology of estrogen replacement therapy and Alzheimer's disease. Neurology 48[Suppl 7]:S27-S35.
11. Jussofie A, Korner I, Schell C, Hienke C (1995) Time course of the effects of steroid hormone deprivation elicited by ovarietomy or ovariectomy plus adrenalectomy on the affinity and density of GABA binding sites in distinct rat brain areas. Exp Clin Endocrinol Diabetes 103:196-204.
12. Kampen DL, Sherwin BB (1996) Estradiol is related to visual memory in healthy young men. Behav Neurosci 110:613-617.
13. Kuiper G, Gustaffson J (1997) The novel estrogen receptor-β subtype: potential role in the cell and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 410:87-90.
14. Li X, Schwartz PE, Rissman EF (1997) Distribution of estrogen receptor-β-like immunoreactivity in rat forebrain. Neuroendocrinology 66:63-67.
15. 2+/ calmodulin-dependent protein kinase II gene expression in rat cerebral cortex. Exp Brain Res 110:163-174.
16. McCarthy MM, Kaufman LC Brooks PJ, Pfaff DW, Schwartz-Giblin S (1995) Estrogen modulation of nRNA levels for the two forms of glutamic acid decarboxylase (GAD) in female rat brain. J Comp Neurol 360:685-697.
17. Marty S, Berninger B, Carroll P, Thoenen H (1996) GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 16:565-570.
18. Murphy DD, Segal M (1996) Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16:4059-4068.
19. Murphy DD, Segal M (1997) Morphological plasticity of dendritic spines in central neurons is mediated by activation of cAMP response element binding protein. Proc Natl Acad Sci USA 94:1482-1487.
20. Netopilova M, Drsata J, Kubova H, Mares P (1995) Differences between immature and adult rats in brain glutamate decarboxylase inhibition by 3-mercaptopropionic acid. Epilepsy Res 20:179-184.
21. Netopilova M, Drsata J, Haugvicova R, Kubova H, Mares P (1997) Inhibition of glutamate decarboxylase activity by 3-mercaptopropionic acid has different time course in the immature and adult rat brains. Neurosci Lett 226:68-70.
22. Packard MG, Kohlmaier JR, Alexander GM (1996) Posttraining intrahippocampal estradiol injections enhance spatial memory in male rats: interaction with cholinergic systems. Behav Neurosci 110:626-632.
23. Papa M, Segal M (1996) Morphological plasticity in dendritic spines of cultured hippocampal neurons. Neuroscience 71:1005-1011.
24. Papa M, Bundman MC, Greenberger V, Segal M (1995) Morphological analysis of the development of dendritic spines in primary cultures of hippocampal neurons. J Neurosci 15:1-11.
25. Pericic D, Manev H, Bujas M (1996) Gonadal hormones and picrotoxin-induced convulsions in male and female rats. Brain Res 736:174-179.
26. Rodriguez Macias KA (1996) Catamenial epilepsy: gynecological and hormonal implications. Five case reports. Gynecol Endocrinol 10:139-142.
27. Segal M (1983) Rat hippocampal neurons in culture: responses to electrical and chemical stimuli. J Neurophysiol 50:1249-1264.
28. Terasawa E, Timiras PL (1968) Electrical activity during the estrous cycle of the rat: cyclical changes in limbic structures. Endocrinology 83:207-216.
29. Unda R, Brann DW, Mahesh VB (1995) Progesterone suppression of glutamic acid decarboxylase (GAD67) levels in the preoptic area: correlation with luteinizing hormone surge. Neuroendocrinology 62:562-570.
30. Weiland NG, Orchinik M (1995) Specific subunit mRNAs of the GABAa receptor are regulated by progesterone in subfields of the hippocampus. Mol Brain Res 32:271-278.
31. Weiland NG, Orikasa C, Hayashi S, McEwen BS (1996) Localization of estrogen receptors in the hippocampus of male and female rats. Soc Neurosci Abstr 22:618.
32. Wong M, Moss RL (1992) Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J Neurosci 12:3217-3225.
33. Woolley CS, McEwen BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554.
34. Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA (1997) Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor mediated synaptic input: correlation with dendritic spine density. J Neurosci 17:1848-1859.
35. Xu J, Xie X, Brinton RD, Berger TW (1997) Direct enhancement of NMDA receptor-mediated EPSPs by 17β-estradiol in hippocampal CA1. Soc Neurosci Abstr 23:2104.
36. Yamada M, Wada Y, Tsukagoshi H, Otmo E, Hayakawa M (1988) A quantitative Golgi study of basal dendrites of hippocampal C1 pyramidal cells in senile dementia of Alzheimer's type. J Neurol Neurosurg Psychiatry 51:1088-1090.