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The Journal of Neuroscience, April 1, 1998, 18(7):2550-2559

Estradiol Increases Dendritic Spine Density by Reducing GABA Neurotransmission in Hippocampal Neurons

Diane D. Murphy1, Nelson B. Cole2, V. Greenberger3, and Menahem Segal3

1 Laboratory of Neurobiology, National Institute of Neurological Diseases and Stroke, and 2 Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, and 3 Department of Neurobiology, The Weizmann Institute, Rehovot, 71600 Israel

We have previously shown that estradiol causes a twofold rise in dendritic spine density in cultured rat hippocampal neurons, as it does in vivo. More recently, estrogen receptors have been localized to aspiny inhibitory hippocampal interneurons, indicating that their effect on spiny pyramidal neurons may be indirect. We therefore examined the possibility that estradiol affects spine density by regulating inhibition in cultured hippocampal interneurons. Immunocytochemically, estrogen receptors were found to be co-localized with glutamate decarboxylase (GAD)-positive neurons (~21% of total neurons in the culture). Exposure of cultures to estradiol for 1 d caused a marked decrease (up to 80%) in the GAD content of the interneurons, measured both by immunohistochemistry and Western blotting. Also, the number of GAD-positive neurons in the cultures decreased to 12% of the total cell population. Moreover, GABAergic miniature IPSCs were reduced in both size and frequency by estradiol, whereas miniature EPSCs increased in frequency. We then mimicked the proposed effects of estradiol by blocking GABA synthesis with mercaptopropionic acid (MA). Cultures treated with MA expressed a dose-dependent decrease in GABA immunostaining that mimicked that seen with estradiol. MA-treated cultures displayed a significant 50% increase in dendritic spine density over controls, similar to that produced by estradiol. These results indicate that estradiol decreases GABAergic inhibition in the hippocampus, which appears to effectively increase the excitatory drive on pyramidal cells, and thus may provide a mechanism for formation of new dendritic spines.

Key words: hippocampus; dendritic spines; interneuron; estrogen receptors; GABA; cultures


Copyright © 1998 Society for Neuroscience  0270-6474/98/1872550-10$05.00/0


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Home page
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Home page
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Home page
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[Abstract] [Full Text] [PDF]


Home page
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[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
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Home page
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[Abstract] [Full Text] [PDF]


Home page
J. Neuropsychiatry Clin. Neurosi.Home page
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[Abstract] [Full Text] [PDF]


Home page
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Home page
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C. M. CHENG, M. COHEN, J. WANG, and C. A. BONDY
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[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
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Home page
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Endocrinology, March 1, 2001; 142(3): 1284 - 1289.
[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
C. Leranth, R. H. Roth, J. D. Elsworth, F. Naftolin, T. L. Horvath, and D. E. Redmond Jr
Estrogen Is Essential for Maintaining Nigrostriatal Dopamine Neurons in Primates: Implications for Parkinson's Disease and Memory
J. Neurosci., December 1, 2000; 20(23): 8604 - 8609.
[Abstract] [Full Text] [PDF]


Home page
J. Neurophysiol.Home page
M. R. Zamani, N. L Desmond, and W. B Levy
Estradiol Modulates Long-Term Synaptic Depression in Female Rat Hippocampus
J Neurophysiol, October 1, 2000; 84(4): 1800 - 1808.
[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
L. H. Calizo and L. M. Flanagan-Cato
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J. Neurosci., February 15, 2000; 20(4): 1589 - 1596.
[Abstract] [Full Text] [PDF]


Home page
Learn. Mem.Home page
H. L. Atwood and J. M. Wojtowicz
Silent Synapses in Neural Plasticity: Current Evidence
Learn. Mem., November 1, 1999; 6(6): 542 - 571.
[Abstract] [Full Text]


Home page
J. Neurosci.Home page
C. Flores, N. Salmaso, S. Cain, D. Rodaros, and J. Stewart
Ovariectomy of Adult Rats Leads to Increased Expression of Astrocytic Basic Fibroblast Growth Factor in the Ventral Tegmental Area and in Dopaminergic Projection Regions of the Entorhinal and Prefrontal Cortex
J. Neurosci., October 1, 1999; 19(19): 8665 - 8673.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
C. Patrone, S. Andersson, L. Korhonen, and D. Lindholm
Estrogen receptor-dependent regulation of sensory neuron survival in developing dorsal root ganglion
PNAS, September 14, 1999; 96(19): 10905 - 10910.
[Abstract] [Full Text] [PDF]


Home page
Endocr. Rev.Home page
B. S. McEwen and S. E. Alves
Estrogen Actions in the Central Nervous System
Endocr. Rev., June 1, 1999; 20(3): 279 - 307.
[Abstract] [Full Text]


Home page
J. Clin. Endocrinol. Metab.Home page
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The Molecular and Neuroanatomical Basis for Estrogen Effects in the Central Nervous System
J. Clin. Endocrinol. Metab., June 1, 1999; 84(6): 1790 - 1797.
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Home page
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Endocrinology, March 1, 1999; 140(3): 1044 - 1047.
[Abstract] [Full Text]


Home page
J. Neurosci.Home page
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J. Neurosci., February 15, 1999; 19(4): 1464 - 1472.
[Abstract] [Full Text] [PDF]


Home page
J. Neurosci.Home page
A. Shimada, C. A. Mason, and M. E. Morrison
TrkB Signaling Modulates Spine Density and Morphology Independent of Dendrite Structure in Cultured Neonatal Purkinje Cells
J. Neurosci., November 1, 1998; 18(21): 8559 - 8570.
[Abstract] [Full Text] [PDF]


Home page
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