 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
Volume 16, Number 21, Issue of November 1, 1996 pp. 6830-6838
Copyright ©1996 Society for NeuroscienceDifferential Regulation of NMDAR1 mRNA and Protein by Estradiol in the Rat Hippocampus
Received June 17, 1996; revised July 25, 1996; accepted Aug. 16, 1996.
Adam H. Gazzaley1, Nancy G. Weiland3, Bruce S. McEwen3, and John H. Morrison1, 2 1 Laboratories for Neurobiology of Aging, Fishberg Research Center for Neurobiology, New York, New York 10029-6574, 2 Department of Geriatrics and Adult Development, The Mount Sinai School of Medicine, New York, New York 10029, and 3 Laboratory of Neuroendocrinology, Rockefeller University, New York, New York 10021
Estradiol treatment increases the number of NMDA receptor binding sites, and changes evoked synaptic currents in a manner consistent with a steroid-induced functional enhancement of NMDA receptors in rat hippocampus. In this study, we investigate the cellular mechanisms of estradiol-induced NMDA receptor regulation at the protein and mRNA levels in ovariectomized rats treated with ovarian steroids using immunocytochemical and in situ hybridization techniques. Confocal laser scanning microscopy was used to quantify alterations in immunofluorescence intensity levels of NMDAR1 subunit proteins within neuronal somata and dendrites of discrete hippocampal fields, whereas in parallel, in situ hybridization was used to examine NMDAR1 mRNA levels in corresponding hippocampal regions. The data indicate that estradiol treatment in ovariectomized rats significantly increases immunofluorescence intensity levels in comparison with nonsteroid treated ovariectomized rats within the somata and dendrites of CA1 pyramidal cells and, to a lesser extent, within the granule cell somata of the dentate gyrus. In contrast, such alterations in immunofluorescence intensity occur without concomitant changes in mRNA hybridization levels. Thus, these data suggest that estradiol modulates NMDA receptor function via post-transcriptional regulation of the NMDAR1 subunit protein. The increase in immunofluorescence intensity may reflect an increase in the concentration of the subunit protein, which could account for estrogen-induced changes in pharmacological and physiological properties of the NMDA receptor.
Key words: excitatory amino acid receptors; NMDAR1; immunocytochemistry; in situ hybridization; estrogen; CA1; confocal microscopy
This article has been cited by other articles:
J.-R. Chen, Y.-T. Yan, T.-J. Wang, L.-J. Chen, Y.-J. Wang, and G.-F. Tseng
Gonadal Hormones Modulate the Dendritic Spine Densities of Primary Cortical Pyramidal Neurons in Adult Female Rat
Cereb Cortex, November 1, 2009; 19(11): 2719 - 2727.
[Abstract] [Full Text] [PDF]
J. Sutcliffe, F. Rhaman, K. Marshall, and J. Neill
Oestradiol attenuates the cognitive deficit induced by acute phencyclidine treatment in mature female hooded-Lister rats
J Psychopharmacol, November 1, 2008; 22(8): 918 - 922.
[Abstract] [PDF]
M. A. Henson, A. C. Roberts, K. Salimi, S. Vadlamudi, R. M. Hamer, J. H. Gilmore, L. F. Jarskog, and B. D. Philpot
Developmental Regulation of the NMDA Receptor Subunits, NR3A and NR1, in Human Prefrontal Cortex
Cereb Cortex, November 1, 2008; 18(11): 2560 - 2573.
[Abstract] [Full Text] [PDF]
J. Hao, P. R. Rapp, W. G. M. Janssen, W. Lou, B. L. Lasley, P. R. Hof, and J. H. Morrison
Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex
PNAS, July 3, 2007; 104(27): 11465 - 11470.
[Abstract] [Full Text] [PDF]
K. B. Jelks, R. Wylie, C. L. Floyd, A. K. McAllister, and P. Wise
Estradiol Targets Synaptic Proteins to Induce Glutamatergic Synapse Formation in Cultured Hippocampal Neurons: Critical Role of Estrogen Receptor-{alpha}
J. Neurosci., June 27, 2007; 27(26): 6903 - 6913.
[Abstract] [Full Text] [PDF]
T. Jover-Mengual, R. S. Zukin, and A. M. Etgen
MAPK Signaling Is Critical to Estradiol Protection of CA1 Neurons in Global Ischemia
Endocrinology, March 1, 2007; 148(3): 1131 - 1143.
[Abstract] [Full Text] [PDF]
J. H. Morrison, R. D. Brinton, P. J. Schmidt, and A. C. Gore
Estrogen, Menopause, and the Aging Brain: How Basic Neuroscience Can Inform Hormone Therapy in Women
J. Neurosci., October 11, 2006; 26(41): 10332 - 10348.
[Full Text] [PDF]
J. Hao, P. R. Rapp, A. E. Leffler, S. R. Leffler, W. G. M. Janssen, W. Lou, H. McKay, J. A. Roberts, S. L. Wearne, P. R. Hof, et al.
Estrogen Alters Spine Number and Morphology in Prefrontal Cortex of Aged Female Rhesus Monkeys
J. Neurosci., March 1, 2006; 26(9): 2571 - 2578.
[Abstract] [Full Text] [PDF]
R. S. Peterson, L. Yarram, B. A Schlinger, and C. J Saldanha
Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain
Proc R Soc B, October 7, 2005; 272(1576): 2089 - 2096.
[Abstract] [Full Text] [PDF]
C. C. Smith and L. L. McMahon
Estrogen-Induced Increase in the Magnitude of Long-Term Potentiation Occurs Only When the Ratio of NMDA Transmission to AMPA Transmission Is Increased
J. Neurosci., August 24, 2005; 25(34): 7780 - 7791.
[Abstract] [Full Text] [PDF]
N. R. Miller, T. Jover, H. W. Cohen, R. S. Zukin, and A. M. Etgen
Estrogen Can Act via Estrogen Receptor {alpha} and {beta} to Protect Hippocampal Neurons against Global Ischemia-Induced Cell Death
Endocrinology, July 1, 2005; 146(7): 3070 - 3079.
[Abstract] [Full Text] [PDF]
C. Li, W. G. Brake, R. D. Romeo, J. C. Dunlop, M. Gordon, R. Buzescu, A. M. Magarinos, P. B. Allen, P. Greengard, V. Luine, et al.
Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice
PNAS, February 17, 2004; 101(7): 2185 - 2190.
[Abstract] [Full Text] [PDF]
Y. Tang, W. G.M. Janssen, J. Hao, J. A. Roberts, H. McKay, B. Lasley, P. B. Allen, P. Greengard, P. R. Rapp, J. H. Kordower, et al.
Estrogen Replacement Increases Spinophilin-immunoreactive Spine Number in the Prefrontal Cortex of Female Rhesus Monkeys
Cereb Cortex, February 1, 2004; 14(2): 215 - 223.
[Abstract] [Full Text] [PDF]
M. M. Adams and J. H. Morrison
Estrogen and the Aging Hippocampal Synapse
Cereb Cortex, December 1, 2003; 13(12): 1271 - 1275.
[Abstract] [Full Text] [PDF]
I. Chen
Focusing on the Big Picture
Sci. Aging Knowl. Environ., September 10, 2003; 2003(36): nf17 - 17.
[Abstract] [Full Text]
P. R. Rapp, J. H. Morrison, and J. A. Roberts
Cyclic Estrogen Replacement Improves Cognitive Function in Aged Ovariectomized Rhesus Monkeys
J. Neurosci., July 2, 2003; 23(13): 5708 - 5714.
[Abstract] [Full Text] [PDF]
W J Cutter, R Norbury, and D G M Murphy
Oestrogen, brain function, and neuropsychiatric disorders
J. Neurol. Neurosurg. Psychiatry, July 1, 2003; 74(7): 837 - 840.
[Full Text] [PDF]
Y. Ji, A. Z. Murphy, and R. J. Traub
Estrogen Modulates the Visceromotor Reflex and Responses of Spinal Dorsal Horn Neurons to Colorectal Stimulation in the Rat
J. Neurosci., May 1, 2003; 23(9): 3908 - 3915.
[Abstract] [Full Text] [PDF]
D. Yokomaku, T. Numakawa, Y. Numakawa, S. Suzuki, T. Matsumoto, N. Adachi, C. Nishio, T. Taguchi, and H. Hatanaka
Estrogen Enhances Depolarization-Induced Glutamate Release through Activation of Phosphatidylinositol 3-Kinase and Mitogen-Activated Protein Kinase in Cultured Hippocampal Neurons
Mol. Endocrinol., May 1, 2003; 17(5): 831 - 844.
[Abstract] [Full Text] [PDF]
V. Znamensky, K. T. Akama, B. S. McEwen, and T. A. Milner
Estrogen Levels Regulate the Subcellular Distribution of Phosphorylated Akt in Hippocampal CA1 Dendrites
J. Neurosci., March 15, 2003; 23(6): 2340 - 2347.
[Abstract] [Full Text] [PDF]
C. L. Jordan, S. E. Christensen, R. J. Handa, J. L. Anderson, W. A. Pouliot, and S. M. Breedlove
Evidence That Androgen Acts Through NMDA Receptors to Affect Motoneurons in the Rat Spinal Nucleus of the Bulbocavernosus
J. Neurosci., November 1, 2002; 22(21): 9567 - 9572.
[Abstract] [Full Text] [PDF]
L. Wang, S. Andersson, M. Warner, and J.-A. Gustafsson
Estrogen Actions in the Brain
Sci. Signal., June 25, 2002; 2002(138): pe29 - pe29.
[Abstract] [Full Text] [PDF]
Y. Shi and E. H. Schlenker
Neonatal sex steroids affect ventilatory responses to aspartic acid and NMDA receptor subunit 1 in rats
J Appl Physiol, June 1, 2002; 92(6): 2457 - 2466.
[Abstract] [Full Text] [PDF]
M. M. Adams, S. E. Fink, R. A. Shah, W. G. M. Janssen, S. Hayashi, T. A. Milner, B. S. McEwen, and J. H. Morrison
Estrogen and Aging Affect the Subcellular Distribution of Estrogen Receptor-alpha in the Hippocampus of Female Rats
J. Neurosci., May 1, 2002; 22(9): 3608 - 3614.
[Abstract] [Full Text] [PDF]
T. Jover, H. Tanaka, A. Calderone, K. Oguro, M. V. L. Bennett, A. M. Etgen, and R. S. Zukin
Estrogen Protects against Global Ischemia-Induced Neuronal Death and Prevents Activation of Apoptotic Signaling Cascades in the Hippocampal CA1
J. Neurosci., March 15, 2002; 22(6): 2115 - 2124.
[Abstract] [Full Text] [PDF]
D. N. D'Souza, R. E. Harlan, and M. M. Garcia
Sexually dimorphic effects of morphine and MK-801: sex steroid-dependent and -independent mechanisms
J Appl Physiol, February 1, 2002; 92(2): 493 - 503.
[Abstract] [Full Text] [PDF]
B. McEwen
Estrogen Actions Throughout the Brain
Recent Prog. Horm. Res., January 1, 2002; 57(1): 357 - 384.
[Abstract] [Full Text] [PDF]
B. S. McEwen
Genome and Hormones: Gender Differences in Physiology: Invited Review: Estrogens effects on the brain: multiple sites and molecular mechanisms
J Appl Physiol, December 1, 2001; 91(6): 2785 - 2801.
[Abstract] [Full Text] [PDF]
H.-K. Hsu, R.-C. Yang, H.-C. Shih, Y.-L. Hsieh, U-Y. Chen, and C. Hsu
Prenatal Exposure of Testosterone Prevents SDN-POA Neurons of Postnatal Male Rats From Apoptosis Through NMDA Receptor
J Neurophysiol, November 1, 2001; 86(5): 2374 - 2380.
[Abstract] [Full Text] [PDF]
C. N. Rudick and C. S. Woolley
Estrogen Regulates Functional Inhibition of Hippocampal CA1 Pyramidal Cells in the Adult Female Rat
J. Neurosci., September 1, 2001; 21(17): 6532 - 6543.
[Abstract] [Full Text] [PDF]
J.-y. Lan, V. A. Skeberdis, T. Jover, X. Zheng, M. V. L. Bennett, and R. S. Zukin
Activation of Metabotropic Glutamate Receptor 1 Accelerates NMDA Receptor Trafficking
J. Neurosci., August 15, 2001; 21(16): 6058 - 6068.
[Abstract] [Full Text] [PDF]
M. M. Adams, R. A. Shah, W. G. M. Janssen, and J. H. Morrison
Different modes of hippocampal plasticity in response to estrogen in young and aged female rats
PNAS, June 20, 2001; (2001) 141215898.
[Abstract] [Full Text] [PDF]
B. McEwen, K. Akama, S. Alves, W. G. Brake, K. Bulloch, S. Lee, C. Li, G. Yuen, and T. A. Milner
Tracking the estrogen receptor in neurons: Implications for estrogen-induced synapse formation
PNAS, June 19, 2001; 98(13): 7093 - 7100.
[Abstract] [Full Text] [PDF]
B. E. Cairns, B. J. Sessle, and J. W. Hu
Characteristics of Glutamate-Evoked Temporomandibular Joint Afferent Activity in the Rat
J Neurophysiol, June 1, 2001; 85(6): 2446 - 2454.
[Abstract] [Full Text] [PDF]
D. Marcantonio, L. E. Chalifour, M. A. Alaoui-Jamali, L. Alpert, and H. T. Huynh
Cloning and Characterization of a Novel Gene That Is Regulated by Estrogen and Is Associated with Mammary Gland Carcinogenesis
Endocrinology, June 1, 2001; 142(6): 2409 - 2418.
[Abstract] [Full Text] [PDF]
R. D. Brinton
Cellular and Molecular Mechanisms of Estrogen Regulation of Memory Function and Neuroprotection Against Alzheimer's Disease: Recent Insights and Remaining Challenges
Learn. Mem., May 1, 2001; 8(3): 121 - 133.
[Abstract] [Full Text] [PDF]
C. Harms, M. Lautenschlager, A. Bergk, J. Katchanov, D. Freyer, K. Kapinya, U. Herwig, D. Megow, U. Dirnagl, J. R. Weber, et al.
Differential Mechanisms of Neuroprotection by 17 {beta}-Estradiol in Apoptotic versus Necrotic Neurodegeneration
J. Neurosci., April 15, 2001; 21(8): 2600 - 2609.
[Abstract] [Full Text] [PDF]
V. A. Skeberdis, J.-y. Lan, X. Zheng, R. S. Zukin, and M. V. L. Bennett
Insulin promotes rapid delivery of N-methyl-D- aspartate receptors to the cell surface by exocytosis
PNAS, March 13, 2001; 98(6): 3561 - 3566.
[Abstract] [Full Text] [PDF]
W. G. Brake, S. E. Alves, J. C. Dunlop, S. J. Lee, K. Bulloch, P. B. Allen, P. Greengard, and B. S. McEwen
Novel Target Sites for Estrogen Action in the Dorsal Hippocampus: An Examination of Synaptic Proteins
Endocrinology, March 1, 2001; 142(3): 1284 - 1289.
[Abstract] [Full Text] [PDF]
E. J. Oh, L. P. Thompson, and D. Weinreich
Sexually Dimorphic Regulation of NK-1 Receptor-Mediated Electrophysiological Responses in Vagal Primary Afferent Neurons
J Neurophysiol, July 1, 2000; 84(1): 51 - 56.
[Abstract] [Full Text] [PDF]
F. Grodstein, R. Mayeux, and M. J. Stampfer
Tofu and Cognitive Function: Food for Thought
J. Am. Coll. Nutr., April 1, 2000; 19(2): 207 - 209.
[Full Text] [PDF]
A. L. Markowska
Sex Dimorphisms in the Rate of Age-Related Decline in Spatial Memory: Relevance to Alterations in the Estrous Cycle
J. Neurosci., September 15, 1999; 19(18): 8122 - 8133.
[Abstract] [Full Text] [PDF]
S. B. Wade, P. Oommen, W. C. Conner, D. J. Earnest, and R. C. Miranda
Overlapping and Divergent Actions of Estrogen and the Neurotrophins on Cell Fate and p53-Dependent Signal Transduction in Conditionally Immortalized Cerebral Cortical Neuroblasts
J. Neurosci., August 15, 1999; 19(16): 6994 - 7006.
[Abstract] [Full Text] [PDF]
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]
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, March 1, 1999; 81(3): 1404 - 1411.
[Abstract] [Full Text] [PDF]
B. S. McEwen, P. Tanapat, and N. G. Weiland
Inhibition of Dendritic Spine Induction on Hippocampal CA1 Pyramidal Neurons by a Nonsteroidal Estrogen Antagonist in Female Rats
Endocrinology, March 1, 1999; 140(3): 1044 - 1047.
[Abstract] [Full Text]
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, February 1, 1999; 81(2): 925 - 929.
[Abstract] [Full Text] [PDF]
S. M. Catalano, C. K. Chang, and C. J. Shatz
Activity-Dependent Regulation of NMDAR1 Immunoreactivity in the Developing Visual Cortex
J. Neurosci., November 1, 1997; 17(21): 8376 - 8390.
[Abstract] [Full Text] [PDF]
J. H. Morrison and P. R. Hof
Life and Death of Neurons in the Aging Brain
Science, October 17, 1997; 278(5337): 412 - 419.
[Abstract] [Full Text]
A. H. Gazzaley, D. L. Benson, G. W. Huntley, and J. H. Morrison
Differential Subcellular Regulation of NMDAR1 Protein and mRNA in Dendrites of Dentate Gyrus Granule Cells after Perforant Path Transection
J. Neurosci., March 15, 1997; 17(6): 2006 - 2017.
[Abstract] [Full Text] [PDF]
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., March 1, 1997; 17(5): 1848 - 1859.
[Abstract] [Full Text] [PDF]
S. Y. Grooms, T. Opitz, M. V. L. Bennett, and R. S. Zukin
Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death
PNAS, March 28, 2000; 97(7): 3631 - 3636.
[Abstract] [Full Text] [PDF]
M. M. Adams, R. A. Shah, W. G. M. Janssen, and J. H. Morrison
Different modes of hippocampal plasticity in response to estrogen in young and aged female rats
PNAS, July 3, 2001; 98(14): 8071 - 8076.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|