 |
 Previous Article | Next Article 
Volume 16, Number 11,
Issue of June 1, 1996
pp. 3620-3629
Copyright ©1996 Society for Neuroscience
17 -Estradiol Potentiates Kainate-Induced Currents via
Activation of the cAMP Cascade
Received Jan. 5, 1996; revised Feb. 27, 1996; accepted March 8, 1996.
Qin Gu and
Robert L. Moss
Department of Physiology, University of Texas Southwestern Medical
Center at Dallas, Dallas, Texas 75235
Evidence for nongenomic actions of steroids is now coming from a
variety of fields of steroid research. Mechanisms of steroid action are
being studied with regard to the membrane receptors and the activation
of second messengers. The present study investigated the mechanism for
the rapid effect of estrogen on acutely dissociated hippocampal CA1
neurons by using the whole-cell, voltage-clamp recording. Under the
perforated patch configuration, 17 -estradiol potentiated
kainate-induced currents in 38% of tested neurons. The potentiation
was stereospecific, rapid in onset, and reversible after the removal of
the steroid. Dose-response curves show that the potentiation by
17-estradiol was evident at a concentration as low as 10 nM and saturated at 10 µM. 17-Estradiol did not affect the kinetics
(i.e., affinity and cooperativity) and reversal potential of
kainate-induced currents. This suggests that the potentiation did not
result from direct interaction with kainate receptors nor the
activation of ion channels other than kainate receptor-channels. The
potentiation by 17-estradiol was similar to the enhancement of
kainate-induced currents evoked by 8-bromo-cAMP, and was modulated by
an inhibitor of phosphodiesterase (IBMX). The estrogen potentiation was
blocked by a specific blocker of PKA (Rp-cAMPS). Under
standard recording configuration, the effect was significantly affected
by intracellular perfusing with GDP--S or GTP- -S. The data
suggest that the potentiation of kainate-induced currents by
17-estradiol was likely a G-protein(s) coupled, cAMP-dependent
phosphorylation event. By involvement of this nongenomic mechanism,
estrogen may play a role in the modulation of excitatory synaptic
transmission in the hippocampus.
Key words:
steroid hormone;
modulator;
non-NMDA receptor;
inward current;
PKA;
G-protein;
nongenomic
This article has been cited by other articles:
|
|
|
|
 
A. R. Gintzler, S. A. Schnell, D. S. Gupta, N.-J. Liu, and M. W. Wessendorf
Relationship of Spinal Dynorphin Neurons to {delta}-Opioid Receptors and Estrogen Receptor {alpha}: Anatomical Basis for Ovarian Sex Steroid Opioid Antinociception
J. Pharmacol. Exp. Ther.,
September 1, 2008;
326(3):
725 - 731.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Schubert, C. Drephal, and D. Albrecht
Gender-dependent ATPA-induced changes in long-term potentiation in the rat lateral amygdala
FASEB J,
April 1, 2008;
22(4):
1268 - 1274.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Dewing, M. I. Boulware, K. Sinchak, A. Christensen, P. G. Mermelstein, and P. Micevych
Membrane Estrogen Receptor-{alpha} Interactions with Metabotropic Glutamate Receptor 1a Modulate Female Sexual Receptivity in Rats
J. Neurosci.,
August 29, 2007;
27(35):
9294 - 9300.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Ish, T. Tsurugizawa, M. Ogiue-Ikeda, M. Asashima, H. Mukai, G. Murakami, Y. Hojo, T. Kimoto, and S. Kawato
Local Production of Sex Hormones and Their Modulation of Hippocampal Synaptic Plasticity
Neuroscientist,
August 1, 2007;
13(4):
323 - 334.
[Abstract]
[PDF]
|
|
|
|
|
|
|
B. C. Trainor, S. Lin, M. S. Finy*, M. R. Rowland, and R. J. Nelson
Photoperiod reverses the effects of estrogens on male aggression via genomic and nongenomic pathways
PNAS,
June 5, 2007;
104(23):
9840 - 9845.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Vasudevan and D. W. Pfaff
Membrane-Initiated Actions of Estrogens in Neuroendocrinology: Emerging Principles
Endocr. Rev.,
February 1, 2007;
28(1):
1 - 19.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. M. Broad, R. Zwart, K. H. Pearson, M. Lee, L. Wallace, G. I. McPhie, R. Emkey, S. P. Hollinshead, C. P. Dell, S. R. Baker, et al.
Identification and Pharmacological Profile of a New Class of Selective Nicotinic Acetylcholine Receptor Potentiators
J. Pharmacol. Exp. Ther.,
September 1, 2006;
318(3):
1108 - 1117.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. B. Dubal, S. W. Rau, P. J. Shughrue, H. Zhu, J. Yu, A. B. Cashion, S. Suzuki, L. M. Gerhold, M. B. Bottner, S. B. Dubal, et al.
Differential Modulation of Estrogen Receptors (ERs) in Ischemic Brain Injury: A Role for ER{alpha} in Estradiol-Mediated Protection against Delayed Cell Death
Endocrinology,
June 1, 2006;
147(6):
3076 - 3084.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. A. Verriere, D. Hynes, S. Faherty, J. Devaney, J. Bousquet, B. J. Harvey, and V. Urbach
Rapid Effects of Dexamethasone on Intracellular pH and Na+/H+ Exchanger Activity in Human Bronchial Epithelial Cells
J. Biol. Chem.,
October 28, 2005;
280(43):
35807 - 35814.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Sedej, T. Rose, and M. Rupnik
cAMP increases Ca2+-dependent exocytosis through both PKA and Epac2 in mouse melanotrophs from pituitary tissue slices
J. Physiol.,
September 15, 2005;
567(3):
799 - 813.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Matagne, M.-C. Lebrethon, A. Gerard, and J.-P. Bourguignon
Kainate/Estrogen Receptor Involvement in Rapid Estradiol Effects in Vitro and Intracellular Signaling Pathways
Endocrinology,
May 1, 2005;
146(5):
2313 - 2323.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. L. Temple, E. Laing, A. Sunder, and S. Wray
Direct Action of Estradiol on Gonadotropin-Releasing Hormone-1 Neuronal Activity via a Transcription-Dependent Mechanism
J. Neurosci.,
July 14, 2004;
24(28):
6326 - 6333.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. E. Navarro, S. A. Saeed, C. Murdock, A. J. Martinez-Fuentes, K. K. Arora, L. Z. Krsmanovic, and K. J. Catt
Erratum
Mol. Endocrinol.,
December 1, 2003;
17(12):
A - 2658.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Qiu, M. A. Bosch, S. C. Tobias, D. K. Grandy, T. S. Scanlan, O. K. Ronnekleiv, and M. J. Kelly
Rapid Signaling of Estrogen in Hypothalamic Neurons Involves a Novel G-Protein-Coupled Estrogen Receptor that Activates Protein Kinase C
J. Neurosci.,
October 22, 2003;
23(29):
9529 - 9540.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
O. A. Sukocheva, L. Wang, N. Albanese, S. M. Pitson, M. A. Vadas, and P. Xia
Sphingosine Kinase Transmits Estrogen Signaling in Human Breast Cancer Cells
Mol. Endocrinol.,
October 1, 2003;
17(10):
2002 - 2012.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. E. Navarro, S. Abdul Saeed, C. Murdock, A. J. Martinez-Fuentes, K. K. Arora, L. Z. Krsmanovic, and K. J. Catt
Regulation of Cyclic Adenosine 3',5'-Monophosphate Signaling and Pulsatile Neurosecretion by Gi-coupled Plasma Membrane Estrogen Receptors in Immortalized Gonadotropin-Releasing Hormone Neurons
Mol. Endocrinol.,
September 1, 2003;
17(9):
1792 - 1804.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Foldvary-Schaefer and T. Falcone
Catamenial epilepsy: Pathophysiology, diagnosis, and management
Neurology,
September 1, 2003;
61(90062):
S2 - 15.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
I. M. Abraham, S.-K. Han, M. G. Todman, K. S. Korach, and A. E. Herbison
Estrogen Receptor {beta} Mediates Rapid Estrogen Actions on Gonadotropin-Releasing Hormone Neurons In Vivo
J. Neurosci.,
July 2, 2003;
23(13):
5771 - 5777.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. M. LOSEL, E. FALKENSTEIN, M. FEURING, A. SCHULTZ, H.-C. TILLMANN, K. ROSSOL-HASEROTH, and M. WEHLING
Nongenomic Steroid Action: Controversies, Questions, and Answers
Physiol Rev,
July 1, 2003;
83(3):
965 - 1016.
[Abstract]
[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]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
S. L. Hardy, G. M. Anderson, M. Valent, J. M. Connors, and R. L. Goodman
Evidence That Estrogen Receptor Alpha, but Not Beta, Mediates Seasonal Changes in the Response of the Ovine Retrochiasmatic Area to Estradiol
Biol Reprod,
March 1, 2003;
68(3):
846 - 852.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. N. Rudick and C. S. Woolley
Selective Estrogen Receptor Modulators Regulate Phasic Activation of Hippocampal CA1 Pyramidal Cells by Estrogen
Endocrinology,
January 1, 2003;
144(1):
179 - 187.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Kumar and T. C. Foster
17beta -Estradiol Benzoate Decreases the AHP Amplitude in CA1 Pyramidal Neurons
J Neurophysiol,
August 1, 2002;
88(2):
621 - 626.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. D. Machado, C. Alonso, A. Morales, J. F. Gomez, and R. Borges
Nongenomic Regulation of the Kinetics of Exocytosis by Estrogens
J. Pharmacol. Exp. Ther.,
May 1, 2002;
301(2):
631 - 637.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Curtis, B. Buisson, S. Bertrand, and D. Bertrand
Potentiation of Human alpha 4beta 2 Neuronal Nicotinic Acetylcholine Receptor by Estradiol
Mol. Pharmacol.,
January 1, 2002;
61(1):
127 - 135.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. B. Wade, S. Robinson, R. A. Shapiro, and D. M. Dorsa
Estrogen Receptor (ER){{alpha}} and ER{beta} Exhibit Unique Pharmacologic Properties When Coupled to Activation of the Mitogen-Activated Protein Kinase Pathway
Endocrinology,
June 1, 2001;
142(6):
2336 - 2342.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Falkenstein, H.-C. Tillmann, M. Christ, M. Feuring, and M. Wehling
Multiple Actions of Steroid Hormones---A Focus on Rapid, Nongenomic Effects
Pharmacol. Rev.,
December 1, 2000;
52(4):
513 - 556.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. L. Goodman, J.-C. Thiery, B. Delaleu, and B. Malpaux
Estradiol Increases Multiunit Electrical Activity in the A15 Area of Ewes Exposed to Inhibitory Photoperiods
Biol Reprod,
November 1, 2000;
63(5):
1352 - 1357.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
I. Stefanovic, B. Adrian, H. T. Jansen, M. N. Lehman, and R. L. Goodman
The Ability of Estradiol to Induce Fos Expression in a Subset of Estrogen Receptor-{alpha}-Containing Neurons in the Preoptic Area of the Ewe Depends on Reproductive Status
Endocrinology,
January 1, 2000;
141(1):
190 - 196.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. B. Dubal, P. J. Shughrue, M. E. Wilson, I. Merchenthaler, and P. M. Wise
Estradiol Modulates bcl-2 in Cerebral Ischemia: A Potential Role for Estrogen Receptors
J. Neurosci.,
August 1, 1999;
19(15):
6385 - 6393.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. M. Wise, M. J. Smith, D. B. Dubal, M. E. Wilson, K. M. Krajnak, and K. L. Rosewell
Neuroendocrine Influences and Repercussions of the Menopause
Endocr. Rev.,
June 1, 1999;
20(3):
243 - 248.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
K. Kasischke, R. Huber, H. Li, M. Timmler, M. W. Riepe, and D. O. Carpenter
Primary Hypoxic Tolerance and Chemical Preconditioning During Estrus Cycle in Mice • Editorial Comment
Stroke,
June 1, 1999;
30(6):
1256 - 1262.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. G. Green, S. R. Dahlqvist, W. M. Isenberg, H. J. Strausbaugh, F. J.-P. Miao, and J. D. Levine
Sex Steroid Regulation of the Inflammatory Response: Sympathoadrenal Dependence in the Female Rat
J. Neurosci.,
May 15, 1999;
19(10):
4082 - 4089.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. A. Singer, X. A. Figueroa-Masot, R. H. Batchelor, and D. M. Dorsa
The Mitogen-Activated Protein Kinase Pathway Mediates Estrogen Neuroprotection after Glutamate Toxicity in Primary Cortical Neurons
J. Neurosci.,
April 1, 1999;
19(7):
2455 - 2463.
[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]
|
|
|
|
|
|
|
Q. Gu, K. S. Korach, and R. L. Moss
Rapid Action of 17{beta}-Estradiol on Kainate-Induced Currents in Hippocampal Neurons Lacking Intracellular Estrogen Receptors
Endocrinology,
February 1, 1999;
140(2):
660 - 666.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
A. E. Herbison
Multimodal Influence of Estrogen upon Gonadotropin-Releasing Hormone Neurons
Endocr. Rev.,
June 1, 1998;
19(3):
302 - 330.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
K. Obrietan and A. N. van den Pol
GABA Activity Mediating Cytosolic Ca2+ Rises in Developing Neurons Is Modulated by cAMP-Dependent Signal Transduction
J. Neurosci.,
June 15, 1997;
17(12):
4785 - 4799.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. H. Lagrange, O. K. Rønnekleiv, and M. J. Kelly
Modulation of G Protein-Coupled Receptors by an Estrogen Receptor that Activates Protein Kinase A
Mol. Pharmacol.,
April 1, 1997;
51(4):
605 - 612.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
H. C. Christian and J. F. Morris
Rapid actions of 17beta-oestradiol on a subset of lactotrophs in the rat pituitary
J. Physiol.,
March 1, 2002;
539(2):
557 - 566.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
