Home LiteratureArticle Details
PMID: 9503335 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Novel mechanism for non-genomic action of 17 beta-oestradiol on kainate-induced currents in isolated rat CA1 hippocampal neurones.

The Journal of physiology ·Vol. 506 ( Pt 3) ·1998-02-01 ·Pages 745-54

Gu Q, Moss RL

Abstract

1. Using whole-cell voltage-clamp recordings of dissociated hippocampal CA1 neurones, we demonstrated that 17 beta-oestradiol rapidly potentiates kainate-induced currents when applied either to the outside or the inside of the neurone. However, when the steroid was conjugated to bovine serum albumin (E2-BSA), application to either the extracellular plasma membrane (E2-BSAout) or the cytosolic side of the cell (E2-BSAin) had no observable effect on kainate-induced currents. However, when applied stimultaneously to both sides of the plasma membrane, E2-BSA potentiated kainate-induced currents. 2. Application of E2-BSAout and GTP gamma S(in) potentiated kainate-induced currents. The potentiation of kainate-induced currents by 17 beta-oestradiol was occluded by cholera toxin pretreatment and appeared to be pertussis toxin insensitive. 3. E2-BSAin prolonged the effect of 8-bromoadenosine 3',5' cyclic monophosphate (8-bromo-cAMP) on kainate-induced currents. The recovery from the 8-bromo-cAMP response was found to be a function of the concentration of E2-BSAin. The application of ATP gamma S(in) occluded the effect of 17 beta-oestradiol. 4. These results suggest that the non-genomic action of 17 beta-oestradiol in the potentiation of kainate-induced currents is mediated via an action on Gs protein-coupled receptors. This operates in concert with an internal action of 17 beta-oestradiol on a cAMP-dependent phosphorylation.

MeSH Terms
Animals Cyclic AMP/physiology Electric Stimulation Electrophysiology Estradiol/pharmacology Excitatory Amino Acid Agonists/pharmacology Female GTP-Binding Proteins/metabolism Hippocampus/drug effects,metabolism In Vitro Techniques Ion Channels/drug effects,metabolism Kainic Acid/pharmacology Male Membrane Potentials/physiology Neurons/drug effects,metabolism Neurotoxins/pharmacology Patch-Clamp Techniques Rats Rats, Sprague-Dawley Serum Albumin, Bovine
Chemicals
Excitatory Amino Acid Agonists Ion Channels Neurotoxins Serum Albumin, Bovine Estradiol Cyclic AMP GTP-Binding Proteins Kainic Acid
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gu Q
Department of Physiology, University of Texas Southwestern Medical Center at Dallas 75235, USA.
Moss R L
References (43)
43 references, click to expand
  1. Nongenomic effects of 17 beta-estradiol on maturing human oocytes: relationship to oocyte developmental potential.
    J Clin Endocrinol Metab. 1995 Apr;80(4):1438-43 PMID: 7714121
  2. Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor.
    J Neurosci. 1996 Jan 15;16(2):595-604 PMID: 8551343
  3. Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain.
    Endocrinology. 1996 May;137(5):2163-6 PMID: 8612562
  4. 17 beta-Estradiol potentiates kainate-induced currents via activation of the cAMP cascade.
    J Neurosci. 1996 Jun 1;16(11):3620-9 PMID: 8642406
  5. Membrane receptors for estrogen, progesterone, and testosterone in the rat brain: fantasy or reality.
    Cell Mol Neurobiol. 1996 Apr;16(2):175-98 PMID: 8743968
  6. Steroids conjugated to bovine serum albumin as tools to demonstrate specific steroid neuronal membrane binding sites.
    J Psychiatry Neurosci. 1996 May;21(3):187-97 PMID: 8935331
  7. Nongenomic actions of estrogen in the brain: physiological significance and cellular mechanisms.
    Crit Rev Neurobiol. 1996;10(2):189-203 PMID: 8971129
  8. Estrogen: nontranscriptional signaling pathway.
    Recent Prog Horm Res. 1997;52:33-68; discussion 68-9 PMID: 9238847
  9. Separation and characterization of two phosphorylase phosphatase inhibitors from rabbit skeletal muscle.
    Eur J Biochem. 1976 Nov 15;70(2):419-26 PMID: 188646
  10. The hormonal control of glycogen metabolism. Phosphorylation of protein phosphatase inhibitor-1 in vivo in response to adrenaline.
    Eur J Biochem. 1979 Jun;97(1):251-6 PMID: 225171
  11. Effect of epinephrine and insulin on the phosphorylation of phosphorylase phosphatase inhibitor 1 in perfused rat skeletal muscle.
    FEBS Lett. 1980 Jun 2;114(2):253-6 PMID: 6993229
  12. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  13. Antagonistic effects of insulin and beta-adrenergic agonists on the activity of protein phosphatase inhibitor-1 in skeletal muscle of the perfused rat hemicorpus.
    J Biol Chem. 1982 Nov 10;257(21):12493-6 PMID: 6290470
  14. Isolation of neurons suitable for patch-clamping from adult mammalian central nervous systems.
    J Neurosci Methods. 1986 May;16(3):227-38 PMID: 3523050
  15. Mechanism of the rapid effect of 17 beta-estradiol on medial amygdala neurons.
    Science. 1986 Jul 11;233(4760):226-8 PMID: 3726531
  16. Partial structure and hormonal regulation of rabbit liver inhibitor-1; distribution of inhibitor-1 and inhibitor-2 in rabbit and rat tissues.
    Biochim Biophys Acta. 1989 Feb 9;1010(2):218-26 PMID: 2912504
  17. Progesterone effects upon dopamine release from the corpus striatum of female rats. II. Evidence for a membrane site of action and the role of albumin.
    Brain Res. 1989 Jan 9;476(2):338-44 PMID: 2539225
  18. Excitatory amino acid receptors in the vertebrate central nervous system.
    Pharmacol Rev. 1989 Jun;41(2):143-210 PMID: 2558391
  19. Dopamine modulates the kinetics of ion channels gated by excitatory amino acids in retinal horizontal cells.
    Proc Natl Acad Sci U S A. 1990 Jan;87(2):767-71 PMID: 1689053
  20. Direct effect of 17 beta-estradiol on striatum: sex differences in dopamine release.
    Synapse. 1990;5(2):157-64 PMID: 2309159
  21. Excitatory amino acid neurotoxicity and neurodegenerative disease.
    Trends Pharmacol Sci. 1990 Sep;11(9):379-87 PMID: 2238094
  22. Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis.
    Neurosci Lett. 1990 Oct 16;118(2):169-71 PMID: 2125712
  23. Electrophysiological evidence for a rapid membrane action of the gonadal steroid, 17 beta-estradiol, on CA1 pyramidal neurons of the rat hippocampus.
    Brain Res. 1991 Mar 8;543(1):148-52 PMID: 2054668
  24. Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases.
    Science. 1991 Sep 6;253(5024):1132-5 PMID: 1653455
  25. Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons.
    Science. 1991 Sep 6;253(5024):1135-8 PMID: 1716001
  26. Evidence for isoproterenol-induced phosphorylation of phosphatase inhibitor-1 in the intact heart.
    Circ Res. 1991 Dec;69(6):1450-7 PMID: 1659500
  27. Receptor tyrosine kinases.
    FASEB J. 1992 Mar;6(6):2332-7 PMID: 1312047
  28. Phosphorylation of DARPP-32 and protein phosphatase inhibitor-1 in rat choroid plexus: regulation by factors other than dopamine.
    J Neurosci. 1992 Aug;12(8):3071-83 PMID: 1494946
  29. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons.
    J Neurosci. 1992 Aug;12(8):3217-25 PMID: 1353794
  30. Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase.
    Nature. 1993 Feb 18;361(6413):637-41 PMID: 8094892
  31. Phosphorylation of amino acid neurotransmitter receptors in synaptic plasticity.
    Trends Neurosci. 1993 Apr;16(4):147-53 PMID: 7682348
  32. Sex differences in striatal dopamine: in vivo microdialysis and behavioral studies.
    Brain Res. 1993 Apr 30;610(1):127-34 PMID: 8518920
  33. Cell signaling and estrogens in female rat osteoblasts: a possible involvement of unconventional nonnuclear receptors.
    J Bone Miner Res. 1993 Nov;8(11):1365-76 PMID: 8266828
  34. Estrogen regulation of dopamine release in the nucleus accumbens: genomic- and nongenomic-mediated effects.
    J Neurochem. 1994 May;62(5):1750-6 PMID: 8158125
  35. Neurosteroids modulate calcium currents in hippocampal CA1 neurons via a pertussis toxin-sensitive G-protein-coupled mechanism.
    J Neurosci. 1994 Apr;14(4):1963-77 PMID: 8158251
  36. Regulation of NMDA receptors in cultured hippocampal neurons by protein phosphatases 1 and 2A.
    Nature. 1994 May 19;369(6477):230-2 PMID: 8183343
  37. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression.
    Nature. 1994 Jun 9;369(6480):486-8 PMID: 7515479
  38. Patch-clamp analysis of direct steroidal modulation of glutamate receptor-channels.
    J Neuroendocrinol. 1994 Jun;6(3):347-55 PMID: 7522740
  39. The potency of mu-opioid hyperpolarization of hypothalamic arcuate neurons is rapidly attenuated by 17 beta-estradiol.
    J Neurosci. 1994 Oct;14(10):6196-204 PMID: 7931572
  40. Cortisol inhibition of calcium currents in guinea pig hippocampal CA1 neurons via G-protein-coupled activation of protein kinase C.
    J Neurosci. 1995 Jan;15(1 Pt 2):903-11 PMID: 7823188
  41. Glutamate receptor modulation by protein phosphorylation.
    J Physiol Paris. 1994;88(3):181-92 PMID: 7530547
  42. Estradiol binding to synaptosomal plasma membranes of rat brain regions.
    Experientia. 1995 Jan 15;51(1):11-5 PMID: 7843323
  43. Membrane estrogen receptors identified by multiple antibody labeling and impeded-ligand binding.
    FASEB J. 1995 Mar;9(5):404-10 PMID: 7896011
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
1998-02-01
Pages
745-54
Language
English
Region
England
NLM ID
0266262
PMCID
PMC2230751
Subset
IM
Grants
NIMH NIH HHS · R01-MH47418 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com