Calcium influx through presynaptic 5-HT3 receptors facilitates GABA release in the hippocampus: in vitro slice and synaptosome studies

Neuroscience. 2004;129(3):703-18. doi: 10.1016/j.neuroscience.2004.08.020.

Abstract

Serotonin 5-hydroxytryptamine type 3 receptors (5HT3R) are Ca2+-permeant, non-selective cation channels that have been localized to presynaptic terminals and demonstrated to modulate neurotransmitter release. In the present study the effect of 5-HT on GABA release in the hippocampus was characterized using both electrophysiological and biochemical techniques. 5-HT elicited a burst-like, 6- to 10-fold increase in the frequency of GABAA receptor-mediated inhibitory postsynaptic currents (IPSCs) measured with whole-cell voltage-clamp recordings of CA1 neurons in hippocampal slices. When tetrodotoxin was used to block action potential propagation, the 5-HT-induced burst of IPSCs was still observed. Stimulation of hippocampal synaptosomes with 5-HT resulted in a significant increase in the amount of [3H]GABA released by hyperosmotic saline. In both preparations, the 5-HT effect was shown to be mediated by 5HT3Rs, as it was mimicked by the selective 5HT3R agonist m-chlorophenyl biguanide and blocked by the selective 5HT3R antagonist 3-tropanylindole-3-carboxylate hydrochloride. The 5HT3R-mediated increase in GABA release was blocked by 100 microM cadmium or by omitting Ca2+ in external solutions, indicating the Ca2+-dependence of the effect. The high voltage-activated Ca2+ channel blockers omega-conotoxin GVIA and omega-conotoxin MVIIC and 10 microM cadmium had no significant effect on the 5-HT3R-mediated enhancement of GABA release, indicating that Ca2+ influx through the 5-HT3R facilitates GABA release. Taken together, these data provide direct evidence that Ca2+ entry via presynaptic 5HT3Rs facilitates the release of GABA from hippocampal interneurons.

Publication types

  • Comparative Study
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Animals, Newborn
  • Bicuculline / analogs & derivatives*
  • Bicuculline / pharmacology
  • Biguanides / pharmacology
  • Cadmium / pharmacology
  • Calcium / metabolism*
  • Calcium / pharmacology
  • Calcium Channel Blockers / pharmacology
  • Dose-Response Relationship, Drug
  • Drug Interactions
  • Electric Stimulation / methods
  • GABA Antagonists / pharmacology
  • Hippocampus / cytology
  • Hippocampus / drug effects
  • Hippocampus / metabolism*
  • In Vitro Techniques
  • Indoles / pharmacology
  • Membrane Potentials
  • Neural Inhibition / drug effects
  • Neural Inhibition / radiation effects
  • Neurons / drug effects
  • Neurons / physiology
  • Patch-Clamp Techniques / methods
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Presynaptic / drug effects
  • Receptors, Presynaptic / metabolism*
  • Receptors, Serotonin, 5-HT3 / metabolism*
  • Serotonin / pharmacology
  • Serotonin 5-HT3 Receptor Antagonists
  • Serotonin Receptor Agonists / pharmacology
  • Sucrose / pharmacology
  • Synaptosomes / drug effects
  • Synaptosomes / metabolism*
  • Synaptosomes / radiation effects
  • Tritium / metabolism
  • Tropisetron
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Biguanides
  • Calcium Channel Blockers
  • GABA Antagonists
  • Indoles
  • Receptors, Presynaptic
  • Receptors, Serotonin, 5-HT3
  • Serotonin 5-HT3 Receptor Antagonists
  • Serotonin Receptor Agonists
  • Cadmium
  • Tritium
  • Serotonin
  • bicuculline methiodide
  • gamma-Aminobutyric Acid
  • Sucrose
  • Tropisetron
  • 1-(3-chlorophenyl)biguanide
  • Calcium
  • Bicuculline