5-hydroxytryptamine-mediated neurotransmission modulates spontaneous and vagal-evoked glutamate release in the nucleus of the solitary tract effect of uptake blockade

J Pharmacol Exp Ther. 2014 May;349(2):288-96. doi: 10.1124/jpet.113.211334. Epub 2014 Mar 11.

Abstract

The effect of blockade of either 5-hydroxytryptamine (5-HT)/serotonin transporter (SERT) with citalopram or the organic cation transporter 3 (OCT3)/plasma membrane monoamine transporter (PMAT) with decynium-22 (D-22) on spontaneous and evoked release of 5-HT in the nucleus tractus solitarius (NTS) was investigated in rat brainstem slices treated with gabazine. 5-HT release was measured indirectly by changes in the frequency and amplitude of glutamatergic miniature excitatory postsynaptic currents (mEPSCs) [in the presence of tetrodotoxin (TTX)] and evoked EPSCs. Blockade of 5-HT3 receptors with granisetron reduced, whereas the 5-HT3 agonist phenylbiguanide increased, the frequency of mEPSCs. 5-HT decreased mEPSC frequency at low concentrations and increased frequency at high concentrations. This inhibition was blocked by the 5-HT1A antagonist N-[2-[4-(2-methoxyphenyl)-1-piperazinyl]ethyl]-N-2-pyridinylcyclohexanecarboxamide (WAY-100635), which was ineffective on its own, whereas the excitation was reversed by granisetron. The addition of citalopram or D-22 caused inhibition, which was prevented by 5-HT1A blockade. Thus, in the NTS, the spontaneous release of 5-HT is able to activate 5-HT3 receptors, but not 5-HT1A receptors, as the release in their vicinity is removed by uptake. The ineffectiveness of corticosterone suggests that the low-affinity, high-capacity transporter is PMAT, not OCT3. For evoked 5-HT release, only D-22 caused an increase in the amplitude of EPSCs, with a decrease in the paired pulse ratio, and increased the number of spontaneous EPSCs after 20-Hz stimulation. Thus, for the evoked release of 5-HT, the low-affinity, high-capacity transporter PMAT, but not 5-HT transporter (5-HTT)/SERT, is important in the regulation of changes in 5-HT extracellular concentration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Citalopram / pharmacology
  • Excitatory Postsynaptic Potentials
  • Glutamic Acid / metabolism*
  • In Vitro Techniques
  • Male
  • Miniature Postsynaptic Potentials
  • Neurons / physiology
  • Organic Anion Transporters, Sodium-Independent / antagonists & inhibitors
  • Plasma Membrane Neurotransmitter Transport Proteins / antagonists & inhibitors
  • Pyridazines / pharmacology
  • Quinolines / pharmacology
  • Rats, Sprague-Dawley
  • Selective Serotonin Reuptake Inhibitors / pharmacology
  • Serotonin / metabolism*
  • Serotonin 5-HT1 Receptor Antagonists / pharmacology
  • Serotonin Plasma Membrane Transport Proteins / metabolism*
  • Solitary Nucleus / drug effects
  • Solitary Nucleus / metabolism*
  • Synaptic Transmission
  • Vagus Nerve / physiology*

Substances

  • Organic Anion Transporters, Sodium-Independent
  • Plasma Membrane Neurotransmitter Transport Proteins
  • Pyridazines
  • Quinolines
  • Serotonin 5-HT1 Receptor Antagonists
  • Serotonin Plasma Membrane Transport Proteins
  • Serotonin Uptake Inhibitors
  • organic anion transport protein 3
  • Citalopram
  • pseudoisocyanine
  • Serotonin
  • Glutamic Acid
  • gabazine