Spontaneous L-glutamate release enhancement in rat substantia gelatinosa neurons by (-)-carvone and (+)-carvone which activate different types of TRP channel

Biochem Biophys Res Commun. 2015 Apr 10;459(3):498-503. doi: 10.1016/j.bbrc.2015.02.135. Epub 2015 Mar 5.

Abstract

Transient receptor potential (TRP) channels in the spinal dorsal horn lamina II (substantia gelatinosa; SG), which are involved in the modulation of nociceptive transmission, have not yet been fully examined in property. Activation of the TRP channels by various plant-derived chemicals results in an increase in the spontaneous release of L-glutamate onto the SG neurons. We examined the effects of a monoterpene ketone (-)-carvone (contained in spearmint) and its stereoisomer (+)-carvone (in caraway) on glutamatergic spontaneous excitatory transmission in SG neurons of adult rat spinal cord slices by using the whole-cell patch-clamp technique. (-)-Carvone and (+)-carvone increased the frequency of spontaneous excitatory postsynaptic current (sEPSC) in a reversible and concentration-dependent manner with a small increase in its amplitude. Half-maximal effective concentrations of (-)-carvone and (+)-carvone in increasing sEPSC frequency were 0.70 mM and 0.72 mM, respectively. The (-)-carvone but not (+)-carvone activity was inhibited by a TRPV1 antagonist capsazepine. On the other hand, the (+)-carvone but not (-)-carvone activity was inhibited by a TRPA1 antagonist HC-030031. These results indicate that (-)-carvone and (+)-carvone activate TRPV1 and TRPA1 channels, respectively, resulting in an increase in spontaneous L-glutamate release onto SG neurons, with almost the same efficacy. Such a difference in TRP activation between the stereoisomers may serve to know the properties of TRP channels in the SG.

Keywords: (+)-Carvone; (−)-Carvone; Glutamate release; Spinal substantia gelatinosa; TRPA1; TRPV1.

MeSH terms

  • Acetanilides / pharmacology
  • Animals
  • Capsaicin / analogs & derivatives
  • Capsaicin / pharmacology
  • Cyclohexane Monoterpenes
  • Excitatory Postsynaptic Potentials / drug effects
  • Glutamic Acid / metabolism*
  • Male
  • Monoterpenes / chemistry
  • Monoterpenes / pharmacology*
  • Neurons / drug effects
  • Neurons / physiology
  • Patch-Clamp Techniques
  • Purines / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Stereoisomerism
  • Substantia Gelatinosa / cytology
  • Substantia Gelatinosa / drug effects*
  • Substantia Gelatinosa / physiology*
  • Synaptic Transmission / drug effects
  • TRPA1 Cation Channel
  • TRPC Cation Channels / agonists
  • TRPC Cation Channels / antagonists & inhibitors
  • TRPV Cation Channels / agonists
  • TRPV Cation Channels / antagonists & inhibitors
  • Transient Receptor Potential Channels / agonists*
  • Transient Receptor Potential Channels / antagonists & inhibitors

Substances

  • 2-(1,3-dimethyl-2,6-dioxo-1,2,3,6-tetrahydro-7H-purin-7-yl)-N-(4-isopropylphenyl)acetamide
  • Acetanilides
  • Cyclohexane Monoterpenes
  • Monoterpenes
  • Purines
  • TRPA1 Cation Channel
  • TRPC Cation Channels
  • TRPV Cation Channels
  • Transient Receptor Potential Channels
  • Trpa1 protein, rat
  • Trpv1 protein, rat
  • Glutamic Acid
  • carvone
  • capsazepine
  • Capsaicin