Suppression of network activity in dorsal horn by gabapentin permeation of TRPV1 channels: implications for drug access to cytoplasmic targets

Neurosci Lett. 2015 Jan 1:584:397-402. doi: 10.1016/j.neulet.2014.07.033. Epub 2014 Jul 29.

Abstract

The effectiveness of gabapentin (GBP) in the treatment of neuropathic pain depends on access to the α2δ-1 accessory subunit of voltage-gated Ca(2+) channels. Access may be limited by its rate of entry via the neuronal system L-neutral amino acid transporter. The open pore of capsaicin-activated TRPV1 channel admits organic molecules such as local anesthetics and we calculated that GBP entry via this route would be 500× more rapid than via the transporter. Capsaicin should therefore increase GBP effectiveness. We used a quaternary GBP derivative (Q-GBP) as sole charge carrier in whole-cell recording experiments on rat dorsal root ganglion (DRG) neurons. Under these conditions, capsaicin produced a capsazepine-sensitive inward current thereby confirming Q-GBP permeation of TRPV1 channels. We have previously established that 5-6 days exposure to 100 μM GBP decreases excitability of dorsal horn neurons whereas 10 μM is ineffective. Excitability was monitored using confocal Ca(2+) imaging of rat spinal cord slices in organotypic culture. GBP effectiveness was augmented by transient exposures of cultures to capsaicin and robust suppression of excitability was seen with 10 μM GBP. Experiments with an inhibitor of the neutral amino acid transporter, 2-aminobicyclo-(2,2,1)-heptane-2-carboxylic acid (BCH 300 μM), showed the actions of GBP seen in the presence of capsaicin were independent of its entry by this route. Capsaicin potentiation of GBP depression of dorsal horn activity may therefore reflect drug permeation of TRPV1 channels. Agonist activation of TRP channels may provide a means for improving drug access to cytoplasmic targets in selective neuronal populations defined on the basis of type of TRP channel expressed.

Keywords: Allodynia; Alpha-2-delta; Capsaicin; Electrophysiology; Gabapentin; Neuropathic pain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amines / pharmacology*
  • Analgesics / pharmacology*
  • Animals
  • Calcium / metabolism
  • Capsaicin / pharmacology
  • Cells, Cultured
  • Cyclohexanecarboxylic Acids / pharmacology*
  • Drug Synergism
  • Gabapentin
  • Ganglia, Spinal / metabolism
  • Male
  • Neurons / drug effects
  • Neurons / metabolism
  • Patch-Clamp Techniques
  • Permeability
  • Rats, Sprague-Dawley
  • Spinal Cord Dorsal Horn / drug effects*
  • Spinal Cord Dorsal Horn / metabolism
  • TRPV Cation Channels / metabolism*
  • gamma-Aminobutyric Acid / pharmacology*

Substances

  • Amines
  • Analgesics
  • Cyclohexanecarboxylic Acids
  • TRPV Cation Channels
  • Trpv1 protein, rat
  • gamma-Aminobutyric Acid
  • Gabapentin
  • Capsaicin
  • Calcium