Activation of µ-opioid receptors and block of Kir3 potassium channels and NMDA receptor conductance by L- and D-methadone in rat locus coeruleus

Br J Pharmacol. 2010 Nov;161(6):1403-13. doi: 10.1111/j.1476-5381.2010.00967.x.

Abstract

Background and purpose: Methadone activates opioid receptors to increase a potassium conductance mediated by G-protein-coupled, inwardly rectifying, potassium (K(IR) 3) channels. Methadone also blocks K(IR) 3 channels and N-methyl-D-aspartic acid (NMDA) receptors. However, the concentration dependence and stereospecificity of receptor activation and channel blockade by methadone on single neurons has not been characterized.

Experimental approach: Intracellular and whole-cell recording were made from locus coeruleus neurons in brain slices and the activation of µ-opioid receptors and blockade of K(IR) 3 and NMDA channels with L- and D-methadone was examined.

Key results: The potency of L-methadone, measured by the amplitude of hyperpolarization was 16.5-fold higher than with D-methadone. A maximum hyperpolarization was caused by both enantiomers (∼30 mV); however, the maximum outward current measured with whole-cell voltage-clamp recording was smaller than the current induced by [Met](5) enkephalin. The K(IR) 3 conductance induced by activation of α(2) -adrenoceptors was decreased with high concentrations of L- and D-methadone (10-30 µM). In addition, methadone blocked the resting inward rectifying conductance (K(IR) ). Both L- and D-methadone blocked the NMDA receptor-dependent current. The block of NMDA receptor-dependent current was voltage-dependent suggesting that methadone acted as a channel blocker.

Conclusions and implications: Methadone activated µ-opioid receptors at low concentrations in a stereospecific manner. K(IR) 3 and NMDA receptor channel block was not stereospecific and required substantially higher concentrations. The separation in the concentration range suggests that the activation of µ-opioid receptors rather than the channel blocking properties mediate both the therapeutic and toxic actions of methadone.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / antagonists & inhibitors*
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / physiology
  • Locus Coeruleus / drug effects*
  • Locus Coeruleus / metabolism
  • Male
  • Methadone / chemistry
  • Methadone / metabolism
  • Methadone / pharmacology*
  • Potassium Channel Blockers / chemistry
  • Potassium Channel Blockers / metabolism
  • Potassium Channel Blockers / pharmacology*
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors*
  • Receptors, N-Methyl-D-Aspartate / physiology
  • Receptors, Opioid, mu / metabolism*
  • Stereoisomerism

Substances

  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • Potassium Channel Blockers
  • Receptors, N-Methyl-D-Aspartate
  • Receptors, Opioid, mu
  • Methadone