G protein-coupled receptor kinase 2 mediates mu-opioid receptor desensitization in GABAergic neurons of the nucleus raphe magnus

J Neurochem. 2001 Apr;77(2):435-44. doi: 10.1046/j.1471-4159.2001.00267.x.

Abstract

Nucleus raphe magnus (NRM) sends the projection to spinal dorsal horn and inhibits nociceptive transmission. Analgesic effect produced by mu-opioid receptor agonists including morphine partially results from activating the NRM-spinal cord pathway. It is generally believed that mu-opioid receptor agonists disinhibit spinally projecting neurons of the NRM and produce analgesia by hyperpolarizing GABAergic interneurons. In the present study, whole-cell patch-clamp recordings combined with single-cell RT-PCR analysis were used to test the hypothesis that DAMGO ([D-Ala(2),N-methyl-Phe(4),Gly-ol(5)]enkephalin), a specific mu-opioid receptor agonist, selectively hyperpolarizes NRM neurons expressing mRNA of glutamate decarboxylase (GAD(67)). Homologous desensitization of mu-opioid receptors in NRM neurons could result in the development of morphine-induced tolerance. G protein-coupled receptor kinase (GRK) is believed to mediate mu-opioid receptor desensitization in vivo. Therefore, we also investigated the involvement of GRK in mediating homologous desensitization of DAMAMGO-induced electrophysiological effects on NRM neurons by using two experimental strategies. First, single-cell RT-PCR assay was used to study the expression of GRK2 and GRK3 mRNAs in individual DAMGO-responsive NRM neurons. Whole-cell recording was also performed with an internal solution containing the synthetic peptide, which corresponds to G(betagamma)-binding domain of GRK and inhibits G(betagamma) activation of GRK. Our results suggest that DAMGO selectively hyperpolarizes NRM GABAergic neurons by opening inwardly rectifying K(+) channels and that GRK2 mediates short-term homologous desensitization of mu-opioid receptors in NRM GABAergic neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Analgesics, Opioid / pharmacology
  • Animals
  • Binding Sites
  • Cyclic AMP-Dependent Protein Kinases / biosynthesis
  • Cyclic AMP-Dependent Protein Kinases / genetics
  • Cyclic AMP-Dependent Protein Kinases / physiology*
  • Drug Tolerance / physiology
  • Enkephalin, Ala(2)-MePhe(4)-Gly(5)- / pharmacology
  • G-Protein-Coupled Receptor Kinase 2
  • G-Protein-Coupled Receptor Kinase 3
  • Glutamate Decarboxylase / biosynthesis
  • Ion Transport / drug effects
  • Membrane Potentials / drug effects
  • Molecular Sequence Data
  • Nerve Tissue Proteins / biosynthesis
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / physiology*
  • Neurons / drug effects
  • Neurons / physiology
  • Oligopeptides / chemical synthesis
  • Oligopeptides / pharmacology
  • Pain / physiopathology
  • Patch-Clamp Techniques
  • Phosphorylation
  • Potassium / metabolism
  • Potassium Channels / metabolism
  • Potassium Channels, Inwardly Rectifying*
  • Protein Processing, Post-Translational
  • Protein Serine-Threonine Kinases / biosynthesis
  • Protein Serine-Threonine Kinases / genetics
  • Protein Structure, Tertiary
  • Protein Transport / drug effects
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • Raphe Nuclei / drug effects
  • Raphe Nuclei / enzymology
  • Raphe Nuclei / physiology*
  • Raphe Nuclei / physiopathology
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Opioid, mu / agonists
  • Receptors, Opioid, mu / physiology*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / drug effects
  • Spinal Cord / physiopathology
  • beta-Adrenergic Receptor Kinases
  • gamma-Aminobutyric Acid / physiology*

Substances

  • Analgesics, Opioid
  • Nerve Tissue Proteins
  • Oligopeptides
  • Potassium Channels
  • Potassium Channels, Inwardly Rectifying
  • RNA, Messenger
  • Receptors, Opioid, mu
  • Enkephalin, Ala(2)-MePhe(4)-Gly(5)-
  • gamma-Aminobutyric Acid
  • Protein Serine-Threonine Kinases
  • Cyclic AMP-Dependent Protein Kinases
  • G-Protein-Coupled Receptor Kinase 3
  • Grk2 protein, rat
  • Grk3 protein, rat
  • beta-Adrenergic Receptor Kinases
  • G-Protein-Coupled Receptor Kinase 2
  • Glutamate Decarboxylase
  • Potassium