μ-Opioid receptor desensitization: homologous or heterologous?

Eur J Neurosci. 2012 Dec;36(12):3636-42. doi: 10.1111/ejn.12003. Epub 2012 Sep 24.

Abstract

There is considerable controversy over whether μ-opioid receptor (MOPr) desensitization is homologous or heterologous and over the mechanisms underlying such desensitization. In different cell types MOPr desensitization has been reported to involve receptor phosphorylation by various kinases, including G-protein-coupled receptor kinases (GRKs), second messenger and other kinases as well as perturbation of the MOPr effector pathway by GRK sequestration of G protein βγ subunits or ion channel modulation. Here we report that in brainstem locus coeruleus (LC) neurons prepared from relatively mature rats (5-8 weeks old) rapid MOPr desensitization induced by the high-efficacy opioid peptides methionine enkephalin and DAMGO was homologous and not heterologous to α(2)-adrenoceptors and somatostatin SST(2) receptors. Given that these receptors all couple through G proteins to the same set of G-protein inwardly rectifying (GIRK) channels it is unlikely therefore that in mature neurons MOPr desensitization involves G protein βγ subunit sequestration or ion channel modulation. In contrast, in slices from immature animals (less than postnatal day 20), MOPr desensitization was observed to be heterologous and could be downstream of the receptor. Heterologous MOPr desensitization was not dependent on protein kinase C or c-Jun N-terminal kinase activity, but the change from heterologous to homologous desensitization with age was correlated with a decrease in the expression levels of GRK2 in the LC and other brain regions. The observation that the mechanisms underlying MOPr desensitization change with neuronal development is important when extrapolating to the mature brain results obtained from experiments on expression systems, cell lines and immature neuronal preparations.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials*
  • Animals
  • Enkephalin, Ala(2)-MePhe(4)-Gly(5)- / pharmacology
  • Enkephalin, Methionine / pharmacology
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / metabolism
  • G-Protein-Coupled Receptor Kinase 2 / genetics
  • G-Protein-Coupled Receptor Kinase 2 / metabolism
  • GTP-Binding Proteins / metabolism
  • Gene Expression
  • Locus Coeruleus / growth & development
  • Locus Coeruleus / physiology
  • Male
  • Mitogen-Activated Protein Kinase 8 / metabolism
  • Neurons / metabolism
  • Neurons / physiology
  • Neurotransmitter Agents / pharmacology
  • Protein Kinase C / metabolism
  • Protein Subunits / metabolism
  • Rats
  • Rats, Wistar
  • Receptors, Adrenergic, alpha-2 / metabolism
  • Receptors, Opioid, mu / metabolism*
  • Receptors, Somatostatin / metabolism

Substances

  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • Neurotransmitter Agents
  • Protein Subunits
  • Receptors, Adrenergic, alpha-2
  • Receptors, Opioid, mu
  • Receptors, Somatostatin
  • Enkephalin, Ala(2)-MePhe(4)-Gly(5)-
  • Enkephalin, Methionine
  • Protein Kinase C
  • Grk2 protein, rat
  • G-Protein-Coupled Receptor Kinase 2
  • Mitogen-Activated Protein Kinase 8
  • GTP-Binding Proteins