Receptor heteromerization expands the repertoire of cannabinoid signaling in rodent neurons

PLoS One. 2012;7(1):e29239. doi: 10.1371/journal.pone.0029239. Epub 2012 Jan 3.

Abstract

A fundamental question in G protein coupled receptor biology is how a single ligand acting at a specific receptor is able to induce a range of signaling that results in a variety of physiological responses. We focused on Type 1 cannabinoid receptor (CB₁R) as a model GPCR involved in a variety of processes spanning from analgesia and euphoria to neuronal development, survival and differentiation. We examined receptor dimerization as a possible mechanism underlying expanded signaling responses by a single ligand and focused on interactions between CB₁R and delta opioid receptor (DOR). Using co-immunoprecipitation assays as well as analysis of changes in receptor subcellular localization upon co-expression, we show that CB₁R and DOR form receptor heteromers. We find that heteromerization affects receptor signaling since the potency of the CB₁R ligand to stimulate G-protein activity is increased in the absence of DOR, suggesting that the decrease in CB₁R activity in the presence of DOR could, at least in part, be due to heteromerization. We also find that the decrease in activity is associated with enhanced PLC-dependent recruitment of arrestin3 to the CB₁R-DOR complex, suggesting that interaction with DOR enhances arrestin-mediated CB₁R desensitization. Additionally, presence of DOR facilitates signaling via a new CB₁R-mediated anti-apoptotic pathway leading to enhanced neuronal survival. Taken together, these results support a role for CB₁R-DOR heteromerization in diversification of endocannabinoid signaling and highlight the importance of heteromer-directed signal trafficking in enhancing the repertoire of GPCR signaling.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Arrestins / metabolism
  • Cannabinoids / metabolism*
  • Cell Line
  • Cell Proliferation
  • Cell Survival
  • Cerebral Cortex / cytology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Gene Expression Regulation
  • Humans
  • Male
  • Mice
  • Neurons / cytology*
  • Neurons / metabolism
  • Protein Multimerization*
  • Protein Structure, Quaternary
  • Protein Transport
  • Receptor, Cannabinoid, CB1 / chemistry*
  • Receptor, Cannabinoid, CB1 / metabolism*
  • Receptors, Opioid, delta / chemistry*
  • Receptors, Opioid, delta / metabolism*
  • Signal Transduction

Substances

  • Arrestins
  • Cannabinoids
  • Receptor, Cannabinoid, CB1
  • Receptors, Opioid, delta
  • arrestin3
  • Extracellular Signal-Regulated MAP Kinases