RGS4 regulates partial agonism of the M2 muscarinic receptor-activated K+ currents

J Physiol. 2014 Mar 15;592(6):1237-48. doi: 10.1113/jphysiol.2013.269803. Epub 2014 Jan 13.

Abstract

Partial agonists are used clinically to avoid overstimulation of receptor-mediated signalling, as they produce a submaximal response even at 100% receptor occupancy. The submaximal efficacy of partial agonists is due to conformational change of the agonist-receptor complex, which reduces effector activation. In addition to signalling activators, several regulators help control intracellular signal transductions. However, it remains unclear whether these signalling regulators contribute to partial agonism. Here we show that regulator of G-protein signalling (RGS) 4 is a determinant for partial agonism of the M2 muscarinic receptor (M2R). In rat atrial myocytes, pilocarpine evoked smaller G-protein-gated K(+) inwardly rectifying (KG) currents than those evoked by ACh. In a Xenopus oocyte expression system, pilocarpine acted as a partial agonist in the presence of RGS4 as it did in atrial myocytes, while it acted like a full agonist in the absence of RGS4. Functional couplings within the agonist-receptor complex/G-protein/RGS4 system controlled the efficacy of pilocarpine relative to ACh. The pilocarpine-M2R complex suppressed G-protein-mediated activation of KG currents via RGS4. Our results demonstrate that partial agonism of M2R is regulated by the RGS4-mediated inhibition of G-protein signalling. This finding helps us to understand the molecular components and mechanism underlying the partial agonism of M2R-mediated physiological responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / pharmacology
  • Animals
  • Cell Membrane / metabolism
  • Dopamine / pharmacology
  • Female
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / genetics
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / metabolism
  • Male
  • Membrane Potentials
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism
  • Oocytes / drug effects
  • Oocytes / metabolism
  • Patch-Clamp Techniques
  • Pilocarpine / pharmacology
  • Potassium / metabolism*
  • Protein Interaction Domains and Motifs
  • RGS Proteins / chemistry
  • RGS Proteins / genetics
  • RGS Proteins / metabolism*
  • Rats
  • Rats, Wistar
  • Receptor, Muscarinic M2 / agonists*
  • Receptor, Muscarinic M2 / genetics
  • Receptor, Muscarinic M2 / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Signal Transduction
  • Xenopus laevis

Substances

  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • RGS Proteins
  • Receptor, Muscarinic M2
  • Recombinant Proteins
  • Pilocarpine
  • RGS4 protein
  • Acetylcholine
  • Potassium
  • Dopamine