Structure and dynamics of the M3 muscarinic acetylcholine receptor

Nature. 2012 Feb 22;482(7386):552-6. doi: 10.1038/nature10867.

Abstract

Acetylcholine, the first neurotransmitter to be identified, exerts many of its physiological actions via activation of a family of G-protein-coupled receptors (GPCRs) known as muscarinic acetylcholine receptors (mAChRs). Although the five mAChR subtypes (M1-M5) share a high degree of sequence homology, they show pronounced differences in G-protein coupling preference and the physiological responses they mediate. Unfortunately, despite decades of effort, no therapeutic agents endowed with clear mAChR subtype selectivity have been developed to exploit these differences. We describe here the structure of the G(q/11)-coupled M3 mAChR ('M3 receptor', from rat) bound to the bronchodilator drug tiotropium and identify the binding mode for this clinically important drug. This structure, together with that of the G(i/o)-coupled M2 receptor, offers possibilities for the design of mAChR subtype-selective ligands. Importantly, the M3 receptor structure allows a structural comparison between two members of a mammalian GPCR subfamily displaying different G-protein coupling selectivities. Furthermore, molecular dynamics simulations suggest that tiotropium binds transiently to an allosteric site en route to the binding pocket of both receptors. These simulations offer a structural view of an allosteric binding mode for an orthosteric GPCR ligand and provide additional opportunities for the design of ligands with different affinities or binding kinetics for different mAChR subtypes. Our findings not only offer insights into the structure and function of one of the most important GPCR families, but may also facilitate the design of improved therapeutics targeting these critical receptors.

Publication types

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

MeSH terms

  • Acetylcholine / chemistry
  • Acetylcholine / metabolism
  • Allosteric Site
  • Animals
  • COS Cells
  • Crystallization
  • Crystallography, X-Ray
  • Kinetics
  • Ligands
  • Models, Molecular
  • Molecular Dynamics Simulation
  • Radioligand Assay
  • Rats
  • Receptor, Muscarinic M3 / chemistry*
  • Receptor, Muscarinic M3 / metabolism*
  • Scopolamine Derivatives / chemistry
  • Scopolamine Derivatives / metabolism
  • Substrate Specificity
  • Tiotropium Bromide

Substances

  • Ligands
  • Receptor, Muscarinic M3
  • Scopolamine Derivatives
  • Acetylcholine
  • Tiotropium Bromide

Associated data

  • PDB/4DAJ