Delineating the conformational landscape of the adenosine A2A receptor during G protein coupling

Cell. 2021 Apr 1;184(7):1884-1894.e14. doi: 10.1016/j.cell.2021.02.041. Epub 2021 Mar 19.

Abstract

G-protein-coupled receptors (GPCRs) represent a ubiquitous membrane protein family and are important drug targets. Their diverse signaling pathways are driven by complex pharmacology arising from a conformational ensemble rarely captured by structural methods. Here, fluorine nuclear magnetic resonance spectroscopy (19F NMR) is used to delineate key functional states of the adenosine A2A receptor (A2AR) complexed with heterotrimeric G protein (Gαsβ1γ2) in a phospholipid membrane milieu. Analysis of A2AR spectra as a function of ligand, G protein, and nucleotide identifies an ensemble represented by inactive states, a G-protein-bound activation intermediate, and distinct nucleotide-free states associated with either partial- or full-agonist-driven activation. The Gβγ subunit is found to be critical in facilitating ligand-dependent allosteric transmission, as shown by 19F NMR, biochemical, and computational studies. The results provide a mechanistic basis for understanding basal signaling, efficacy, precoupling, and allostery in GPCRs.

Keywords: (19)F NMR; G protein; GPCR; adenosine A(2A) receptor; allostery; partial agonism; precoupling; rigidity transmission allostery.

Publication types

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

MeSH terms

  • Allosteric Regulation
  • Binding Sites
  • Heterotrimeric GTP-Binding Proteins / chemistry*
  • Heterotrimeric GTP-Binding Proteins / genetics
  • Heterotrimeric GTP-Binding Proteins / metabolism
  • Humans
  • Kinetics
  • Ligands
  • Lipid Bilayers / chemistry
  • Lipid Bilayers / metabolism
  • Magnetic Resonance Spectroscopy
  • Molecular Dynamics Simulation
  • Nanostructures / chemistry
  • Protein Binding
  • Protein Conformation
  • Protein Subunits / chemistry
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Receptor, Adenosine A2A / chemistry*
  • Receptor, Adenosine A2A / genetics
  • Receptor, Adenosine A2A / metabolism
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / isolation & purification
  • Signal Transduction

Substances

  • Ligands
  • Lipid Bilayers
  • Protein Subunits
  • Receptor, Adenosine A2A
  • Recombinant Proteins
  • Heterotrimeric GTP-Binding Proteins