Interhelical interaction and receptor phosphorylation regulate the activation kinetics of different human β1-adrenoceptor variants

J Biol Chem. 2015 Jan 16;290(3):1760-9. doi: 10.1074/jbc.M114.607333. Epub 2014 Dec 1.

Abstract

G protein-coupled receptors represent the largest class of drug targets, but genetic variation within G protein-coupled receptors leads to variable drug responses and, thereby, compromises their therapeutic application. One of the most intensely studied examples is a hyperfunctional variant of the human β1-adrenoceptor that carries an arginine at position 389 in helix 8 (Arg-389-ADRB1). However, the mechanism underlying the higher efficacy of the Arg-389 variant remained unclear to date. Despite its hyperfunctionality, we found the Arg-389 variant of ADRB1 to be hyperphosphorylated upon continuous stimulation with norepinephrine compared with the Gly-389 variant. Using ADRB1 sensors to monitor activation kinetics by fluorescence resonance energy transfer, Arg-389-ADRB1 exerted faster activation speed and arrestin recruitment than the Gly-389 variant. Both activation speed and arrestin recruitment depended on phosphorylation of the receptor, as shown by knockdown of G protein-coupled receptor kinases and phosphorylation-deficient ADRB1 mutants. Structural modeling of the human β1-adrenoceptor suggested interaction of the side chain of Arg-389 with opposing amino acid residues in helix 1. Site-directed mutagenesis of Lys-85 and Thr-86 in helix 1 revealed that this interaction indeed determined ADRB1 activation kinetics. Taken together, these findings indicate that differences in interhelical interaction regulate the different activation speed and efficacy of ADRB1 variants.

Keywords: Adrenergic Receptor; Cardiovascular Disease; FRET; G Protein-coupled Receptor (GPCR); Genetic Variation; SNP.

MeSH terms

  • Arginine / chemistry
  • Arrestins / metabolism
  • Cardiovascular Diseases / metabolism
  • Crystallography, X-Ray
  • Cyclic AMP / metabolism
  • Fluorescence Resonance Energy Transfer
  • HEK293 Cells
  • Humans
  • Microscopy, Confocal
  • Mutagenesis, Site-Directed
  • Phosphorylation
  • Polymorphism, Single Nucleotide
  • Protein Binding
  • Protein Conformation
  • RNA, Small Interfering / metabolism
  • Receptors, Adrenergic, beta-1 / genetics
  • Receptors, Adrenergic, beta-1 / metabolism*
  • Receptors, G-Protein-Coupled / metabolism
  • Signal Transduction
  • beta-Arrestins

Substances

  • Arrestins
  • RNA, Small Interfering
  • Receptors, Adrenergic, beta-1
  • Receptors, G-Protein-Coupled
  • beta-Arrestins
  • Arginine
  • Cyclic AMP

Associated data

  • PDB/4AMJ