Conformational Profiling of the AT1 Angiotensin II Receptor Reflects Biased Agonism, G Protein Coupling, and Cellular Context

J Biol Chem. 2017 Mar 31;292(13):5443-5456. doi: 10.1074/jbc.M116.763854. Epub 2017 Feb 17.

Abstract

Here, we report the design and use of G protein-coupled receptor-based biosensors to monitor ligand-mediated conformational changes in receptors in intact cells. These biosensors use bioluminescence resonance energy transfer with Renilla luciferase (RlucII) as an energy donor, placed at the distal end of the receptor C-tail, and the small fluorescent molecule FlAsH as an energy acceptor, its binding site inserted at different positions throughout the intracellular loops and C-terminal tail of the angiotensin II type I receptor. We verified that the modifications did not compromise receptor localization or function before proceeding further. Our biosensors were able to capture effects of both canonical and biased ligands, even to the extent of discriminating between different biased ligands. Using a combination of G protein inhibitors and HEK 293 cell lines that were CRISPR/Cas9-engineered to delete Gαq, Gα11, Gα12, and Gα13 or β-arrestins, we showed that Gαq and Gα11 are required for functional responses in conformational sensors in ICL3 but not ICL2. Loss of β-arrestin did not alter biased ligand effects on ICL2P2. We also demonstrate that such biosensors are portable between different cell types and yield context-dependent readouts of G protein-coupled receptor conformation. Our study provides mechanistic insights into signaling events that depend on either G proteins or β-arrestin.

Keywords: G protein; G protein-coupled receptor (GPCR); angiotensin II; cell signaling; signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / metabolism
  • Cell Engineering / methods
  • Cell Line
  • Fluorescence Resonance Energy Transfer
  • GTP-Binding Proteins / antagonists & inhibitors
  • GTP-Binding Proteins / metabolism
  • Humans
  • Ligands
  • Methods
  • Protein Conformation
  • Receptor, Angiotensin, Type 1 / chemistry*
  • Signal Transduction
  • beta-Arrestins / metabolism

Substances

  • Ligands
  • Receptor, Angiotensin, Type 1
  • beta-Arrestins
  • Angiotensin II
  • GTP-Binding Proteins

Associated data

  • PDB/4YAY

Grants and funding