Cardioprotective Angiotensin-(1-7) Peptide Acts as a Natural-Biased Ligand at the Angiotensin II Type 1 Receptor

Hypertension. 2016 Dec;68(6):1365-1374. doi: 10.1161/HYPERTENSIONAHA.116.08118. Epub 2016 Oct 3.

Abstract

Hyperactivity of the renin-angiotensin-aldosterone system through the angiotensin II (Ang II)/Ang II type 1 receptor (AT1-R) axis constitutes a hallmark of hypertension. Recent findings indicate that only a subset of AT1-R signaling pathways is cardiodeleterious, and their selective inhibition by biased ligands promotes therapeutic benefit. To date, only synthetic biased ligands have been described, and whether natural renin-angiotensin-aldosterone system peptides exhibit functional selectivity at AT1-R remains unknown. In this study, we systematically determined efficacy and potency of Ang II, Ang III, Ang IV, and Ang-(1-7) in AT1-R-expressing HEK293T cells on the activation of cardiodeleterious G-proteins and cardioprotective β-arrestin2. Ang III and Ang IV fully activate similar G-proteins than Ang II, the prototypical AT1-R agonist, despite weaker potency of Ang IV. Interestingly, Ang-(1-7) that binds AT1-R fails to promote G-protein activation but behaves as a competitive antagonist for Ang II/Gi and Ang II/Gq pathways. Conversely, all renin-angiotensin-aldosterone system peptides act as agonists on the AT1-R/β-arrestin2 axis but display biased activities relative to Ang II as indicated by their differences in potency and AT1-R/β-arrestin2 intracellular routing. Importantly, we reveal Ang-(1-7) a known Mas receptor-specific ligand, as an AT1-R-biased agonist, selectively promoting β-arrestin activation while blocking the detrimental Ang II/AT1-R/Gq axis. This original pharmacological profile of Ang-(1-7) at AT1-R, similar to that of synthetic AT1-R-biased agonists, could, in part, contribute to its cardiovascular benefits. Accordingly, in vivo, Ang-(1-7) counteracts the phenylephrine-induced aorta contraction, which was blunted in AT1-R knockout mice. Collectively, these data suggest that Ang-(1-7) natural-biased agonism at AT1-R could fine-tune the physiology of the renin-angiotensin-aldosterone system.

Keywords: G-protein–coupled receptor; angiotensin 1-7; angiotensin II type 1 receptor; biased agonism; renin–angiotensin system; β-arrestin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin I / metabolism*
  • Angiotensin II / pharmacology*
  • Animals
  • Aorta, Abdominal / drug effects
  • Aorta, Abdominal / physiology
  • Cardiotonic Agents / metabolism*
  • Cells, Cultured / drug effects
  • Cells, Cultured / metabolism
  • HEK293 Cells / drug effects
  • HEK293 Cells / metabolism*
  • Humans
  • Muscles
  • Peptide Fragments / metabolism*
  • Phenylephrine / pharmacology
  • Receptor, Angiotensin, Type 2 / metabolism*
  • Renin-Angiotensin System / drug effects
  • Renin-Angiotensin System / physiology
  • Sensitivity and Specificity
  • Signal Transduction
  • Vasoconstriction / drug effects
  • Vasoconstriction / physiology
  • beta-Arrestins / metabolism

Substances

  • Cardiotonic Agents
  • Peptide Fragments
  • Receptor, Angiotensin, Type 2
  • beta-Arrestins
  • Angiotensin II
  • Phenylephrine
  • Angiotensin I
  • angiotensin I (1-7)