Induction of cardiac fibrosis by β-blocker in G protein-independent and G protein-coupled receptor kinase 5/β-arrestin2-dependent Signaling pathways

J Biol Chem. 2012 Oct 12;287(42):35669-35677. doi: 10.1074/jbc.M112.357871. Epub 2012 Aug 10.

Abstract

G-protein coupled receptors (GPCRs) have long been known as receptors that activate G protein-dependent cellular signaling pathways. In addition to the G protein-dependent pathways, recent reports have revealed that several ligands called "biased ligands" elicit G protein-independent and β-arrestin-dependent signaling through GPCRs (biased agonism). Several β-blockers are known as biased ligands. All β-blockers inhibit the binding of agonists to the β-adrenergic receptors. In addition to β-blocking action, some β-blockers are reported to induce cellular responses through G protein-independent and β-arrestin-dependent signaling pathways. However, the physiological significance induced by the β-arrestin-dependent pathway remains much to be clarified in vivo. Here, we demonstrate that metoprolol, a β(1)-adrenergic receptor-selective blocker, could induce cardiac fibrosis through a G protein-independent and β-arrestin2-dependent pathway. Metoprolol, a β-blocker, increased the expression of fibrotic genes responsible for cardiac fibrosis in cardiomyocytes. Furthermore, metoprolol induced the interaction between β(1)-adrenergic receptor and β-arrestin2, but not β-arrestin1. The interaction between β(1)-adrenergic receptor and β-arrestin2 by metoprolol was impaired in the G protein-coupled receptor kinase 5 (GRK5)-knockdown cells. Metoprolol-induced cardiac fibrosis led to cardiac dysfunction. However, the metoprolol-induced fibrosis and cardiac dysfunction were not evoked in β-arrestin2- or GRK5-knock-out mice. Thus, metoprolol is a biased ligand that selectively activates a G protein-independent and GRK5/β-arrestin2-dependent pathway, and induces cardiac fibrosis. This study demonstrates the physiological importance of biased agonism, and suggests that G protein-independent and β-arrestin-dependent signaling is a reason for the diversity of the effectiveness of β-blockers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic beta-1 Receptor Antagonists / adverse effects*
  • Adrenergic beta-1 Receptor Antagonists / pharmacology
  • Animals
  • Arrestins / genetics
  • Arrestins / metabolism*
  • Fibrosis
  • G-Protein-Coupled Receptor Kinase 5 / genetics
  • G-Protein-Coupled Receptor Kinase 5 / metabolism*
  • HEK293 Cells
  • Heart Diseases / chemically induced*
  • Heart Diseases / genetics
  • Heart Diseases / metabolism*
  • Heart Diseases / pathology
  • Humans
  • Metoprolol / adverse effects*
  • Metoprolol / pharmacology
  • Mice
  • Mice, Knockout
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / drug effects*
  • Signal Transduction / genetics
  • beta-Arrestins

Substances

  • Adrenergic beta-1 Receptor Antagonists
  • Arrestins
  • Muscle Proteins
  • beta-Arrestins
  • G-Protein-Coupled Receptor Kinase 5
  • Grk5 protein, mouse
  • Grk5 protein, rat
  • Metoprolol