Enhanced G(i) signaling selectively negates beta2-adrenergic receptor (AR)--but not beta1-AR-mediated positive inotropic effect in myocytes from failing rat hearts

Circulation. 2003 Sep 30;108(13):1633-9. doi: 10.1161/01.CIR.0000087595.17277.73. Epub 2003 Sep 15.

Abstract

Background: Myocardial contractile response to beta1- and beta2-adrenergic receptor (AR) stimulation is severely impaired in chronic heart failure, in which G(i) signaling and the ratio of beta2/beta1 are often increased. Because beta2-AR but not beta1-AR couples to G(s) and G(i) with the G(i) coupling negating the G(s)-mediated contractile response, we determined whether the heart failure-associated augmentation of G(i) signaling contributes differentially to the defects of these beta-AR subtypes and, if so, whether inhibition of G(i) or selective activation of beta2-AR/G(s) by ligands restores beta2-AR contractile response in the failing heart.

Methods and results: Cardiomyocytes were isolated from 18- to 24-month-old failing spontaneously hypertensive (SHR) or age-matched Wistar-Kyoto (WKY) rat hearts. In SHR cardiomyocytes, either beta-AR subtype-mediated inotropic effect was markedly diminished, whereas G(i) proteins and the beta2/beta1 ratio were increased. Disruption of G(i) signaling by pertussis toxin (PTX) enabled beta2- but not beta1-AR to induce a full positive inotropic response in SHR myocytes. Furthermore, screening of a panel of beta2-AR ligands revealed that the contractile response mediated by most beta2-AR agonists, including zinterol, salbutamol, and procaterol, was potentiated by PTX, indicating concurrent G(s) and G(i) activation. In contrast, fenoterol, another beta2-AR agonist, induced a full positive inotropic effect in SHR myocytes even in the absence of PTX.

Conclusions: We conclude that enhanced G(i) signaling is selectively involved in the dysfunction of beta2- but not beta1-AR in failing SHR hearts and that disruption of G(i) signaling by PTX or selective activation of beta2-AR/G(s) signaling by fenoterol restores the blunted beta2-AR contractile response in the failing heart.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adrenergic beta-1 Receptor Antagonists*
  • Adrenergic beta-2 Receptor Agonists
  • Adrenergic beta-Agonists / pharmacology
  • Animals
  • Cardiac Output, Low / etiology
  • Cardiac Output, Low / metabolism
  • Cardiac Output, Low / physiopathology*
  • Cardiotonic Agents / pharmacology
  • Cells, Cultured
  • Chronic Disease
  • Fenoterol / pharmacology
  • GTP-Binding Protein alpha Subunits, Gi-Go / antagonists & inhibitors
  • GTP-Binding Protein alpha Subunits, Gi-Go / metabolism*
  • Heterotrimeric GTP-Binding Proteins / analysis
  • Ligands
  • Myocardial Contraction* / drug effects
  • Myocardium / chemistry
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / physiology
  • Pertussis Toxin / pharmacology
  • Rats
  • Rats, Inbred SHR
  • Rats, Inbred WKY
  • Receptors, Adrenergic, beta-1 / analysis
  • Receptors, Adrenergic, beta-1 / metabolism
  • Receptors, Adrenergic, beta-2 / analysis
  • Receptors, Adrenergic, beta-2 / metabolism*
  • Signal Transduction / drug effects

Substances

  • Adrenergic beta-1 Receptor Antagonists
  • Adrenergic beta-2 Receptor Agonists
  • Adrenergic beta-Agonists
  • Cardiotonic Agents
  • Ligands
  • Receptors, Adrenergic, beta-1
  • Receptors, Adrenergic, beta-2
  • Fenoterol
  • Pertussis Toxin
  • GTP-Binding Protein alpha Subunits, Gi-Go
  • Heterotrimeric GTP-Binding Proteins