Chronic sympathetic activation promotes downregulation of β-adrenoceptor-mediated effects in the guinea pig heart independently of structural remodeling and systolic dysfunction

Pflugers Arch. 2011 Oct;462(4):529-43. doi: 10.1007/s00424-011-1005-7. Epub 2011 Aug 3.

Abstract

It is uncertain if downregulation of β-adrenoceptor signaling pathway is promoted by an enhanced adrenergic tone at an early stage of cardiac disease, or it develops secondary to detrimental local myocardial changes in advanced heart failure. We examined the integrity of β-adrenoceptor signaling pathway upon chronic infusion of isoproterenol, a β-adrenoceptor agonist, at a dose producing no structural left ventricular (LV) remodeling and systolic dysfunction. Subcutaneous isoproterenol infusion (400 μg kg(-1) h(-1) over 16 days) to guinea pigs using osmotic minipumps produced no change in cardiac weights, LV internal dimensions, myocyte cross-sectional area, extent of interstitial fibrosis, and basal contractile function. Isolated, perfused heart preparations from isoproterenol-treated guinea pigs exhibited attenuated responsiveness to acute β-adrenoceptor stimulation, as evidenced by reduced LV developed pressure increase, less shortening of LV epicardial monophasic action potential and effective refractory period, and less myocardial cyclic adenosine monophosphate elevation, in response to isoproterenol exposure, when compared to saline-treated controls. Pharmacological responses to forskolin, an activator of the adenylate cyclase catalytic subunit, were well preserved in isoproterenol-treated hearts. Downregulation of β-adrenoceptor-mediated effects upon chronic isoproterenol infusion was associated with markedly reduced stimulatory G-protein α-subunit (G(sα)) myocardial expression levels. No change in expression levels of β-adrenoceptors, G-protein-coupled receptor kinase 2, inhibitory G-protein α-subunit (G(iα2)), and Ca(v)1.2 and K(v)7.1 ion channels was determined in isoproterenol-treated hearts. We therefore conclude that sustained adrenergic overstimulation may promote downregulation of myocardial β-adrenoceptor-mediated effects independently of structural LV remodeling and systolic failure, an effect attributed to β-adrenoceptor uncoupling from adenylate cyclase due to reduced G(sα)-protein expression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic beta-Agonists / pharmacology*
  • Animals
  • Calcium Channels, L-Type / metabolism
  • Colforsin / pharmacology
  • Cyclic AMP / metabolism
  • Down-Regulation / drug effects
  • G-Protein-Coupled Receptor Kinase 2 / biosynthesis
  • GTP-Binding Protein alpha Subunits, Gs / biosynthesis
  • Guinea Pigs
  • Isoproterenol / pharmacology
  • KCNQ1 Potassium Channel / metabolism
  • Male
  • Myocardial Contraction / drug effects
  • Myocardium / metabolism*
  • Receptors, Adrenergic, beta / drug effects*
  • Receptors, Adrenergic, beta / physiology
  • Refractory Period, Electrophysiological
  • Signal Transduction / drug effects*
  • Systole / drug effects*
  • Ventricular Remodeling / drug effects

Substances

  • Adrenergic beta-Agonists
  • Calcium Channels, L-Type
  • KCNQ1 Potassium Channel
  • Receptors, Adrenergic, beta
  • Colforsin
  • Cyclic AMP
  • G-Protein-Coupled Receptor Kinase 2
  • GTP-Binding Protein alpha Subunits, Gs
  • Isoproterenol