Disruption of type 5 adenylyl cyclase prevents β-adrenergic receptor cardiomyopathy: a novel approach to β-adrenergic receptor blockade

Am J Physiol Heart Circ Physiol. 2014 Nov 15;307(10):H1521-8. doi: 10.1152/ajpheart.00491.2014. Epub 2014 Sep 5.

Abstract

β-Adrenergic receptor (β-AR) blockade is widely used to treat heart failure, since the adverse effects of chronic β-AR stimulation are central to the pathogenesis of this disease state. Transgenic (Tg) mice, where β-AR signaling is chronically enhanced by overexpression of cardiac β₂-ARs, is a surrogate for this mechanism, since these mice develop cardiomyopathy as reflected by reduced left ventricular (LV) function, increased fibrosis, apoptosis, and myocyte hypertrophy. We hypothesized that disruption of type 5 adenylyl cyclase (AC5), which is in the β-AR signaling pathway in the heart, but exerts only a minor β-AR blocking effect, could prevent the cardiomyopathy in β₂-AR Tg mice without the negative effects of full β-AR blockade. Accordingly, we mated β₂-AR Tg mice with AC5 knockout (KO) mice. The β₂-AR Tg × AC5 KO bigenic mice prevented the cardiomyopathy as reflected by improved LV ejection fraction, reduced apoptosis, fibrosis, and myocyte size and preserved exercise capacity. The rescue was not simply due to a β-blocking effect of AC5 KO, since neither baseline LV function nor the response to isoproterenol was diminished substantially compared with the negative inotropic effects of β-blockade. However, AC5 disruption in β₂-AR Tg activates the antioxidant, manganese superoxide dismutase, an important mechanism protecting the heart from cardiomyopathy. These results indicate that disruption of AC5 prevents the cardiomyopathy induced by chronically enhanced β-AR signaling in mice with overexpressed β₂-AR, potentially by enhancing resistance to oxidative stress and apoptosis, suggesting a novel, alternative approach to β-AR blockade.

Keywords: oxidative stress; β-adrenergic receptor signaling.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenylyl Cyclases / deficiency
  • Adenylyl Cyclases / genetics
  • Adenylyl Cyclases / metabolism*
  • Adrenergic beta-Agonists*
  • Animals
  • Apoptosis
  • Cardiomyopathies / chemically induced
  • Cardiomyopathies / enzymology
  • Cardiomyopathies / genetics
  • Cardiomyopathies / pathology
  • Cardiomyopathies / physiopathology
  • Cardiomyopathies / prevention & control*
  • Cell Size
  • Disease Models, Animal
  • Enzyme Activation
  • Exercise Tolerance
  • Fibrosis
  • Isoproterenol*
  • Mice, Knockout
  • Myocardium / enzymology*
  • Myocardium / pathology
  • Receptors, Adrenergic, beta-2 / genetics
  • Receptors, Adrenergic, beta-2 / metabolism*
  • Signal Transduction
  • Stroke Volume
  • Superoxide Dismutase / metabolism
  • Ventricular Function, Left

Substances

  • Adrenergic beta-Agonists
  • Receptors, Adrenergic, beta-2
  • Superoxide Dismutase
  • Adenylyl Cyclases
  • adenylyl cyclase type V
  • Isoproterenol