Blunted cardiac beta-adrenergic response as an early indication of cardiac dysfunction in Duchenne muscular dystrophy

Cardiovasc Res. 2014 Jul 1;103(1):60-71. doi: 10.1093/cvr/cvu119. Epub 2014 May 8.

Abstract

Aims: To determine whether altered beta-adrenergic responses contribute to early cardiac dysfunction in mdx (X-linked muscular dystrophy) mice, an animal model for human Duchenne muscular dystrophy.

Methods and results: Replacement fibrosis in mdx hearts gradually increased with age, suggesting a gradual loss of cardiomyocytes. Echocardiography and intra-left ventricular haemodynamic measurements detected baseline cardiac dysfunction in mdx mice at ≥8 months. However, a reduction of cardiac beta-adrenergic response to isoproterenol (ISO) was already present in mdx mice at 4 months. Ventricular myocytes (VMs) isolated from 4- and 8-month-old mdx mice had greater baseline contractile function {fractional shortening, [Ca(2+)]i, and sarcoplasmic reticulum (SR) Ca(2+) content} and ICa-L than age-matched control VMs and than myocytes isolated from 2-month-old mdx mice. ISO increased myocyte function in the VMs of 4- and 8-month-old mdx mice to the same level as in age-matched control VMs. In the VMs of 12-month-old mdx mice, ISO failed to increase myocyte function to the level in VMs of 12-month-old control mice and could not further increaseICa-L. No differences were observed in the expression of Cav1.2α1c, Cav1.2β1, Cav1.2β2, sarco/endoplasmic reticulum Ca(2+) ATPase (SERCA), and the Na(+)/Ca(2+) exchanger. In contrast, total ryanodine receptor 2 (RyR2) and basal phosphorylation of RyR2, phospholamban, and Cav1.2α1c were found to be increased in hearts of 4-month-old mdx mice; baseline protein kinase A activity was also increased. After ISO treatment, phosphorylation levels were the same in mdx and control hearts. VMs of 4-month-old mdx mice had reduced beta1-adrenergic receptor (β1-AR) density and beta-adrenergic sensitivity.

Conclusion: In young mdx mice, the myocyte increases its contractile function to compensate for myocyte loss. However, these myocytes with enhanced baseline function have reduced potential for stimulation, decreased β1-AR density/sensitivity, leading to blunted cardiac beta-adrenergic response.

Keywords: Beta-adrenergic response; Calcium; Duchenne muscular dystrophy; Heart; Myocyte contraction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic beta-Agonists / pharmacology*
  • Age Factors
  • Animals
  • Calcium / metabolism
  • Calcium Channels, L-Type / metabolism
  • Calcium-Binding Proteins / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Fibrosis
  • Heart / drug effects*
  • Heart / physiopathology*
  • Humans
  • Isoproterenol / pharmacology
  • Male
  • Mice
  • Mice, Inbred mdx
  • Muscular Dystrophy, Animal / genetics
  • Muscular Dystrophy, Animal / physiopathology*
  • Muscular Dystrophy, Duchenne / physiopathology*
  • Myocardial Contraction / drug effects
  • Myocardial Contraction / physiology
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / physiology
  • Receptors, Adrenergic, beta-1 / metabolism
  • Ryanodine Receptor Calcium Release Channel / metabolism
  • Sarcoplasmic Reticulum / metabolism

Substances

  • Adrenergic beta-Agonists
  • CACNA1C protein, mouse
  • Calcium Channels, L-Type
  • Calcium-Binding Proteins
  • Receptors, Adrenergic, beta-1
  • Ryanodine Receptor Calcium Release Channel
  • phospholamban
  • Cyclic AMP-Dependent Protein Kinases
  • Isoproterenol
  • Calcium