Cardiac responses to β-adrenoceptor stimulation is partly dependent on mitochondrial calcium uniporter activity

Br J Pharmacol. 2014 Sep;171(18):4207-21. doi: 10.1111/bph.12684. Epub 2014 Jul 1.

Abstract

Background and purpose: Despite the importance of mitochondrial Ca(2+) to metabolic regulation and cell physiology, little is known about the mechanisms that regulate Ca(2+) entry into the mitochondria. Accordingly, we established a system to determine the role of the mitochondrial Ca(2+) uniporter in an isolated heart model, at baseline and during increased workload following β-adrenoceptor stimulation.

Experimental approach: Cardiac contractility, oxygen consumption and intracellular Ca(2+) transients were measured in ex vivo perfused murine hearts. Ru360 and spermine were used to modify mitochondrial Ca(2+) uniporter activity. Changes in mitochondrial Ca(2+) content and energetic phosphate metabolite levels were determined.

Key results: The addition of Ru360 , a selective inhibitor of the mitochondrial Ca(2+) uniporter, induced progressively and sustained negative inotropic effects that were dose-dependent with an EC50 of 7 μM. Treatment with spermine, a uniporter agonist, showed a positive inotropic effect that was blocked by Ru360 . Inotropic stimulation with isoprenaline elevated oxygen consumption (2.7-fold), Ca(2+) -dependent activation of pyruvate dehydrogenase (5-fold) and mitochondrial Ca(2+) content (2.5-fold). However, in Ru360 -treated hearts, this parameter was attenuated. In addition, β-adrenoceptor stimulation in the presence of Ru360 did not affect intracellular Ca(2+) handling, PKA or Ca(2+) /calmodulin-dependent PK signalling.

Conclusions and implications: Inhibition of the mitochondrial Ca(2+) uniporter decreases β-adrenoceptor response, uncoupling between workload and production of energetic metabolites. Our results support the hypothesis that the coupling of workload and energy supply is partly dependent on mitochondrial Ca(2+) uniporter activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic beta-Agonists / pharmacology
  • Animals
  • Calcium / physiology*
  • Calcium Channels / physiology*
  • Calcium-Binding Proteins / metabolism
  • Cardiotonic Agents / pharmacology
  • Cyclic AMP / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Glutathione / metabolism
  • Heart / drug effects
  • Heart / physiology*
  • Isoproterenol / pharmacology
  • Male
  • Mice
  • Mitochondria, Heart / drug effects
  • Mitochondria, Heart / physiology*
  • Myocytes, Cardiac / metabolism
  • Oxidative Stress / drug effects
  • Oxygen Consumption
  • Rats, Wistar
  • Receptors, Adrenergic, beta / physiology*
  • Ruthenium Compounds / pharmacology
  • Spermine / pharmacology

Substances

  • Adrenergic beta-Agonists
  • Calcium Channels
  • Calcium-Binding Proteins
  • Cardiotonic Agents
  • Receptors, Adrenergic, beta
  • Ru 360
  • Ruthenium Compounds
  • mitochondrial calcium uniporter
  • phospholamban
  • Spermine
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • Glutathione
  • Isoproterenol
  • Calcium