Induced overexpression of phospholemman S68E mutant improves cardiac contractility and mortality after ischemia-reperfusion

Am J Physiol Heart Circ Physiol. 2014 Apr 1;306(7):H1066-77. doi: 10.1152/ajpheart.00861.2013. Epub 2014 Jan 31.

Abstract

Phospholemman (PLM), when phosphorylated at Ser(68), inhibits cardiac Na+ / Ca2+ exchanger 1 (NCX1) and relieves its inhibition on Na+ -K+ -ATPase. We have engineered mice in which expression of the phosphomimetic PLM S68E mutant was induced when dietary doxycycline was removed at 5 wk. At 8-10 wk, compared with noninduced or wild-type hearts, S68E expression in induced hearts was ∼35-75% that of endogenous PLM, but protein levels of sarco(endo)plasmic reticulum Ca2+ -ATPase, α1- and α2-subunits of Na+ -K+ -ATPase, α1c-subunit of L-type Ca2+ channel, and phosphorylated ryanodine receptor were unchanged. The NCX1 protein level was increased by ∼47% but the NCX1 current was depressed by ∼34% in induced hearts. Isoproterenol had no effect on NCX1 currents but stimulated Na+ -K+ -ATPase currents equally in induced and noninduced myocytes. At baseline, systolic intracellular Ca2+ concentrations ([Ca2+]i), sarcoplasmic reticulum Ca2+ contents, and [Ca(2+)]i transient and contraction amplitudes were similar between induced and noninduced myocytes. Isoproterenol stimulation resulted in much higher systolic [Ca2+]i, sarcoplasmic reticulum Ca2+ content, and [Ca2+]i transient and contraction amplitudes in induced myocytes. Echocardiography and in vivo close-chest catheterization demonstrated similar baseline myocardial function, but isoproterenol induced a significantly higher +dP/dt in induced compared with noninduced hearts. In contrast to the 50% mortality observed in mice constitutively overexpressing the S68E mutant, induced mice had similar survival as wild-type and noninduced mice. After ischemia-reperfusion, despite similar areas at risk and left ventricular infarct sizes, induced mice had significantly higher +dP/dt and -dP/dt and lower perioperative mortality compared with noninduced mice. We propose that phosphorylated PLM may be a novel therapeutic target in ischemic heart disease.

Keywords: FXYD proteins; in vivo hemodynamics; intracellular Ca2+ regulation; ischemic cardiomyopathy.

Publication types

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

MeSH terms

  • Adrenergic beta-Agonists / pharmacology
  • Animals
  • Calcium Channels, L-Type / metabolism
  • Calcium Signaling
  • Cardiotonic Agents / pharmacology
  • Disease Models, Animal
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Transgenic
  • Mutation*
  • Myocardial Contraction* / drug effects
  • Myocardial Infarction / drug therapy
  • Myocardial Infarction / metabolism*
  • Myocardial Infarction / pathology
  • Myocardial Infarction / physiopathology
  • Myocardial Reperfusion Injury / drug therapy
  • Myocardial Reperfusion Injury / metabolism*
  • Myocardial Reperfusion Injury / pathology
  • Myocardial Reperfusion Injury / physiopathology
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism*
  • Recovery of Function
  • Ryanodine Receptor Calcium Release Channel / metabolism
  • Sarcoplasmic Reticulum / metabolism
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism
  • Sodium-Calcium Exchanger / metabolism
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Stroke Volume
  • Up-Regulation
  • Ventricular Dysfunction, Left / metabolism
  • Ventricular Dysfunction, Left / pathology
  • Ventricular Dysfunction, Left / physiopathology
  • Ventricular Dysfunction, Left / prevention & control*
  • Ventricular Function, Left* / drug effects
  • Ventricular Pressure

Substances

  • Adrenergic beta-Agonists
  • CACNA1C protein, mouse
  • Calcium Channels, L-Type
  • Cardiotonic Agents
  • Membrane Proteins
  • NCX1 protein, mouse
  • Phosphoproteins
  • Ryanodine Receptor Calcium Release Channel
  • Sodium-Calcium Exchanger
  • phospholemman
  • Atp1a2 protein, mouse
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Atp2a2 protein, mouse
  • Atp1a1 protein, mouse
  • Sodium-Potassium-Exchanging ATPase