Regulation of in vivo cardiac contractility by phospholemman: role of Na+/Ca2+ exchange

Am J Physiol Heart Circ Physiol. 2011 Mar;300(3):H859-68. doi: 10.1152/ajpheart.00894.2010. Epub 2010 Dec 30.

Abstract

Phospholemman (PLM), when phosphorylated at serine 68, relieves its inhibition on Na(+)-K(+)-ATPase but inhibits Na(+)/Ca(2+) exchanger 1 (NCX1) in cardiac myocytes. Under stress when catecholamine levels are high, enhanced Na(+)-K(+)-ATPase activity by phosphorylated PLM attenuates intracellular Na(+) concentration ([Na(+)](i)) overload. To evaluate the effects of PLM on NCX1 on in vivo cardiac contractility, we injected recombinant adeno-associated virus (serotype 9) expressing either the phosphomimetic PLM S68E mutant or green fluorescent protein (GFP) directly into left ventricles (LVs) of PLM-knockout (KO) mice. Five weeks after virus injection, ∼40% of isolated LV myocytes exhibited GFP fluorescence. Expression of S68E mutant was confirmed with PLM antibody. There were no differences in protein levels of α(1)- and α(2)-subunits of Na(+)-K(+)-ATPase, NCX1, and sarco(endo)plasmic reticulum Ca(2+)-ATPase between KO-GFP and KO-S68E LV homogenates. Compared with KO-GFP myocytes, Na(+)/Ca(2+) exchange current was suppressed, but resting [Na(+)](i), Na(+)-K(+)-ATPase current, and action potential amplitudes were similar in KO-S68E myocytes. Resting membrane potential was slightly lower and action potential duration at 90% repolarization (APD(90)) was shortened in KO-S68E myocytes. Isoproterenol (Iso; 1 μM) increased APD(90) in both groups of myocytes. After Iso, [Na(+)](i) increased monotonically in paced (2 Hz) KO-GFP but reached a plateau in KO-S68E myocytes. Both systolic and diastolic [Ca(2+)](i) were higher in Iso-stimulated KO-S68E myocytes paced at 2 Hz. Echocardiography demonstrated similar resting heart rate, ejection fraction, and LV mass between KO-GFP and KO-S68E mice. In vivo closed-chest catheterization demonstrated enhanced contractility in KO-S68E compared with KO-GFP hearts stimulated with Iso. We conclude that under catecholamine stress when [Na(+)](i) is high, PLM minimizes [Na(+)](i) overload by relieving its inhibition of Na(+)-K(+)-ATPase and preserves inotropy by simultaneously inhibiting Na(+)/Ca(2+) exchanger.

Publication types

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

MeSH terms

  • Animals
  • Cardiotonic Agents / pharmacology
  • Cells, Cultured
  • Heart / drug effects
  • Heart / physiology
  • Isoproterenol / pharmacology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myocardial Contraction / drug effects
  • Myocardial Contraction / physiology*
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / physiology
  • Phosphoproteins / metabolism
  • Phosphoproteins / physiology*
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / physiology
  • Sodium-Calcium Exchanger / metabolism
  • Sodium-Calcium Exchanger / physiology*
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Sodium-Potassium-Exchanging ATPase / physiology

Substances

  • Cardiotonic Agents
  • Membrane Proteins
  • NCX1 protein, mouse
  • Phosphoproteins
  • Sodium-Calcium Exchanger
  • phospholemman
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Sodium-Potassium-Exchanging ATPase
  • Isoproterenol