Adiponectin regulates SR Ca(2+) cycling following ischemia/reperfusion via sphingosine 1-phosphate-CaMKII signaling in mice

J Mol Cell Cardiol. 2014 Sep:74:183-92. doi: 10.1016/j.yjmcc.2014.05.010. Epub 2014 May 20.

Abstract

The adipocyte-secreted hormone adiponectin (APN) exerts protective effects on the heart under stress conditions. Recent studies have demonstrated that APN induces a marked Ca(2+) influx in skeletal muscle. However, whether APN modulates [Ca(2+)]i activity, especially [Ca(2+)]i transients in cardiomyocytes, is still unknown. This study was designed to determine whether APN modulates [Ca(2+)]i transients in cardiomyocytes. Adult male wild-type (WT) and APN knockout (APN KO) mice were subjected to myocardial ischemia/reperfusion (I/R, 30min/30min) injury. CaMKII-PLB phosphorylation and SR Ca(2+)-ATPase (SERCA2) activity were downregulated in I/R hearts of WT mice and further decreased in those of APN KO mice. Both the globular domain of APN and full-length APN significantly reversed the decrease in CaMKII-PLB phosphorylation and SERCA2 activity in WT and APN KO mice. Interestingly, compared with WT littermates, single myocytes isolated from APN KO mice had remarkably decreased [Ca(2+)]i transients, cell shortening, and a prolonged Ca(2+) decay rate. Further examination revealed that APN enhances SERCA2 activity via CaMKII-PLB signaling. In in vivo and in vitro experiments, both APN receptor 1/2 and S1P were necessary for the APN-stimulated CaMKII-PLB-SERCA2 activation. In addition, S1P activated CaMKII-PLB signaling in neonatal cardiomyocytes in a dose dependent manner and improved [Ca(2+)]i transients in APN KO myocytes via the S1P receptor (S1PR1/3). Further in vivo experiments revealed that pharmacological inhibition of S1PR1/3 and SERCA2 siRNA suppressed APN-mediated cardioprotection during I/R. These data demonstrate that S1P is a novel regulator of SERCA2 that activates CaMKII-PLB signaling and mediates APN-induced cardioprotection.

Keywords: Adiponectin; Myocardial ischemia/reperfusion; SERCA2; Sphingosine 1-phosphate.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adiponectin / antagonists & inhibitors
  • Adiponectin / genetics*
  • Adiponectin / metabolism
  • Adiponectin / pharmacology
  • Animals
  • Calcium / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics*
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
  • Gene Expression Regulation
  • Lysophospholipids / metabolism*
  • Lysophospholipids / pharmacology
  • Male
  • Mice
  • Mice, Knockout
  • Myocardial Reperfusion Injury / genetics*
  • Myocardial Reperfusion Injury / metabolism
  • Myocardial Reperfusion Injury / pathology
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Phosphorylation
  • Protein Structure, Tertiary
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Receptors, Adiponectin / genetics
  • Receptors, Adiponectin / metabolism
  • Receptors, Lysosphingolipid / genetics
  • Receptors, Lysosphingolipid / metabolism
  • Sarcoplasmic Reticulum / drug effects
  • Sarcoplasmic Reticulum / metabolism*
  • Sarcoplasmic Reticulum / pathology
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / genetics*
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism
  • Signal Transduction
  • Sphingosine / analogs & derivatives*
  • Sphingosine / metabolism
  • Sphingosine / pharmacology
  • Sphingosine-1-Phosphate Receptors

Substances

  • Adiponectin
  • Adipoq protein, mouse
  • Lysophospholipids
  • RNA, Small Interfering
  • Receptors, Adiponectin
  • Receptors, Lysosphingolipid
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • adiponectin receptor 1, mouse
  • adiponectin receptor 2, mouse
  • sphingosine-1-phosphate receptor-3, human
  • sphingosine 1-phosphate
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Atp2a2 protein, mouse
  • Sphingosine
  • Calcium