Important role of energy-dependent mitochondrial pathways in cultured rat cardiac myocyte apoptosis

Am J Physiol Heart Circ Physiol. 2001 Oct;281(4):H1637-47. doi: 10.1152/ajpheart.2001.281.4.H1637.

Abstract

Recent studies have suggested that apoptosis and necrosis share common features in their signaling pathway and that apoptosis requires intracellular ATP for its mitochondrial/apoptotic protease-activating factor-1 suicide cascade. The present study was, therefore, designed to examine the role of intracellular energy levels in determining the form of cell death in cardiac myocytes. Neonatal rat cardiac myocytes were first incubated for 1 h in glucose-free medium containing oligomycin to achieve metabolic inhibition. The cells were then incubated for another 4 h in similar medium containing staurosporine and graded concentrations of glucose to manipulate intracellular ATP levels. Under ATP-depleting conditions, the cell death caused by staurosporine was primarily necrotic, as determined by creatine kinase release and nuclear staining with ethidium homodimer-1. However, under ATP-replenishing conditions, staurosporine increased the percentage of apoptotic cells, as determined by nuclear morphology and DNA fragmentation. Caspase-3 activation by staurosporine was also ATP dependent. However, loss of mitochondrial transmembrane potential (DeltaPsi(m)), Bax translocation, and cytochrome c release were observed in both apoptotic and necrotic cells. Moreover, cyclosporin A, an inhibitor of mitochondrial permeability transition, attenuated staurosporine-induced apoptosis and necrosis through the inhibition of DeltaPsi(m) reduction, cytochrome c release, and caspase-3 activation. Our data therefore suggest that staurosporine induces cell demise through a mitochondrial death signaling pathway and that the presence of intracellular ATP favors a shift from necrosis to apoptosis through caspase activation.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Apoptosis / physiology*
  • Biological Transport
  • Caspase 3
  • Caspases / metabolism
  • Cell Survival / drug effects
  • Cells, Cultured
  • Cyclosporine / pharmacology
  • Cytochrome c Group / metabolism
  • Energy Metabolism*
  • Enzyme Activation / drug effects
  • Enzyme Inhibitors / pharmacology
  • Glucose / pharmacology
  • Heart / physiology*
  • Membrane Potentials
  • Mitochondria, Heart / physiology*
  • Myocardium / cytology
  • Myocardium / metabolism
  • Osmolar Concentration
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-bcl-2*
  • Rats
  • Rats, Wistar
  • Staurosporine / pharmacology
  • bcl-2-Associated X Protein

Substances

  • Bax protein, rat
  • Cytochrome c Group
  • Enzyme Inhibitors
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • bcl-2-Associated X Protein
  • Cyclosporine
  • Adenosine Triphosphate
  • Casp3 protein, rat
  • Caspase 3
  • Caspases
  • Staurosporine
  • Glucose