Membrane electrical activity elicits inositol 1,4,5-trisphosphate-dependent slow Ca2+ signals through a Gbetagamma/phosphatidylinositol 3-kinase gamma pathway in skeletal myotubes

J Biol Chem. 2006 Apr 28;281(17):12143-54. doi: 10.1074/jbc.M511218200. Epub 2006 Mar 2.

Abstract

Tetanic electrical stimulation of myotubes evokes a ryanodine receptor-related fast calcium signal, during the stimulation, followed by a phospholipase C/inositol 1,4,5-trisphosphate-dependent slow calcium signal few seconds after stimulus end. L-type calcium channels (Cav 1.1, dihydropyridine receptors) acting as voltage sensors activate an unknown signaling pathway involved in phospholipase C activation. We demonstrated that both G protein and phosphatidylinositol 3-kinase were activated by electrical stimulation, and both the inositol 1,4,5-trisphosphate rise and slow calcium signal induced by electrical stimulation were blocked by pertussis toxin, by a Gbetagamma scavenger peptide, and by phosphatidylinositol 3-kinase inhibitors. Immunofluorescence using anti-phosphatidylinositol 3-kinase gamma antibodies showed a clear location in striations within the cytoplasm, consistent with a position near the I band region of the sarcomere. The time course of phosphatidylinositol 3-kinase activation, monitored in single living cells using a pleckstrin homology domain fused to green fluorescent protein, was compatible with sequential phospholipase Cgamma1 activation as confirmed by phosphorylation assays for the enzyme. Co-transfection of a dominant negative form of phosphatidylinositol 3-kinase gamma inhibited the phosphatidylinositol 3-kinase activity as well as the slow calcium signal. We conclude that Gbetagamma/phosphatidylinositol 3-kinase gamma signaling pathway is involved in phospholipase C activation and the generation of the slow calcium signal induced by tetanic stimulation. We postulate that membrane potential fluctuations in skeletal muscle cells can activate a pertussis toxin-sensitive G protein, phosphatidylinositol 3-kinase, phospholipase C pathway toward modulation of long term, activity-dependent plastic changes.

Publication types

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

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Class Ib Phosphatidylinositol 3-Kinase
  • Cytoplasm / metabolism
  • Electrophysiology
  • Enzyme Inhibitors / pharmacology
  • GTP-Binding Protein beta Subunits / metabolism*
  • GTP-Binding Protein gamma Subunits / metabolism*
  • Inositol 1,4,5-Trisphosphate / metabolism*
  • Isoenzymes / metabolism
  • Membrane Potentials / physiology*
  • Muscle Fibers, Skeletal / cytology
  • Muscle Fibers, Skeletal / metabolism*
  • Muscle, Skeletal / cytology
  • Muscle, Skeletal / metabolism
  • Peptide Fragments / metabolism
  • Pertussis Toxin / pharmacology
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Rats
  • Signal Transduction*
  • Type C Phospholipases / metabolism

Substances

  • Enzyme Inhibitors
  • GTP-Binding Protein beta Subunits
  • GTP-Binding Protein gamma Subunits
  • Isoenzymes
  • Peptide Fragments
  • Inositol 1,4,5-Trisphosphate
  • Pertussis Toxin
  • Phosphatidylinositol 3-Kinases
  • Class Ib Phosphatidylinositol 3-Kinase
  • Type C Phospholipases
  • Calcium