Type 1 inositol (1,4,5)-trisphosphate receptor activates ryanodine receptor 1 to mediate calcium spark signaling in adult mammalian skeletal muscle

J Biol Chem. 2013 Jan 25;288(4):2103-9. doi: 10.1074/jbc.M112.425975. Epub 2012 Dec 5.

Abstract

Functional coupling between inositol (1,4,5)-trisphosphate receptor (IP(3)R) and ryanodine receptor (RyR) represents a critical component of intracellular Ca(2+) signaling in many excitable cells; however, the role of this mechanism in skeletal muscle remains elusive. In skeletal muscle, RyR-mediated Ca(2+) sparks are suppressed in resting conditions, whereas application of transient osmotic stress can trigger activation of Ca(2+) sparks that are restricted to the periphery of the fiber. Here we show that onset of these spatially confined Ca(2+) sparks involves interaction between activation of IP(3)R and RyR near the sarcolemmal membrane. Pharmacological prevention of IP(3) production or inhibition of IP(3)R channel activity abolishes stress-induced Ca(2+) sparks in skeletal muscle. Although genetic ablation of the type 2 IP(3)R does not appear to affect Ca(2+) sparks in skeletal muscle, specific silencing of the type 1 IP(3)R leads to ablation of stress-induced Ca(2+) sparks. Our data indicate that membrane-delimited signaling involving cross-talk between IP(3)R1 and RyR1 contributes to Ca(2+) spark activation in skeletal muscle.

Publication types

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

MeSH terms

  • Animals
  • Calcium / chemistry
  • Calcium / metabolism*
  • Calcium Signaling
  • Gene Expression Regulation*
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism*
  • Mice
  • Microscopy, Confocal / methods
  • Models, Biological
  • Models, Genetic
  • Muscle Fibers, Skeletal / metabolism*
  • Muscle, Skeletal / metabolism*
  • Osmosis
  • Patch-Clamp Techniques
  • Plasmids / metabolism
  • RNA, Small Interfering / metabolism
  • Ryanodine Receptor Calcium Release Channel / metabolism*
  • Signal Transduction

Substances

  • Inositol 1,4,5-Trisphosphate Receptors
  • RNA, Small Interfering
  • Ryanodine Receptor Calcium Release Channel
  • Calcium