Mini-dystrophin expression down-regulates overactivation of G protein-mediated IP3 signaling pathway in dystrophin-deficient muscle cells

J Gen Physiol. 2006 Feb;127(2):171-82. doi: 10.1085/jgp.200509456.

Abstract

We present here evidence for the enhancement of an inositol 1,4,5-trisphosphate (IP3) mediated calcium signaling pathway in myotubes from dystrophin-deficient cell lines (SolC1(-)) as compared to a cell line from the same origin but transfected with mini-dystrophin (SolD(+)). With confocal microscopy, we demonstrated that calcium rise, induced by the perifusion of a solution containing a high potassium concentration, was higher in SolC1(-) than in SolD(+) myotubes. The analysis of amplitude and kinetics of the calcium increase in SolC1(-) and in SolD(+) myotubes during the exposure with SR Ca2+ channel inhibitors (ryanodine and 2-APB) suggested the presence of two mechanisms of SR calcium release: (1) a fast SR calcium release that depended on ryanodine receptors and (2) a slow SR calcium release mediated by IP3 receptors. Detection analyses of mRNAs (reverse transcriptase [RT]-PCR) and proteins (Western blot and immunolocalization) demonstrated the presence of the three known isoforms of IP3 receptors in both SolC1(-) and SolD(+) myotubes. Furthermore, analysis of the kinetics of the rise in calcium revealed that the slow IP3-dependent release may be increased in the SolC1(-) as compared to the SolD(+), suggesting an inhibitory effect of mini-dystrophin in this signaling pathway. Upon incubation with pertussis toxin (PTX), an inhibitory effect similar to that of the IP3R inhibitor (2-APB) was observed on K+-evoked calcium release. This result suggests the involvement of a Gi protein upstream of the IP3 pathway in these stimulation conditions. A hypothetical model is depicted in which both Gi protein and IP3 production could be involved in K+-evoked calcium release as well as a possible interaction with mini-dystrophin. Our findings demonstrate the existence of a potential relationship between mini-dystrophin and SR calcium release as well as a regulatory role of mini-dystrophin on intracellular signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Calcium / metabolism*
  • Calcium Channels / analysis
  • Calcium Channels / chemistry
  • Calcium Channels / drug effects
  • Calcium Channels / genetics
  • Calcium Channels / metabolism
  • Calcium Channels / physiology
  • Calcium Signaling*
  • Cell Line
  • Down-Regulation
  • Dystrophin / analysis
  • Dystrophin / deficiency
  • Dystrophin / genetics
  • Dystrophin / physiology*
  • GTP-Binding Protein alpha Subunits, Gi-Go / physiology
  • GTP-Binding Proteins / physiology*
  • Gene Expression
  • Inositol 1,4,5-Trisphosphate / metabolism*
  • Inositol 1,4,5-Trisphosphate Receptors
  • Mice
  • Mice, Inbred C3H
  • Microscopy, Confocal
  • Muscle Fibers, Skeletal / metabolism*
  • Pertussis Toxin / pharmacology
  • Potassium / pharmacology
  • RNA, Messenger / analysis
  • Receptors, Cytoplasmic and Nuclear / chemistry
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Ryanodine Receptor Calcium Release Channel / physiology

Substances

  • Calcium Channels
  • Dystrophin
  • Inositol 1,4,5-Trisphosphate Receptors
  • RNA, Messenger
  • Receptors, Cytoplasmic and Nuclear
  • Ryanodine Receptor Calcium Release Channel
  • Inositol 1,4,5-Trisphosphate
  • Pertussis Toxin
  • GTP-Binding Proteins
  • GTP-Binding Protein alpha Subunits, Gi-Go
  • Potassium
  • Calcium