Triadin binding to the C-terminal luminal loop of the ryanodine receptor is important for skeletal muscle excitation contraction coupling

J Gen Physiol. 2007 Oct;130(4):365-78. doi: 10.1085/jgp.200709790. Epub 2007 Sep 10.

Abstract

Ca(2+) release from intracellular stores is controlled by complex interactions between multiple proteins. Triadin is a transmembrane glycoprotein of the junctional sarcoplasmic reticulum of striated muscle that interacts with both calsequestrin and the type 1 ryanodine receptor (RyR1) to communicate changes in luminal Ca(2+) to the release machinery. However, the potential impact of the triadin association with RyR1 in skeletal muscle excitation-contraction coupling remains elusive. Here we show that triadin binding to RyR1 is critically important for rapid Ca(2+) release during excitation-contraction coupling. To assess the functional impact of the triadin-RyR1 interaction, we expressed RyR1 mutants in which one or more of three negatively charged residues (D4878, D4907, and E4908) in the terminal RyR1 intraluminal loop were mutated to alanines in RyR1-null (dyspedic) myotubes. Coimmunoprecipitation revealed that triadin, but not junctin, binding to RyR1 was abolished in the triple (D4878A/D4907A/E4908A) mutant and one of the double (D4907A/E4908A) mutants, partially reduced in the D4878A/D4907A double mutant, but not affected by either individual (D4878A, D4907A, E4908A) mutations or the D4878A/E4908A double mutation. Functional studies revealed that the rate of voltage- and ligand-gated SR Ca(2+) release were reduced in proportion to the degree of interruption in triadin binding. Ryanodine binding, single channel recording, and calcium release experiments conducted on WT and triple mutant channels in the absence of triadin demonstrated that the luminal loop mutations do not directly alter RyR1 function. These findings demonstrate that junctin and triadin bind to different sites on RyR1 and that triadin plays an important role in ensuring rapid Ca(2+) release during excitation-contraction coupling in skeletal muscle.

Publication types

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

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Binding Sites
  • Calcium Channels / metabolism
  • Calcium Channels, L-Type
  • Calcium Signaling*
  • Calcium-Binding Proteins / chemistry
  • Calcium-Binding Proteins / metabolism
  • Calsequestrin / metabolism
  • Carrier Proteins / chemistry*
  • Carrier Proteins / metabolism*
  • Cell Line, Transformed
  • Cells, Cultured
  • Electrophysiology
  • Kinetics
  • Membrane Proteins / chemistry
  • Membrane Proteins / metabolism
  • Mice
  • Mixed Function Oxygenases / chemistry
  • Mixed Function Oxygenases / metabolism
  • Models, Biological
  • Muscle Contraction / physiology*
  • Muscle Fibers, Skeletal / metabolism
  • Muscle Proteins / chemistry*
  • Muscle Proteins / metabolism*
  • Protein Binding
  • Protein Interaction Mapping
  • Rabbits
  • Ryanodine Receptor Calcium Release Channel / chemistry*
  • Ryanodine Receptor Calcium Release Channel / metabolism*
  • Sarcoplasmic Reticulum / metabolism

Substances

  • Calcium Channels
  • Calcium Channels, L-Type
  • Calcium-Binding Proteins
  • Calsequestrin
  • Carrier Proteins
  • Membrane Proteins
  • Muscle Proteins
  • Ryanodine Receptor Calcium Release Channel
  • triadin
  • Asph protein, mouse
  • Mixed Function Oxygenases