Functional interactions between cytoplasmic domains of the skeletal muscle Ca2+ release channel

J Biol Chem. 1997 Oct 3;272(40):25051-61. doi: 10.1074/jbc.272.40.25051.

Abstract

The skeletal muscle Ca2+ release channel (RYR1), which plays a critical role in excitation-contraction coupling, is a homotetramer with a subunit molecular mass of 565 kDa. Oxidation of the channel increases its activity and produces intersubunit cross-links within the RYR1 tetramer (Aghdasi, B., Zhang, J., Wu, Y., Reid, M. B., and Hamilton, S. L. (1997) J. Biol. Chem. 272, 3739-3748). Alkylation of hyperreactive sulfhydryls on RYR1 with N-ethylmaleimide (NEM) inhibits channel function and blocks the intersubunit cross-linking. We used calpain and tryptic cleavage, two-dimensional SDS-polyacrylamide gel electrophoresis, N-terminal sequencing, sequence-specific antibody Western blotting, and [14C]NEM labeling to identify the domains involved in these effects. Our data are consistent with a model in which 1) diamide, an oxidizing agent, simultaneously produces an intermolecular cross-link between adjacent subunits within the RYR1 tetramer and an intramolecular cross-link within a single subunit; 2) all of the cysteines involved in both cross-links are in either the region between amino acids approximately 2100 and 2843 or the region between amino acids 2844 and 4685; 3) oxidation exposes a new calpain cleavage site in the central domain of the RYR1 (in the region around amino acid 2100); 4) sulfhydryls that react most rapidly with NEM are located in the N-terminal domain (between amino acids 426 and 1396); 5) alkylation of the N-terminal cysteines completely inhibits the formation of both inter- and intrasubunit cross-links. In summary, we present evidence for interactions between the N-terminal region and the putatively cytoplasmic central domains of RYR1 that appear to influence subunit-subunit interactions and channel activity.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels / chemistry*
  • Calcium Channels / isolation & purification
  • Calcium Channels / metabolism*
  • Calpain / metabolism
  • Cross-Linking Reagents
  • Diamide
  • Ethylmaleimide / metabolism
  • Ethylmaleimide / pharmacology
  • Intracellular Membranes / metabolism
  • Macromolecular Substances
  • Models, Structural
  • Molecular Weight
  • Muscle Proteins / chemistry*
  • Muscle Proteins / isolation & purification
  • Muscle Proteins / metabolism*
  • Muscle, Skeletal / metabolism*
  • Peptide Fragments / chemistry
  • Peptide Fragments / isolation & purification
  • Protein Structure, Secondary*
  • Rabbits
  • Ryanodine / metabolism
  • Ryanodine Receptor Calcium Release Channel
  • Sarcoplasmic Reticulum / metabolism

Substances

  • Calcium Channel Blockers
  • Calcium Channels
  • Cross-Linking Reagents
  • Macromolecular Substances
  • Muscle Proteins
  • Peptide Fragments
  • Ryanodine Receptor Calcium Release Channel
  • Diamide
  • Ryanodine
  • Calpain
  • Ethylmaleimide