Nitric oxide protects the skeletal muscle Ca2+ release channel from oxidation induced activation

J Biol Chem. 1997 Oct 10;272(41):25462-7. doi: 10.1074/jbc.272.41.25462.

Abstract

Reactive oxygen intermediates and nitric oxide modulate the contractile function of skeletal muscle fibers, possibly via direct interaction with the Ca2+ release channel. Oxidants produce disulfide bonds between subunits of the Ca2+ release channel tetramer, and this is accompanied by an increase in channel activity. The sulfhydryl alkylating agent N-ethylmaleimide has three distinct effects on Ca2+ release channel activity: first, channel activity is decreased (phase 1); then with continued exposure the activity is dramatically increased (phase 2); and finally, the channel is again inhibited (phase 3) (Aghdasi, B., Zhang, J. Z., Wu, Y., Reid, M. B., and Hamilton, S. L., (1997) J. Biol. Chem. 272, 3739-3749). Both H2O2 and nitric oxide (NO) block the phase 1 inhibitory effect of N-ethylmaleimide. NO donors, at concentrations that have no detectable effect on channel activity, block intersubunit cross-linking and prevent activation of the channel by the disulfide inducing agent, diamide. These findings support a model in which NO modulates the activity of the Ca2+ release channel by preventing oxidation of regulatory sulfhydryls. However, higher concentrations of NO donors activate the channel and produce intersubunit cross-links, supporting a bifunctional effect of NO on channel activity. Low NO concentrations prevent oxidation of the Ca2+ release channel whereas higher concentrations oxidize it.

Publication types

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

MeSH terms

  • Alkylation
  • Animals
  • Ethylmaleimide / metabolism
  • Hydrogen Peroxide / pharmacology
  • Lipid Bilayers / metabolism
  • Muscle Contraction
  • Muscle, Skeletal / metabolism*
  • Nitric Oxide / metabolism*
  • Oxidation-Reduction
  • Protein Conformation
  • Rabbits
  • Reactive Oxygen Species / metabolism
  • Ryanodine Receptor Calcium Release Channel / metabolism*
  • Sulfhydryl Compounds / metabolism

Substances

  • Lipid Bilayers
  • Reactive Oxygen Species
  • Ryanodine Receptor Calcium Release Channel
  • Sulfhydryl Compounds
  • Nitric Oxide
  • Hydrogen Peroxide
  • Ethylmaleimide