Force generated by myosin cross-bridges is reduced in myofibrils exposed to ROS/RNS

Am J Physiol Cell Physiol. 2019 Dec 1;317(6):C1304-C1312. doi: 10.1152/ajpcell.00272.2019. Epub 2019 Sep 25.

Abstract

Skeletal muscle weakness is associated with oxidative stress and oxidative posttranslational modifications on contractile proteins. There is indirect evidence that reactive oxygen/nitrogen species (ROS/RNS) affect skeletal muscle myofibrillar function, although the details of the acute effects of ROS/RNS on myosin-actin interactions are not known. In this study, we examined the effects of peroxynitrite (ONOO-) on the contractile properties of individual skeletal muscle myofibrils by monitoring myofibril-induced displacements of an atomic force cantilever upon activation and relaxation. The isometric force decreased by ~50% in myofibrils treated with the ONOO- donor (SIN-1) or directly with ONOO-, which was independent of the cross-bridge abundancy condition (i.e., rigor or relaxing condition) during SIN-1 or ONOO- treatment. The force decrease was attributed to an increase in the cross-bridge detachment rate (gapp) in combination with a conservation of the force redevelopment rate (kTr) and hence, an increase in the population of cross-bridges transitioning from force-generating to non-force-generating cross-bridges during steady-state. Taken together, the results of this study provide important information on how ROS/RNS affect myofibrillar force production which may be of importance for conditions where increased oxidative stress is part of the pathophysiology.

Keywords: cross-bridges; myofibrils; oxidative stress; peroxynitrite; skeletal muscle.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / antagonists & inhibitors
  • Actins / chemistry
  • Actins / physiology
  • Animals
  • Isometric Contraction / drug effects*
  • Isometric Contraction / physiology
  • Molsidomine / analogs & derivatives*
  • Molsidomine / chemistry
  • Molsidomine / pharmacology
  • Myofibrils / drug effects*
  • Myofibrils / physiology
  • Myofibrils / ultrastructure
  • Myosins / antagonists & inhibitors*
  • Myosins / chemistry
  • Myosins / physiology
  • Nitric Oxide Donors / chemistry
  • Nitric Oxide Donors / pharmacology*
  • Oxidants / pharmacology*
  • Oxidative Stress
  • Peroxynitrous Acid / pharmacology*
  • Psoas Muscles / drug effects
  • Psoas Muscles / physiology
  • Psoas Muscles / ultrastructure
  • Rabbits
  • Tissue Culture Techniques

Substances

  • Actins
  • Nitric Oxide Donors
  • Oxidants
  • Peroxynitrous Acid
  • linsidomine
  • Molsidomine
  • Myosins