The structural basis of the increase in isometric force production with temperature in frog skeletal muscle

J Physiol. 2005 Sep 1;567(Pt 2):459-69. doi: 10.1113/jphysiol.2005.089672. Epub 2005 Jun 16.

Abstract

X-ray diffraction patterns were recorded from isolated single fibres of frog skeletal muscle during isometric contraction at temperatures between 0 and 17 degrees C. Isometric force was 43 +/- 2% (mean +/- S.E.M., n = 10) higher at 17 degrees C than 0 degrees C. The intensity of the first actin layer line increased by 57 +/- 18% (n = 5), and the ratio of the intensities of the equatorial 1,1 and 1,0 reflections by 20 +/- 7% (n = 10), signalling radial or azimuthal motions of the myosin head domains. The M3 X-ray reflection from the axial repeat of the heads along the filaments was 27 +/- 4% more intense at 17 degrees C, suggesting that the heads became more perpendicular to the filaments. The ratio of the intensities of the higher and lower angle peaks of the M3 reflection (R(M3)) was 0.93 +/- 0.02 (n = 5) at 0 degrees C and 0.77 +/- 0.02 at 17 degrees C. These peaks are due to interference between the two halves of each myosin filament, and the R(M3) decrease shows that heads move towards the midpoint of the myosin filament at the higher temperature. Calculations based on a crystallographic model of the heads indicated that the observed R(M3) change corresponds to tilting of their light-chain domains by 9 deg, producing an axial displacement of 1.4 nm, which is equal to that required to strain the actin and myosin filaments under the increased force. We conclude that the higher force generated by skeletal muscle at higher temperature can be accounted for by axial tilting of the myosin heads.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / chemistry
  • Actins / physiology*
  • Actins / ultrastructure*
  • Animals
  • Cells, Cultured
  • Isometric Contraction / physiology*
  • Models, Biological
  • Models, Chemical
  • Models, Molecular
  • Molecular Motor Proteins / chemistry
  • Molecular Motor Proteins / physiology
  • Muscle Fibers, Skeletal / physiology
  • Muscle Fibers, Skeletal / ultrastructure
  • Muscle, Skeletal / chemistry
  • Muscle, Skeletal / physiology*
  • Muscle, Skeletal / ultrastructure*
  • Myosins / chemistry
  • Myosins / physiology*
  • Myosins / ultrastructure*
  • Rana temporaria
  • Sarcomeres / chemistry
  • Sarcomeres / physiology
  • Sarcomeres / ultrastructure
  • Stress, Mechanical
  • Structure-Activity Relationship
  • Temperature*

Substances

  • Actins
  • Molecular Motor Proteins
  • Myosins

Grants and funding