HOP Skip and Jump; but How?

Abstract

Apart from fast, efficient and coordinated contraction of several skeletal muscles, running and jumping require effective absorption of the kinetic energy of the body during the landing phase, to absorb impact forces and prevent injury. This is done not only by joints, bones and tendons, but also by activated muscles which resist stretch. During lengthening, skeletal muscle bears higher force and has higher instantaneous stiffness than during isometric contraction, and yet consumes very little ATP. These properties allow muscle to absorb the energy of a fall or landing by stretching. Our work shows how the actomyosin molecules change their structure and interaction to implement these physiologically useful mechanical and thermodynamical properties. The low angle x-ray diffraction pattern of rabbit skeletal muscle fibers was monitored during isometric contraction and compared to that during ramp stretch. The experiments were carried out at physiological temperature, using low-angle X-ray synchrotron radiation at ID2, ESRF, Grenoble. The intensities of the off-meridional layer lines and fine interference structure of the meridional M3 myosin X-ray reflection were resolved. Mechanical and structural data show that upon stretch the fraction of actin-bound myosin heads is higher than during isometric contraction. This finding accounts for the higher stiffness and greater energy absorbing capacity of stretched muscle compared to isometric. However the intensities of the actin layer lines are lower than during isometric contraction. These results suggest that during stretch, a significant fraction of actin-bound heads is bound weakly or non-stereo-specifically. That is, the actin-bound myosin heads are disordered azimuthally but are stiff axially. As the strong or stereo-specific myosin binding to actin is necessary for actin activation of the myosin ATPase, this finding explains the low metabolic cost of energy absorption by muscle during the landing phase of locomotion.