Why Muscle is an Efficient Shock Absorber

Abstract

Skeletal muscles power body movement by converting free energy of ATP hydrolysis into mechanical work. During the landing phase of running or jumping some activated skeletal muscles are subjected to stretch. Upon stretch they absorb body energy quickly and effectively thus protecting joints and bones from impact damage. This is achieved because during lengthening, skeletal muscle bears higher force and has higher instantaneous stiffness than during isometric contraction, and yet consumes very little ATP. We wish to understand how the actomyosin molecules change their structure and interaction to implement these physiologically useful mechanical and thermodynamical properties. We monitored changes in the low angle x-ray diffraction pattern of rabbit skeletal muscle fibers during ramp stretch compared to those during isometric contraction at physiological temperature using synchrotron radiation. 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. On the other hand, the intensities of the actin layer lines are lower than during isometric contraction. Taken together, these results suggest that during stretch, a significant fraction of actin-bound heads is bound non-stereo-specifically, i.e. they are disordered azimuthally although 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.

The lifetime of the actomyosin complex in vitro under load corresponding to stretch of contracting muscle

“…These de novo attached heads are possibly partners of the 'already attached' heads of the same molecules ). It has also been shown that during stretch a majority of actin-bound myosin heads are attached non-stereospecifically or weakly (Ferenczi et al 2014). The rate of forced detachment of myosin heads during fast stretch of muscle fibers was shown to increase with the stretching force (Colombini et al 2007), in agreement with Bell's theory (Bell 1978).…”

“…In muscle, such force corresponds to the stretch of contracting muscle or eccentric contraction, which is widely experienced in sport exercises. The eccentric contraction is characterized by the increased number of actin-bound myosin heads, possibly because of enhanced binding of the second partner head of a myosin molecule Ferenczi et al 2014). During stretch, muscle cross-bridges consume very little ATP (Bickham et al 2011), and the mode of the actinmyosin binding becomes non-stereospecific (Ferenczi et al 2014).…”

“…The eccentric contraction is characterized by the increased number of actin-bound myosin heads, possibly because of enhanced binding of the second partner head of a myosin molecule Ferenczi et al 2014). During stretch, muscle cross-bridges consume very little ATP (Bickham et al 2011), and the mode of the actinmyosin binding becomes non-stereospecific (Ferenczi et al 2014). Soon after stretch, the ATPase rate has been shown to return to a high level (Bickham et al 2011).…”

“…Specific properties of skeletal muscle subjected to stretch such as high stiffness (Lombardi and Piazzesi 1990), low ATP consumption (Bickham et al 2011), and efficient energy absorption (Linari et al 2003) are important for energy conservation and effective protection of bones and joints of animals from impact damage during the landing phase of running and jumping (Ferenczi et al 2014). The mechanism of functioning of myosin cross-bridges under load that exceeds the isometric level is unresolved.…”

“…The mechanism of functioning of myosin cross-bridges under load that exceeds the isometric level is unresolved. For example, time-resolved X-ray experiments with muscle fibers have shown that stretch promotes binding to actin of additional myosin heads, which were detached during isometric contraction Ferenczi et al 2014). These de novo attached heads are possibly partners of the 'already attached' heads of the same molecules ).…”