Changes in intracellular Ca2+ induced by shortening imposed during tetanic contractions.

Abstract

Calcium transients, monitored by aequorin, and force were recorded simultaneously during tetanic contractions of isolated frog skeletal muscle fibers. Quick length changes were applied to the fibers during contractions at sarcomere lengths on the descending limb of the length-tension relationship. Previous experiments showed that regulatory Ca2+ binding sites are apparently saturated during a plateau of tetanic force development at these sarcomere lengths. However, quick releases of greater than 4 to 5% of fiber length produced a momentary fall in the calcium transient that followed a time course similar to the redevelopment of force. The fall in the Ca2+ transient after a release was maximum at striation spacings about half way along the descending limb (2.6-2.7 microns), which suggests it is not related to an increase in the number of Ca2+ binding sites distributed uniformly along the filaments. The effect was absent or barely detectable when highly stretched fibers were released during contraction. The fall in the Ca2+ transient was unrelated to the time during a tetanus that a release was made or to the velocity of the release. One explanation of these results is that complexes between actin and myosin are broken by a sudden reduction of length, and as they reform during the recovery of force the affinity of troponin for Ca2+ increases. Quick stretch had no effect on the rapid decay of Ca2+ transients, but stretch increased peak force and slowed relaxation for almost a second after the end of stimulation. Evidently the decrease in the rate of relaxation produced by stretch is unrelated to changes in the amount of Ca2+ released or the rate of Ca2+ removal, which supports suggestions that the kinetics of muscle relaxation are determined by more than one mechanism. The apparent increase in the overall duration of mechanical activity after stretch probably results from the longitudinal inhomogeneity in the duration of activity - known to occur during relaxation - coupled with the decreased compliance of stretched fibers.