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Kinetics of Regeneration of Cross-Bridge Power Stroke in Shortening Muscle

1993; Springer Nature; Linguagem: Inglês

10.1007/978-1-4615-2872-2_61

2214-8019

Gabriella Piazzesi, Marco Linari, Vincenzo Lombardi,

Neuroscience and Neural Engineering

The force developed by a muscle during steady shortening is due to cyclic interactions between the cross-bridges extending from the thick myosin filament to the thin actin filament. Each interaction consists of a power stroke of the myosin molecule that accounts for a limited amount of sliding between the two sets of filaments (about 12 nm according to quick release experiments1)2)), and is widely believed to be coupled to the hydrolysis of one ATP molecule3)4). On the other hand both energetics studies in muscle5) and in vitro motility assays6), indicating that shortening per ATP split is much larger than 12 nm, postulate that during shortening cross-bridges interact at a rate much faster than the ATP splitting rate. In the experiments reported here, made on intact fibres from frog skeletal muscle, the rate of regeneration of the power stroke was determined. Tension transients were elicited by imposing test step releases at different times (2-20 ms) after a conditioning release of about 5 nm. When the test step was imposed at 2 ms after the conditioning step, the tension attained at the end of the quick phase of recovery (T 2, due to the force generating stroke of the attached cross-bridges) was depressed and the T 2 curve (the plot of T 2 tension versus size of the test step) intercepted the length axis to the right, with respect to the intercept of the control T 2 curve, by an amount similar to the size of the conditioning step. By increasing the interval between conditioning and test step the T 2 tension increased progressively and the T 2 curve intercept approached the intercept of the control curve with a time constant of 6–7 ms. These results indicate that the force generating stroke elicited by a shortening step is followed by a relatively rapid process of detachment and reattachment by most of the cross-bridges, allowing for the generation of another power stroke. The rate of this process, 150/s, is one order of magnitude higher than that expected from the ATPase rate, suggesting that several actomyosin interactions occur in shortening muscle by the time one ATP is split. The results are simulated with a mechanical kinetic model of contraction7), in which, for a critical amount of shortening, cross-bridges can detach, rapidly reattach and generate force before the completion of the "normal" isometric cycle.