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Correlations have been made between the mechanical and biochemical descriptions of muscle relaxation. Skinned muscle fibres in the rigor state were incubated in a solution containing P3-1-(2-nitro)phenylethyladenosine-5'-triphosphate, 'caged ATP', an inert photolabile precursor of ATP, and free Ca2+ concentration less than 10(-8) M. The mechanical response of the fibre was monitored during relaxation initiated by liberating ATP with a pulse of 347 nm light from a frequency-doubled ruby laser. Tension first dropped and then rose briefly, before finally declining to the relaxed level. Stiffness, in phase with a sinusoidal length change, declined monotonically after the laser pulse. Out-of-phase stiffness increased briefly after a delay, then returned to the base line during the final relaxation. The development of the out-of-phase stiffness signal was taken as evidence that during the relaxation some cross-bridges were present with properties similar to those in an active contraction. The tension rise and slower phase of relaxation can be explained by a mechanism in which some of the cross-bridges reattach, generate force and finally detach in the absence of Ca2+ ions. In this model cross-bridge attachment is facilitated by protein co-operativity within the myofilaments. Detailed analysis of the mechanical transients makes other possible models for the initial tension rise unlikely. Stretching or releasing fibres prior to photolysis changed the time course of the early parts of the tension transient without significant effect on the later phases or on stiffness. The tension records from stretch, release and isometric trials converged to a final common time course of relaxation. Analysis of the convergence of tension records provided a means for measuring the cross-bridge detachment rate from the thin filament as a function of ATP concentration. The apparent second-order rate constant for detachment was at least 5 X 10(5) M-1 S-1 at 20-22 degrees C. The final relaxation rate was less dependent on ATP concentration than the early convergence. The results indicate that ATP binding and cross-bridge detachment from the nucleotide-free intermediate of the cross-bridge cycle are rapid compared to the cross-bridge cycling rate.
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