The efficiency of contraction in rabbit skeletal muscle fibres, determined from the rate of release of inorganic phosphate

Abstract

The mechanical efficiency of muscle contraction is the ratio of work performed to the chemical energy produced by the hydrolysis of ATP. Chemical energy which is not converted into work or absorbed by the reaction is lost as heat. The efficiency of contraction is zero when no work is produced, either because the muscle does not shorten, i.e. during isometric contractions, or when the force produced by the muscle is zero, as is the case when the muscle is allowed to shorten under zero load. In the latter case, the shortening velocity is the maximum which the muscle can achieve. It is also necessary to consider the internal work which does not translate into macroscopic movement, but which may be relevant to considerations of efficiency. Here we have precisely determined the work resulting from the actomyosin ATPase activity, without interference from the effects of tendon elasticity and of ATP hydrolysis due to activation of the muscle machinery, namely calcium release and re-uptake by the sarcoplasmic reticulum. This was achieved by using segments of permeabilized muscle fibres obtained from the rabbit psoas muscle and initiating contraction by the photolytic release of ATP from the PÅ-1-(2-nitrophenyl)ethyl ester of ATP (NPE-caged ATP; Ferenczi et al. 1984) in the presence of a saturating concentration of calcium (32 ìÒ). The ability of the muscle fibres to perform work was measured by recording the force response during a period of applied constant velocity shortening. The ends of such fibre segments may be damaged at their point of attachment to the apparatus, resulting in local stretching during force development. So we measured the sarcomere length in the segment during contraction and shortening, thus providing a direct measurement of the shortening velocity of the sarcomeres. The other aspect of efficiency calculations is the determination of chemical energy utilized. For this, we used a fluorescence assay which is sensitive to the amount of inorganic phosphate (Pé) released in the muscle fibre by the hydrolysis of ATP (He et al. 1997 1. The relationship between mechanical power output and the rate of ATP hydrolysis was investigated in segments of permeabilized fibres isolated from rabbit psoas muscle. 2. Contractions were elicited at 12°C by photolytic release of ATP from the PÅ-1-(2-nitrophenyl)ethyl ester of ATP (NPE-caged ATP). Inorganic phosphate (Pé) release was measured by a fluorescence method using a coumarin-labelled phosphate binding protein.Force and sarcomere length were also monitored. 3. ATPase activity was determined from the rate of appearance of Pé during each phase of contraction. The ATPase rate was 10·3 s¢ immediately following release of ATP and 5·1 s¢ during the isometric phase prior to the applied shortening. It rose hyperbolically with shortening velocity, reaching 18·5 s¢ at a maximal shortening velocity > 1 ML s¢ (muscle lengths s¢). 4. Sarcomeres shortened at 0·09 ML s¢ immediately following the photolytic release of ATP and at 0·04 ML s¢ prior to the period of applied shorteni...

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