Chemo‐mechanical energy transduction in relation to myosin isoform composition in skeletal muscle fibres of the rat

Abstract

ATP consumption and force development were determined in single skinned muscle fibres of the rat at 12 °C. Myofibrillar ATPase consumption was measured photometrically from NADH oxidation which was coupled to ATP hydrolysis. Myosin heavy chain (MHC) and light chain (MLC) isoforms were identified by gel electrophoresis. Slow fibres (n= 14) containing MHCI and fast fibres (n= 18) containing MHCIIB were compared. Maximum shortening velocity was 1.02 ± 0.63 and 3.05 ± 0.23 lengths s−1, maximum power was 1.47 ± 0.22 and 9.59 ± 0.84 W l−1, and isometric ATPase activity was 0.034 ± 0.003 and 0.25 ± 0.01 mM s−1 in slow and in fast fibres, respectively. In fast as well as in slow fibres ATP consumption during shortening increased above isometric ATP consumption. The increase was much greater in fast fibres than in slow fibres, but became similar when expressed relative to the isometric ATPase rate. Efficiency was calculated from mechanical power and free energy change associated with ATP hydrolysis. Maximum efficiency was larger in slow than in fast fibres (0.38 ± 0.04 versus 0.28 ± 0.03) and was reached at a lower shortening velocity. Within the group of fast fibres efficiency was lower in fibres which contained more MLC3f. We conclude that both MHC and essential MLC isoforms contribute to determine efficiency of chemo‐mechanical transduction.

High mechanical efficiency of the cross-bridge powerstroke in skeletal muscle

“…4). This may be consistent with the result that a roughly proportional relationship exists between the rate of ATP utilization and the fibre shortening velocity (Reggiani et al, 1997;He et al, 2000;Potma and Stienen, 1996), but not with the biphasic relationship between the rate of energy liberation (heat + work) and the shortening velocity in whole muscle (Hill, 1964;Linari and Woledge, 1995). The approximately linear dependence of the amount of ATP utilized for work production on the distance of shortening (Fig.…”

“…The maximum mechanical efficiency of Ca 2+ -activated skeletal muscle fibres has been reported to range from 0.2 to 0.46 (He et al, 1997;Reggiani et al, 1997;Sun et al, 2001), indicating that the net maximum mechanical efficiency of cross-bridges during their asynchronous activity is much smaller than the maximum mechanical efficiency of individual cross-bridges obtained in the present study. In this connection, it is of interest that, in demembranated cardiac myocytes, the maximum Ca 2+ -activated isometric force increases by one third when the ATP concentration is reduced to 200 µmol l -1 (Fabiato and Fabiato, 1975).…”

Myofibrillar myosin ATPase activity in hindlimb muscles from young and aged rats

“…These discrepancies are likely due to the various species, strains, muscles, ages, and techniques to quantitate MHC isoforms that were utilized in the studies. Shortening velocity is influenced by the essential MLC as well, presumably by altering ATPase hydrolysis (Reggiani et al, 1997). Only small age-related isoform shifts in MLC proteins occurred in the myofibril samples.…”

First and second law work production efficiency of a muscle cell

“…Widen and Barclay (2006) suggested that the enthalpy output by the mouse papillary muscle was partitioned into force-dependent, and force independent fractions, pointing the importance of the unavoidable additional metabolic energy expense, accompanying the muscle work. The procedure described in this paper is different than that of Reggiani et al (1997), who based their calculations on the free energy change of the ATP hydrolysis, and experimentally determined mechanical work performance.…”

“…Numerous experimental and analytical studies are performed to determine the heat released and work produced via muscle contractions since the pioneer work of Hill (Reggiani et al 1997;Holmes, 2006). Energy (either enthalpy or free energy), which is released upon ATP hydrolysis depends on cellular conditions (Alberty 1969;Woledge and Reilly 1988).…”