Pre-power stroke cross bridges contribute to force during stretch of skeletal muscle myofibrils

Abstract

When activated skeletal muscle is stretched, force increases in two phases. This study tested the hypothesis that the increase in stretch force during the first phase is produced by pre-power stroke cross bridges. Myofibrils were activated in sarcomere lengths (SLs) between 2.2 and 2.5 mm, and stretched by approximately 5-15 per cent SL. When stretch was performed at 1 mm s K1 SL K1, the transition between the two phases occurred at a critical stretch (SL c ) of 8.4G0.85 nm half-sarcomere (hs)K1 and the force (critical force; F c ) was 1.62G0.24 times the isometric force (nZ23). At stretches performed at a similar velocity (1 mm s K1 SL K1), 2,3-butanedione monoxime (BDM; 1 mM) that biases cross bridges into prepower stroke states decreased the isometric force to 21.45G9.22 per cent, but increased the relative F c to 2.35G0.34 times the isometric force and increased the SL c to 14.6G0.6 nm hs K1 (nZ23), suggesting that pre-power stroke cross bridges are largely responsible for stretch forces.

Force produced by isolated sarcomeres and half-sarcomeres after an imposed stretch

“…The microneedles were produced with a vertical pipette puller (KOPF 720, David Kopf Instruments) and calibrated by a cross-bending method (2, 32), using pairs of microfabricated cantilevers of known stiffness as reference beams. Cantilevers with a stiffness varying between 22 and 348 nN/ m were used in this study, similar to those used previously in our laboratory for force measurements with optimal reproducibility (32,35,36). The final stiffness of the microneedles used during these experiments varied between 180 and 410 nN/ m.…”

“…Myofibrils and sarcomeres from the rabbit psoas muscle were prepared following published procedures (31,32,35,36). Briefly, small sections of the muscles were dissected and tied to small wood sticks.…”

“…The force remains elevated after the stretch to reach a steady-state level that is higher than that produced during isometric contractions at corresponding lengths (8,24,38). The mechanisms responsible for this "residual force enhancement" remain elusive and there is substantial disagreement in the literature.Recent studies with isolated myofibrils, preparations in which individual sarcomeres (22,23,36,37,41,43) and half-sarcomeres in series (44, 45) can be evaluated, have shown intriguing results. Whereas a few studies suggest that force enhancement could be linked to sarcomeres and half-SL nonuniformity, as half-sarcomeres change their length continuously during activation and relaxation (36,44,45), some others show that sarcomeres may be stable (22,37), and that the increase in force after stretch are caused by contractile and/or passive structures.…”

“…Whereas a few studies suggest that force enhancement could be linked to sarcomeres and half-SL nonuniformity, as half-sarcomeres change their length continuously during activation and relaxation (36,44,45), some others show that sarcomeres may be stable (22,37), and that the increase in force after stretch are caused by contractile and/or passive structures. Furthermore, studies that attribute the residual force enhancement to sarcomeric structures present experimental data and interpretations that are highly variable.…”

“…It has been directly associated with several experimental observations, including the force "creep" observed at long muscle lengths (11,16), the relation between force and filament overlap (11,17,19), the kinetics of force development and relaxation (9,43), and the effects of muscle stretch in force production (7,8,13,18,36,37). The latest is particularly important: when a stretch is applied to skeletal muscles during activation, force increases significantly while the energy consumption decreases (1,30).…”