Temperature Effects on Force and Actin–Myosin Interaction in Muscle: A Look Back on Some Experimental Findings

Abstract

Observations made in temperature studies on mammalian muscle during force development, shortening, and lengthening, are re-examined. The isometric force in active muscle goes up substantially on warming from less than 10 °C to temperatures closer to physiological (>30 °C), and the sigmoidal temperature dependence of this force has a half-maximum at ~10 °C. During steady shortening, when force is decreased to a steady level, the sigmoidal curve is more pronounced and shifted to higher temperatures, whereas, in lengthening muscle, the curve is shifted to lower temperatures, and there is a less marked increase with temperature. Even with a small rapid temperature-jump (T-jump), force in active muscle rises in a definitive way. The rate of tension rise is slower with adenosine diphosphate (ADP) and faster with increased phosphate. Analysis showed that a T-jump enhances an early, pre-phosphate release step in the acto-myosin (crossbridge) ATPase cycle, thus inducing a force-rise. The sigmoidal dependence of steady force on temperature is due to this endothermic nature of crossbridge force generation. During shortening, the force-generating step and the ATPase cycle are accelerated, whereas during lengthening, they are inhibited. The endothermic force generation is seen in different muscle types (fast, slow, and cardiac). The underlying mechanism may involve a structural change in attached myosin heads and/or their attachments on heat absorption.

A myosin II-based nanomachine devised for the study of Ca2+-dependent mechanisms of muscle regulation

“…As shown in Fig. 3b and c and in Table 1, the relations and the underlying mechanical and energetic parameters predicted by the model for the half-sarcomere of the mammalian muscle agree with those derived from published data [16,19]. Notably, φ0 calculated by the flux through step 1 at F0, is 11.6 s -1 .…”

“…3a) is used first to fit the functional features of the fast mammalian skeletal muscle and then scaled down to the dimension of the synthetic machine powered by eight HMM fragments from the rabbit psoas myosin. The bulk of mechanical and energetic data present in the literature of mammalian muscle [16,19] are taken into account to constrain the rate functions of state transitions ( Supplementary Fig. 1) at the temperature (24 °C) of the nanomachine experiments.…”

“…The kinetics of state transitions is firstly constrained to fit the mechanics and energetics of the skeletal muscle. In the absence of a direct estimate of the mechanical parameters of the intact fast rabbit muscle, the muscle of reference that provides adequate mechanical and energetic information to be used as constraints for interfacing with in vitro results is the extensor digitorum longus (EDL) from the rat ( [16] and references therein). This may imply a 10% overestimation of the kinetic parameters used in the simulation of rabbit muscle, due the smaller size of the rat, on the basis the size effect on ortholog myosin isoforms [17]; however, for reason of simplicity we did not apply any correction in adapting the rat muscle parameters for the rabbit myosin nanomachine.…”

“…The mechanical constraints from the whole muscle experiments at the temperature of the nanomachine experiments (24°C) are: (i) isometric tetanic force F0 250 kPa, (ii) unloaded shortening velocity V0 8.6 m s -1 per half-sarcomere, (iii) F-V relation as in Fig. 3b, in which the data from [16] and references therein are fitted with Hill hyperbolic equation (dashed line), which gives a value of a/F0 (the parameter that estimates the curvature of the relation) of 0.36. The density of force per cross-sectional area can be translated to force per half thick filament (htf) taking into account the thick filament density (5.8.10 14 m -2 , [18] and references therein) and corresponds to 460 pN per htf (see abscissa intercept of the dashed line in Fig.…”

“…The parameters reported in the Table are defined below and are accompanied by the references that provide the standard values used to constraint the simulation at the level of the muscle half-sarcomere. N, number of available motors, which, per half-thick filament, are (49 crowns x 6 motors per crown =) 294 [29]; F0, isometric force referred to the half-thick filament [16]; r0, isometric duty ratio [32]; φ0, flux through step 1 of the cycle in Fig. 3a in isometric condition, corresponding to the ATP hydrolysis rate per myosin head at F0 [19] and references therein; V0, maximum shortening velocity [16]; Pmax, maximum power; φPmax, ATP hydrolysis rate per myosin head at Pmax [19,33].…”