Elastic Properties of Isolated Thick Filaments Measured by Nanofabricated Cantilevers

Abstract

Using newly developed nanofabricated cantilever force transducers, we have measured the mechanical properties of isolated thick filaments from the anterior byssus retractor muscle of the blue mussel Mytilus edulis and the telson levator muscle of the horseshoe crab Limulus polyphemus. The single thick filament specimen was suspended between the tip of a flexible cantilever and the tip of a stiff reference beam. Axial stress was placed on the filament, which bent the flexible cantilever. Cantilever tips were microscopically imaged onto a photodiode array to extract tip positions, which could be converted into force by using the cantilever stiffness value. Length changes up to 23% initial length (Mytilus) and 66% initial length (Limulus) were fully reversible and took place within the physiological force range. When stretch exceeded two to three times initial length (Mytilus) or five to six times initial length (Limulus), at forces approximately 18 nN and approximately 7 nN, respectively, the filaments broke. Appreciable and reversible strain within the physiological force range implies that thick-filament length changes could play a significant physiological role, at least in invertebrate muscles.

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

“…The filament compliance accounts for approximately 50 per cent of the sarcomeres compliance (Huxley et al 1994;Wakabayashi et al 1994), but their contribution to the total strain-force relationship is unknown, and certainly small. When isolated thick and thin filaments are stretched from zero tension to maximal physiological tensions, strains of 0.3 and 1.5 per cent are observed, respectively ( Neumann et al 1998;Liu & Pollack 2002), a value that is too small to explain the changes observed in this study. Even if one assumes that the compliance would affect the results and explain part of the stretch forces, BDM does not probably affect the compliance of the filaments, and therefore the comparisons made between the two situations are still valid.…”

Invertebrate muscles: Thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle

“…In many muscles it may thus suffice simply to have enough thin filaments that the thick filament heads can generally find a thin filament to bind to without the thin and thick filaments being arranged in some 'ideal' fashion with respect to their respective helix repeats. This conclusion is supported by work showing that physiologically relevant forces applied to thick filaments can lengthen them 23% in Mytilus and 66% in Limulus (Neumann et al, 1998). These length changes are presumably great enough, unless compensated for by matching changes in thin filament length, to alter thin:thick filament helix staggers.…”

A macroscopic ansatz to deduce the Hill relation

“…It maps compliant structures within the muscle fibres (Hill, 1938(Hill, , 1950Katz, 1939;Krueger and Pollack, 1975;Kishino and Yanagida, 1988;Levin and Wyman, 1927;Lindstedt et al, 2002;Maruyama et al, 1977;Neumann et al, 1998;Pandy et al, 1990;Wakabayashi et al, 1994;Zajac, 1989). A recent approach (Denoth et al, 2002;Telley and Denoth, 2007), modelling the muscle as an inhomogeneous chain of many force generators coupled visco-elastically to each other both in parallel and in series, incorporates series elasticity as a key feature.…”

“…1994; Kishino and Yanagida, 1988;Wakabayashi et al, 1994), myosin (Huxley et al, 1994;Neumann et al, 1998;Wakabayashi et al, 1994), crossbridge (Ford et al, 1981;Goldman and Huxley, 1994;Huxley and Tideswell, 1996), and titin (Maruyama et al, 1977) the SE is not just a force transmitter but also an integral catalytic converter generating the macroscopic energy drain PDE by mechanically feeding back any crossbridge work stroke to other crossbridges. As a consequence, our model backs the view that the mechanics of concentric contractions and the origin of maintenance heat rate are indeed due to the same process (Huxley, 1957).…”