Multiple sources of passive stress relaxation in muscle fibres.
The forces developed during stretch of nonactivated muscle consist of velocity-sensitive (viscous/viscoelastic) and velocity-insensitive (elastic) components. At the myofibrillar level, the elastic-force component has been described in terms of the entropic-spring properties of the giant protein titin, but entropic elasticity cannot account for viscoelastic properties, such as stress relaxation. Here we examine the contribution of titin to passive stress relaxation of isolated rat-cardiac myofibrils depleted of actin by gelsolin treatment. Monte Carlo simulations show that, up to approximately 5 s after a stretch, the time course of stress relaxation can be described assuming unfolding of 1-2 immunoglobulin domains per titin molecule. For extended periods of stress relaxation, the simulations failed to correctly describe the myofibril data, suggesting that in situ, titin-Ig domains may be more stable than predicted in earlier single-molecule atomic-force-microscopy studies. The reasons behind this finding remain unknown; simply assuming a reduced unfolding probability of domains--an effect found here by AFM force spectroscopy on titin-Ig domains in the presence of a chaperone, alpha-B-crystallin--did not help correctly simulate the time course of stress relaxation. We conclude that myofibrillar stress relaxation likely has multiple sources. Evidence is provided that in intact myofibrils, an initial, rapid phase of stress relaxation results from viscous resistance due to the presence of actin filaments.