The mechanism of the resistance to stretch of isometrically contracting single muscle fibres

Abstract

Rapid attachment to actin of the detached motor domain of myosin dimers with one motor domain already attached has been hypothesized to explain the stretch-induced changes in X-ray interference and stiffness of active muscle. Here, using half-sarcomere mechanics in single frog muscle fibres (2.15 μm sarcomere length and 4• C), we show that: (1) an increase in stiffness of the half-sarcomere under stretch is specific to isometric contraction and does not occur in rigor, indicating that the mechanism of stiffness increase is an increase in the number of attached motors; (2) 2 ms after 100 μs stretches (amplitude 2-8 nm per half-sarcomere) imposed during an isometric tetanus, the stiffness of the array of myosin motors in each half-sarcomere (e m ) increases above the isometric value (e m0 ); (3) e m has a sigmoidal dependence on the distortion of the motor domains ( z) attached in isometric contraction, with a maximum ∼2 e m0 for a distortion of ∼6 nm; e m is influenced by detachment of motors at z > 6 nm; (4) at the end of the 100 μs stretch the relation between e m /e m0 and z lies slightly but not significantly above that at 2 ms. These results support the idea that stretch-induced sliding of the actin filament distorts the actin-attached motor domain of the myosin dimers away from the centre of the sarcomere, providing the steric conditions for rapid attachment of the second motor domain. The rate of new motor attachment must be as high as 7.5 × 10 4 s −1 and explains the rapid and efficient increase of the resistance of active muscle to stretch. Abbreviations hs, half-sarcomere; T 0 , isometric tetanic force; e, half-sarcomere stiffness; e 0 , half-sarcomere stiffness at T 0 ; C f , myofilament compliance; e m , motor array stiffness; e m0 , motor array stiffness at T 0 ; z, distortion of the myosin motor; M3, third order of the myosin-based meridional reflections; I M3 , intensity of M3; R M3 , ratio of the intensities of the higher and lower angle peaks of M3.

Effects of blebbistatin and Ca2+ concentration on force produced during stretch of skeletal muscle fibers

“…22), increasing P c more significantly than what is observed at low Ca 2ϩ concentrations. The force produced during stretch after blebbistatin treatment increases such that it virtually overlaps with the force produced before blebbistatin.…”

Human muscle fascicle behavior in agonist and antagonist isometric contractions

“…48 In conclusion, for an identical level of EMG activity, the in vivo behavior of GM and TA muscle assessed via its architecture was different during either isometric agonist or antagonist contractions. As suggested by the interplay between stretching of the series elastic component (SEC) and the isometric contraction at the molecular level, 49 our findings further highlight the complexity of the isometric contraction. At the fascicle level, we have found that the tension produced during this mode of contraction is not strictly achieved isometrically, whether the muscle behaves as an agonist or an antagonist.…”

The mechanisms of the residual force enhancement after stretch of skeletal muscle: non-uniformity in half-sarcomeres and stiffness of titin

“…Some authors suggest that the increase in force is caused by an increased mean force produced by the cross-bridges [50,51] and a redistribution of cross-bridges between pre-powerstroke and post-powerstroke states [19,22,23,26,52]. Others suggest the increase in force is caused by an increase in the number of cross-bridges attached to actin [49,53], which may include the involvement of a second, adjacent cross-bridge that shares the same myosin neck fragment. Regardless of the actual mechanism, the increase in stiffness vanishes quickly after stretch, to levels between 0 and 7 per cent (between 10 and 300 ms after the stretch) [19,49], which weakens the possibility that cross-bridges contribute to the residual force enhancement.…”