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CELLULAR |
1 Muscle Contraction Group, Department of Physiology, School of Medical Sciences, University of Bristol, Bristol BS8 1TD, UK
Lengthening of active muscle is an essential feature of animal locomotion, but the molecular processes occurring are incompletely understood. We therefore examined and modelled tension responses to ramp stretches (5% fibre length, L0) over a wide range of velocities (0.1–10 L0 s–1) of tetanized intact rat muscle fibre bundles (L0
2 mm) with a resting sarcomere length of 2.5 µm at 20°C. Tension rose to a peak during stretch and decayed afterwards to a level which was higher than the prestretch tetanic tension. This residual force enhancement was insensitive to velocity. The tension rise during stretch showed an early transition (often appearing as an inflection) at 1 ms. Both the stretch (L1) and the tension rise at this transition increased in proportion to velocity. A second transition, marked by a reduction in slope, occurred at a stretch of 18 nm per half-sarcomere; the rise in tension at this transition increased with velocity towards a plateau. Based on analyses of the velocity dependence of the tension and modelling, we propose that the initial steep increase in tension arises from increasing strain of all attached crossbridges and that the first transition reflects the tension loss due to the original post-stroke heads executing a reverse power stroke. Modelling indicates that the reduction in slope at the second transition occurs when the last of the heads that were attached at the start of the ramp become detached. Thereafter, the crossbridge cycle is largely truncated, with prepower stroke crossbridges rapidly detaching at high strain and attaching at low strain, the tension being borne mainly by the prestroke heads. Analysis of the tension decay after the ramp and the velocity dependence of the peak tension suggest that a non-crossbridge component increasingly develops tension throughout the stretch; this decays only slowly, reaching at 500 ms after the ramp 20% of its peak value. This is supported by the finding that, in the presence of 10 µM
N-benzyl-p-toluene sulphonamide (a myosin inhibitor), while isometric tension is reduced to 15%, and the crossbridge contribution to stretch-induced tension rise is reduced to 30–40%, the peak non-crossbridge contribution and the residual force enhancement remain high. We propose that the residual force enhancement is due to changes upon activation in parallel elastic elements, specifically that titin stiffens and C-protein–actin interactions may be recruited.
(Received 25 November 2005;
accepted after revision 14 April 2006;
first published online 20 April 2006)
Corresponding author K. W. Ranatunga: Muscle Contraction Group, Department of Physiology, School of Medical Sciences, University of Bristol, Bristol BS8 1TD, UK Email: k.w.ranatunga{at}bristol.ac.uk
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