Thermal stress and Ca-independent contractile activation in mammalian skeletal muscle fibers at high temperatures

Abstract

Temperature dependence of the isometric tension was examined in chemically skinned, glycerinated, rabbit Psoas, muscle fibers immersed in relaxing solution (pH approximately 7.1 at 20 degrees C, pCa approximately 8, ionic strength 200 mM); the average rate of heating/cooling was 0.5-1 degree C/s. The resting tension increased reversibly with temperature (5-42 degrees C); the tension increase was slight in warming to approximately 25 degrees C (a linear thermal contraction, -alpha, of approximately 0.1%/degree C) but became more pronounced above approximately 30 degrees C (similar behavior was seen in intact rat muscle fibers). The extra tension rise at the high temperatures was depressed in acidic pH and in the presence of 10 mM inorganic phosphate; it was absent in rigor fibers in which the tension decreased with heating (a linear thermal expansion, alpha, of approximately 4 x 10(-5)/degree C). Below approximately 20 degrees C, the tension response after a approximately 1% length increase (complete < 0.5 ms) consisted of a fast decay (approximately 150.s-1 at 20 degrees C) and a slow decay (approximately 10.s-1) of tension. The rate of fast decay increased with temperature (Q10 approximately 2.4); at 35-40 degrees C, it was approximately 800.s-1, and it was followed by a delayed tension rise (stretch-activation) at 30-40.s-1. The linear rise of passive tension in warming to approximately 25 degrees C may be due to increase of thermal stress in titin (connectin)-myosin composite filament, whereas the extra tension above approximately 30 degrees C may arise from cycling cross-bridges; based on previous findings from regulated actomyosin in solution (Fuchs, 1975), it is suggested that heating reversibly inactivates the troponin-tropomyosin control mechanism and leads to Ca-independent thin filament activation at high temperatures. Additionally, we propose that the heating-induced increase of endo-sarcomeric stress within titin-myosin composite filament makes the cross-bridge mechanism stretch-sensitive at high temperatures.

A molecular map of titin/connectin elasticity reveals two different mechanisms acting in series

“…The tandem Ig regions are therefore expected to counteract external force only once the domain chain is fully extended. This point is reached at about 3 pm sarcomere length in M. psoas and is near the upper limit of the physiological working range of the sarcomere [14,15]. Above this sarcomere length, there is no further significant extension of the tandem Ig region (Fig.…”

“…At small sarcomere lengths up to 2.8 urn, the movement of the MGl epitope to the Z-disk dominates sarcomere extension. The passive tension is low in this region [14,15]. The extension of the tandem Ig region was approximately linear along sarcomeric length ranges of up to 262.8 km, where resting tension is low [14,15].…”

“…The passive tension is low in this region [14,15]. The extension of the tandem Ig region was approximately linear along sarcomeric length ranges of up to 262.8 km, where resting tension is low [14,15]. The tandem Ig regions can therefore be extended to a linear arrangement with a relatively low energy cost.…”

“…2a,b). Above 2.6 pm, there is an exponential increase in resting tension in M. psoas [14,15]. Whereas the extension of the tandem Ig region levels off at higher sarcomere lengths (Fig.…”

“…Psoas muscle was excised from freshly killed rabbits on ice, single fibres dissected, stretched in relaxing solution [14,15] and fixed with 4% paraformaldehyde.…”