Transient tension changes initiated by laser temperature jumps in rabbit psoas muscle fibres.

Abstract

SUMMARY1. A technique was developed to generate 2-8°C step temperature perturbations (T-jumps) in single muscle fibres to study the thermodynamics of muscle contraction. A solid-state pulsed holmium laser emitting at 2-065 usm heated the fibre and surrounding solution in approximately 150 /is. The signal from a 100 ,um thermocouple fed back to a heating wire maintained the elevated temperature after the laser pulse.2. Tension of glycerol-extracted muscle fibres from rabbit psoas muscle did not change significantly following T-jumps when the fibre was relaxed.3. In rigor, tension decreased abruptly on heating indicating normal (not rubberlike) thermoelasticity. The thermoelastic coefficient (negative ratio of relative length change to relative temperature change) of the fibre was estimated to be -0-021 at sarcomere lengths of 2-5-2-8 ,um. Rigor tension was constant after the temperature step and returned to the original value on recooling.4. In maximal Ca2+ activation, tension transients initiated by T-jumps had several phases. An immediate tension decrease suggests that thermoelasticity during contraction is similar to that in rigor. Active tension then recovered to the value before the T-jump with an apparent rate constant of approximately 400 s-1 (at 10-20°C). This rate constant did not have an appreciable dependence on the final temperature. Finally, tension increased exponentially to a new higher level with a rate constant of approximately 20 s-5 at 20 'C. This rate constant increased with temperature with a Q10 of 1-4.5. At submaximal Ca2+ activation the tension rise was followed by a decay to below the value before the T-jump. This decline was expected from the temperature dependence of steady pCa-tension curves. The final tension decline occurred on the 1-5 s time scale.6. The value and amplitude dependence of the rate constant for the quick recovery following T-jumps were similar to those of the quick recovery following length steps during active contractions. The enthalpy change associated with the quick tension

Use of thin filament reconstituted muscle fibres to probe the mechanism of force generation

“…ΔH° > 0, ΔS° > 0 and ΔC P < 0 have been observed in rabbit psoas fibres (Zhao and Kawai 1994a;Murphy et al 1996) and soleus slow twitch fibres (Wang and Kawai 2001) on the step that generates force. This mechanism is consistent with the well known observation that isometric tension increases with an increase in the temperature both in mammalian skeletal (Goldman et al 1987;Ranatunga et al 1987;Zhao and Kawai 1994a;Coupland et al 2001;Wang and Kawai 2001) and cardiac (Ranatunga 1999;) muscle fibres, and reviewed by Kawai (2003).…”

“…2C), and "relaxation" is induced by the solution that adds 40 mM BDM to the relaxing solution and by lowering the temperature to 2°C. As it has been known for some time, active tension increases with temperature in mammalian muscles (Goldman et al 1987;Ranatunga et al 1987;Bershitsky and Tsaturyan 1992;Zhao and Kawai 1994a). Figure 2C demonstrates that the active tension is not sensitive to Ca 2+ , as expected.…”

“…Other examples are temperature jump (Goldman et al 1987;Bershitsky and Taturyan 1992), pressure release (Fortune et al 1991), and a use of caged compounds which releases a specific ligand on photoflash (Goldman et al 1984;Dantzig et al 1992;Araujo and Walker 1996). The released ligand binds to a contractile protein to initiate a transient.…”

Light as a trigger for time-resolved structural experiments on muscle, lipids, p21 and bacteriorhodopsin

“…After about 1.4 s tension declines, which is attributed to cooling. The fast rate is in good agreement with the data of Goldman, McCray & Ranatunga (1987), even though these authors found an additional even faster rate during the first milliseconds after the T jump at a rate of 400 s which is beyond the time resolution of our experiment. The structural alteration as expressed by the ratio of the intensities of the 11 over the 10 reflection shows a rapid change which is paralleled with a similarly rapid first phase in the spacing of the 11 reflection (Figs.…”

Force Responses and Sarcomere Dynamics of Cardiac Myofibrils Induced by Rapid Changes in [Pi]

“…It is generally accepted that the first and major force-generating step is not coupled to the cleavage of ATP into ADP and inorganic phosphate (P i ) but rather to the subsequent, reversible release of P i , e.g., through the backdoor of the myosin molecule (1)(2)(3)(4). To explore the chemomechanical coupling, force changes were induced in muscle fibers by rapid length changes (5-10), temperature jumps (5,11), pressure jumps (12), or photolytic release of caged-P i (13)(14)(15)(16)(17), and the kinetics of these force changes were interpreted in terms of cross-bridge models. The rapid change in [P i ] provides a well-defined approach because it specifically perturbs the reversible equilibrium of the P i -release.…”