Kinetic Effects of Fiber Type on the Two Subcomponents of the Huxley-Simmons Phase 2 in Muscle

Davis, Julien S.; Epstein, Neal D.

doi:10.1016/s0006-3495(03)74483-x

Cited by 15 publications

(44 citation statements)

References 47 publications

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“…Phase 2 slow (orange), the other slower component of phase 2, has properties consistent with de novo tension generation (7). Its T-jump equivalent is phase 2 (7,9,18,19,25,28). Phase 3 (blue) appears associated with the kinetics of P i release (see Table 2 in ref.…”

Section: L-jump Tension Transientsmentioning

confidence: 94%

“…The fastest [phase 2 fast (red)], is a component of the classical phase 2. Its rate is virtually temperature-insensitive, and its amplitude is proportional to phase 1 stiffness (19). Thus, phase 2 fast has the mechanical properties of a damped (slow-responding) entropic spring (27).…”

Section: L-jump Tension Transientsmentioning

confidence: 99%

“…Phase 3 (blue) appears associated with the kinetics of P i release (see Table 2 in ref. 19). Phase 4 (green), the slowest phase, mediates the asymptotic return to isometric tension.…”

Section: L-jump Tension Transientsmentioning

confidence: 99%

“…Defining the link between tension generation and the release of the products of hydrolysis and to the free energy change of P i release, in particular, has proved demanding. Articles placing tension generation before (11)(12)(13)(14), during (15,16), or after (7,(17)(18)(19)(20) P i release reflect this issue. In contrast, there is general agreement that dissociation of ADP occurs last from low-strain cross-bridges at the end of the cycle.…”

mentioning

confidence: 99%

“…One exponential phase (phase 2 slow in the L-jump, 2 in the laser T-jump) appears associated with de novo tension generation. Phase 2 slow and phase 2 fast , a damped elasticity, comprise the classical Huxley-Simmons phase 2 (7,19) or ''rapid recovery of tension'' associated with studies on tension generation in muscle for well on 3 decades (1).…”

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confidence: 99%

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Mechanistic role of movement and strain sensitivity in muscle contraction

Davis

Epstein

2009

Proc. Natl. Acad. Sci. U.S.A.

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Tension generation can be studied by applying step perturbations to contracting muscle fibers and subdividing the mechanical response into exponential phases. The de novo tension-generating isomerization is associated with one of these phases. Earlier work has shown that a temperature jump perturbs the equilibrium constant directly to increase tension. Here, we show that a length jump functions quite differently. A step release (relative movement of thick and thin filaments) appears to release a steric constraint on an ensemble of noncompetent postphosphate release actomyosin cross-bridges, enabling them to generate tension, a concentration jump in effect. Structural studies [Taylor KA, et al. (1999) Tomographic 3D reconstruction of quick-frozen, Ca 2؉ -activated contracting insect flight muscle. Cell 99:421-431] that map to these kinetics indicate that both catalytic and lever arm domains of noncompetent myosin heads change angle on actin, whereas lever arm movement alone mediates the power stroke. Together, these kinetic and structural observations show a 13-nm overall interaction distance of myosin with actin, including a final 4-to 6-nm power stroke when the catalytic domain is fixed on actin. Raising fiber temperature with both perturbation techniques accelerates the forward, but slows the reverse rate constant of tension generation, kinetics akin to the unfolding/folding of small proteins. Decreasing strain, however, causes both forward and reverse rate constants to increase. Despite these changes in rate, the equilibrium constant is strain-insensitive. Activation enthalpy and entropy data show this invariance to be the result of enthalpyentropy compensation. Reaction amplitudes confirm a strain-invariant equilibrium constant and thus a strain-insensitive ratio of pretension-to tension-generating states as work is done.enthalpy-entropy compensation ͉ length step ͉ non-Arrhenius ͉ protein folding ͉ tension generation T he question of how the many asynchronously operating myosin motors generate tension and movement in muscle fibers is a critical issue in biology. Two different mechanisms have been proposed. In one, thermal fluctuations in position enable myosin heads (cross-bridges) to bind actin in a strained configuration to generate tension (1, 2). This rectification process can occur between detached and attached heads or by heads changing angle between subsites while attached to actin. For these thermal ratchet models to function at physiological rates, a sequence of multiple attached states is generally required, the stiffer the cross-bridge the larger the number of states. Heterogeneous mechanisms, some with sequential temperature-sensitive and -insensitive tension-generating transitions, have also been invoked (3-5). Power stroke mechanisms in which tension generation occurs as a single-step conformational change in attached cross-bridges offer an alternative mechanism e.g. (6-10). Other important aspects include the relationship between intermediate states of the ATPase cycle and tension generation....

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Section: L-jump Tension Transientsmentioning

confidence: 94%

Section: L-jump Tension Transientsmentioning

confidence: 99%

“…Phase 3 (blue) appears associated with the kinetics of P i release (see Table 2 in ref. 19). Phase 4 (green), the slowest phase, mediates the asymptotic return to isometric tension.…”

Section: L-jump Tension Transientsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Mechanistic role of movement and strain sensitivity in muscle contraction

Davis

Epstein

2009

Proc. Natl. Acad. Sci. U.S.A.

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Reinterpretation of the Tension Response of Muscle to Stretches and Releases

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Ranatunga

2016

Biophysical Journal

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We have reexamined the experimental time courses of tension in frog muscle after rapid length steps. The early tension recoveries are biexponential. After 3 nm/hs stretches and releases, the rates of the immediate rapid tension changes are similar but the subsequent tension fall after a stretch is much slower than the rise after a release. After 1.5 nm/hs length steps, the entire tension responses are more nearly mirror images. To identify the underlying processes, we used a model of the muscle cross-bridge cycle with two tension-generating (tensing) steps. Analysis of the time course of the tension, the rates of the steps in the cycle, and their contributions to tension provided insights into previously puzzling features of the experimental response. After a stretch, the initial rapid tension fall in the model is caused principally by the reversal of the first tensing step, but after a few milliseconds the tensing step resumes its forward direction. We conclude that the remaining response should not be included in phase 2, the period of early tension recovery. With this exclusion, T 2 , the tension at the end of this period, rises with an increase of stretch. The rate of early tension recovery also increases with stretch size, showing that the reversal of the first tensing step is strain sensitive. After small length steps, the fast and slow components of the early tension recovery are both caused mainly by the first tensing step. The fast component is triggered by the initial sliding of the filaments, and the slow component is due to further sliding that occurs as the tension recovers. With small length steps (<0.5 nm/hs), the time course of the response to a stretch is the reverse of that to a release.

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The Location and Rate of the Phosphate Release Step in the Muscle Cross-Bridge Cycle

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Ranatunga

2020

Biophysical Journal

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It is controversial whether the phosphate (Pi) release step in the cross-bridge cycle occurs before or after the first tension-generating step and whether it is fast or slow. We have therefore modified our previous model of the frog cross-bridge cycle by including a Pi release step either before (model A) or after (model B) the first tension-generating step and refined the two models by downhill simplex runs against experimental data for the force-velocity relation and the tension transients after length steps. Pi release step was initially made slow (70 s À1 ), but after refinement, it became fast ($500 s À1 for model A and $6000 s À1 for model B). The two models gave similar fits to the experimental tension transients after length steps, but model A gave a better fit to the lengthening limb of the force-velocity relation than model B.

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Kinetic Effects of Fiber Type on the Two Subcomponents of the Huxley-Simmons Phase 2 in Muscle

Cited by 15 publications

References 47 publications

Mechanistic role of movement and strain sensitivity in muscle contraction

Mechanistic role of movement and strain sensitivity in muscle contraction

Reinterpretation of the Tension Response of Muscle to Stretches and Releases

The Location and Rate of the Phosphate Release Step in the Muscle Cross-Bridge Cycle

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