Effect of temperature on elementary steps of the cross‐bridge cycle in rabbit soleus slow‐twitch muscle fibres

Wang, Brant G.; Kawai, Masataka

doi:10.1111/j.1469-7793.2001.0219j.x

Cited by 62 publications

(92 citation statements)

References 54 publications

(107 reference statements)

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“…The MgATP-dependent cross-bridge detachment rates from skinned rat soleus fibers at 17 C (Fig. 4 K) are consistent with the 2pc-MgATP relationships measured in skinned rabbit soleus fibers at 20 C (37,38). Specifically, we show that the myosin detachment rate increased from 8. soleus fibers at 20 C (37) compared to rat soleus fibers at 17 C (Fig.…”

Section: Discussionsupporting

confidence: 74%

Myosin MgADP Release Rate Decreases as Sarcomere Length Increases in Skinned Rat Soleus Muscle Fibers

Fenwick

Leighton

Tanner

2016

Biophysical Journal

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Actin-myosin cross-bridges use chemical energy from MgATP hydrolysis to generate force and shortening in striated muscle. Previous studies show that increases in sarcomere length can reduce thick-to-thin filament spacing in skinned muscle fibers, thereby increasing force production at longer sarcomere lengths. However, it is unclear how changes in sarcomere length and lattice spacing affect cross-bridge kinetics at fundamental steps of the cross-bridge cycle, such as the MgADP release rate. We hypothesize that decreased lattice spacing, achieved through increased sarcomere length or osmotic compression of the fiber via dextran T-500, could slow MgADP release rate and increase cross-bridge attachment duration. To test this, we measured cross-bridge cycling and MgADP release rates in skinned soleus fibers using stochastic length-perturbation analysis at 2.5 and 2.0 mm sarcomere lengths as pCa and [MgATP] varied. In the absence of dextran, the force-pCa relationship showed greater Ca 2þ sensitivity for 2.5 vs. 2.0 mm sarcomere length fibers (pCa 50 ¼ 5.68 5 0.01 vs. 5.60 5 0.01). When fibers were compressed with 4% dextran, the length-dependent increase in Ca 2þ sensitivity of force was attenuated, though the Ca 2þ sensitivity of the force-pCa relationship at both sarcomere lengths was greater with osmotic compression via 4% dextran compared to no osmotic compression. Without dextran, the cross-bridge detachment rate slowed by~15% as sarcomere length increased, due to a slower MgADP release rate (11.2 5 0.5 vs. 13.5 5 0.7 s À1 ). In the presence of dextran, cross-bridge detachment was~20% slower at 2.5 vs. 2.0 mm sarcomere length due to a slower MgADP release rate (10.1 5 0.6 vs. 12.9 5 0.5 s À1 ). However, osmotic compression of fibers at either 2.5 or 2.0 mm sarcomere length produced only slight (and statistically insignificant) slowing in the rate of MgADP release. These data suggest that skeletal muscle exhibits sarcomere-length-dependent changes in cross-bridge kinetics and MgADP release that are separate from, or complementary to, changes in lattice spacing.

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Section: Discussionsupporting

confidence: 74%

Myosin MgADP Release Rate Decreases as Sarcomere Length Increases in Skinned Rat Soleus Muscle Fibers

Fenwick

Leighton

Tanner

2016

Biophysical Journal

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“…Assuming a duty cycle of ∼0.5 (Kaya and Higuchi, 2010), this translates to a duration of about 335 ms for the bound life of a cross-bridge in frog muscle contracting isometrically at 0°C. Studies of rabbit muscle fibers suggest that Q 10 values for cross-bridge detachment rates are quite high, between 3 and 4 (Wang and Kawai, 2001). For a Q 10 of 3, we would expect the process of detachment and reattachment to increase by a factor of 27 from 0 to 30°C; thus, the duration of binding for a cross-bridge would be less than 10 ms at typical avian or mammalian body temperatures.…”

Section: Cross-bridge and Myofilament Elasticitymentioning

confidence: 99%

Contribution of elastic tissues to the mechanics and energetics of muscle function during movement

Roberts

2016

Journal of Experimental Biology

163

115

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Muscle force production occurs within an environment of tissues that exhibit spring-like behavior, and this elasticity is a critical determinant of muscle performance during locomotion. Muscle force and power output both depend on the speed of contraction, as described by the isotonic force-velocity curve. By influencing the speed of contractile elements, elastic structures can have a profound effect on muscle force, power and work. In very rapid movements, elastic mechanisms can amplify muscle power by storing the work of muscle contraction slowly and releasing it rapidly. When energy must be dissipated rapidly, such as in landing from a jump, energy stored rapidly in elastic elements can be released more slowly to stretch muscle contractile elements, reducing the power input to muscle and possibly protecting it from damage. Elastic mechanisms identified so far rely primarily on in-series tendons, but many structures within muscles exhibit springlike properties. Actomyosin cross-bridges, actin and myosin filaments, titin, and the connective tissue scaffolding of the extracellular matrix all have the potential to store and recover elastic energy during muscle contraction. The potential contribution of these elements can be assessed from their stiffness and estimates of the strain they undergo during muscle function. Such calculations provide boundaries for the possible roles these springs might play in locomotion, and may help to direct future studies of the uses of elastic elements in muscle.

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“…ΔH° > 0 and ΔS° > 0 have been observed on actomyosin interaction in solution (Tonomura et al 1962;Highsmith 1977) and in myofibrils (Ishiwata et al 1986). 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).…”

Section: Temperature Effect and Hydrophobic Interactionmentioning

confidence: 95%

“…That is, K 1 may change as a result of change in isometric tension. It was reported that the ATP binding step (K 1 ) may be influenced by loop 1 of myosin, because the charge distribution on the loop 1 and K 1 may be correlated (Wang and Kawai 2001); loop 1 comes close to the ATP binding site. It is possible that the position of loop 1 changes according to the strain on the myosin head, and this change in turn alters the ATP binding to the myosin head.…”

Section: Tropomyosin or Troponin?mentioning

confidence: 99%

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

Kawai

Ishiwata

2006

J Muscle Res Cell Motil

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The technique of selective removal of the thin filament by gelsolin in bovine cardiac muscle fibres, and reconstitution of the thin filament from isolated proteins is reviewed, and papers that used reconstituted preparations are discussed. By comparing the results obtained in the absence/presence of regulatory proteins tropomyosin (Tm) and troponin (Tn), it is concluded that the role of Tm and Tn in force generation is not only to expose the binding site of actin to myosin, but also to modify actin for better stereospecific and hydrophobic interaction with myosin. This conclusion is further supported by experiments that used a truncated Tm mutant and the temperature study of reconstituted fibres. The conclusion is consistent with the hypothesis that there are three states in the thin filament: blocked state, closed state, and open state. Tm is the major player to produce these effects, with Tn playing the role of Ca 2+ sensing and signal transmission mechanism. Experiments that changed the number of negative charges at the N-terminal finger of actin demonstrates that this part of actin is essential to promote the strong interaction between actin and myosin molecules, in addition to the well-known weak interaction that positions the myosin head at the active site of actin prior to force generation. KeywordsActin; Regulatory proteins; Tropomyosin; Troponin; Myosin; Gelsolin; Cross-bridge kinetics; Sinusoidal analysis; BDM Thin filament reconstituted muscle fibre systemFor the purpose of understanding the cross-bridge interaction with actin and the role of regulatory proteins in this interaction, we reconstituted the thin filament in cardiac muscle fibres. This method is schematically represented in Fig. 1. The thin filament is first removed by gelsolin (Fig. 1A to 1B), followed by sequential reconstitution with G-actin (Fig. 1C), and regulatory proteins, tropomyosin (Tm) and troponin (Tn) (Fig. 1D). Gelsolin is an actin and thin filament severing protein, hence its action is specific and it does not disrupt other sarcomeric structure. However, overtreatment with gelsolin would disrupt the Z-line structure, because actin is one of the main constituents in the Z-line. The thin filament reconstitution method was initially developed at Ishiwata's laboratory and the key properties of the Correspondence to: Masataka Kawai, masataka-kawai@uiowa.edu. reconstituted fibres, such as the recovery of isometric tension, the tension-pCa relationship, and the function of spontaneous oscillatory contraction, were examined on skeletal fibres (Funatsu et al. 1994), followed by cardiac fibres (Fujita et al. 1996; Ishiwata 1998, 1999; for brief review see Ishiwata et al. 1998). In these works, it was demonstrated that bovine cardiac fibres were successful as the reconstituted system, in which actin, Tm and Tn can be replaced with those prepared from other muscles, for example, rabbit skeletal muscle proteins (Fujita et al. 1996;Fujita and Ishiwata 1999). The reconstitution method in cardiac fibres was successfully applied at ...

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Effect of temperature on elementary steps of the cross‐bridge cycle in rabbit soleus slow‐twitch muscle fibres

Cited by 62 publications

References 54 publications

Myosin MgADP Release Rate Decreases as Sarcomere Length Increases in Skinned Rat Soleus Muscle Fibers

Myosin MgADP Release Rate Decreases as Sarcomere Length Increases in Skinned Rat Soleus Muscle Fibers

Contribution of elastic tissues to the mechanics and energetics of muscle function during movement

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

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