Temperature change as a probe of muscle crossbridge kinetics: a review and discussion

Woledge, Roger C.; Barclay, Christopher John; Curtin, N. A.

doi:10.1098/rspb.2009.0177

Cited by 34 publications

(46 citation statements)

References 30 publications

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“…The mechanism underlying the steep dependence of force generation on temperature in hummingbird and finch pectoralis fibers in not known. It is possible that an increase in temperature shifts attached crossbridges to a higher force-generating state that is not extensively populated at lower temperatures (Woledge et al, 2009). Regardless of whether the observed temperature sensitivity is due to greater force per crossbridge and/or a shift in the crossbridge population, the change(s) appear to be of far greater magnitude than in other studied muscles.…”

Section: Discussionmentioning

confidence: 62%

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Reiser

Welch

Suarez

et al. 2013

Journal of Experimental Biology

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SUMMARYHummingbird flight muscle is estimated to have among the highest mass-specific power output among vertebrates, based on aerodynamic models. However, little is known about the fundamental contractile properties of their remarkable flight muscles. We hypothesized that hummingbird pectoralis fibers generate relatively low force when activated in a tradeoff for high shortening speeds associated with the characteristic high wingbeat frequencies that are required for sustained hovering. Our objective was to measure maximal force-generating ability (maximal force/cross-sectional area, P o /CSA) in single, skinned fibers from the pectoralis and supracoracoideus muscles, which power the wing downstroke and upstroke, respectively, in hummingbirds (Calypte anna) and in another similarly sized species, zebra finch (Taeniopygia guttata), which also has a very high wingbeat frequency during flight but does not perform a sustained hover. Mean P o /CSA in hummingbird pectoralis fibers was very low -1.6, 6.1 and 12.2kNm -2 , at 10, 15 and 20°C, respectively. P o /CSA in finch pectoralis fibers was also very low (for both species, ~5% of the reported P o /CSA of chicken pectoralis fast fibers at 15°C). Q 10-force (force generated at 20°C/force generated at 10°C) was very high for hummingbird and finch pectoralis fibers (mean=15.3 and 11.5, respectively) compared with rat slow and fast fibers (1.8 and 1.9, respectively). P o /CSA in hummingbird leg fibers was much higher than in pectoralis fibers at each temperature, and the mean Q 10-force was much lower. Thus, hummingbird and finch pectoralis fibers have an extremely low force-generating ability compared with other bird and mammalian limb fibers, and an extremely high temperature dependence of force generation. However, the extrapolated maximum force-generating ability of hummingbird pectoralis fibers in vivo (~48kNm -2 ) is substantially higher than the estimated requirements for hovering flight of C. anna. The unusually low P o /CSA of hummingbird and zebra finch pectoralis fibers may reflect a constraint imposed by a need for extremely high contraction frequencies, especially during hummingbird hovering. Supplementary material available online at

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Section: Discussionmentioning

confidence: 62%

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Reiser

Welch

Suarez

et al. 2013

Journal of Experimental Biology

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“…Some of the adaptations to permit this are related to calcium channel function (Wang et al, 2002; Hauton et al, 2011). However, the force from motor proteins at low temperatures is reduced (Rall and Woledge, 1990;Piazzesi et al, 2003;Woledge et al, 2009), and yet ground squirrel hearts function at near-freezing temperatures, while simultaneously supporting cardiac performance when body temperature returns to euthermy, a temperature differential of over 30°C. Second, the activity of the heart, as quantified by heart rate, ranges from over 350-400 beats min -1 prior to hibernation, to a low of 4-5 beats min -1 during torpor.…”

Section: Echocardiogram and Myosin Of Hibernatorsmentioning

confidence: 99%

Increase in cardiac myosin heavy-chain (MyHC) alpha protein isoform in hibernating ground squirrels, with echocardiographic visualization of ventricular wall hypertrophy and prolonged contraction.

Nelson

Rourke

2013

Journal of Experimental Biology

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SUMMARYDeep hibernators such as golden-mantled ground squirrels (Callospermophilus lateralis) have multiple challenges to cardiac function during low temperature torpor and subsequent arousals. As heart rates fall from over 300 beats min -1 to less than 10, chamber dilation and reduced cardiac output could lead to congestive myopathy. We performed echocardiography on a cohort of individuals prior to and after several months of hibernation. The left ventricular chamber exhibited eccentric and concentric hypertrophy during hibernation and thus calculated ventricular mass was ~30% greater. Ventricular ejection fraction was mildly reduced during hibernation but stroke volumes were greater due to the eccentric hypertrophy and dramatically increased diastolic filling volumes. Globally, the systolic phase in hibernation was ~9.5 times longer, and the diastolic phase was 28× longer. Left atrial ejection generally was not observed during hibernation. Atrial ejection returned weakly during early arousal. Strain echocardiography assessed the velocity and total movement distance of contraction and relaxation for regional ventricular segments in active and early arousal states. Myocardial systolic strain during early arousal was significantly greater than the active state, indicating greater total contractile movement. This mirrored the increased ventricular ejection fraction noted with early arousal. However, strain rates were slower during early arousal than during the active period, particularly systolic strain, which was 33% of active, compared with the rate of diastolic strain, which was 67% of active. As heart rate rose during the arousal period, myocardial velocities and strain rates also increased; this was matched closely by cardiac output. Curiously, though heart rates were only 26% of active heart rates during early arousal, the cardiac output was nearly 40% of the active state, suggesting an efficient pumping system. We further analyzed proportions of cardiac myosin heavy-chain (MyHC) isoforms in a separate cohort of squirrels over 5 months, including time points before hibernation, during hibernation and just prior to emergence. Hibernating individuals were maintained in both a 4°C cold room and a 20°C warm room. Measured by SDS-PAGE, relative percentages of cardiac MyHC alpha were increased during hibernation, at both hibernacula temperatures. A potential increase in contractile speed, and power, from more abundant MyHC alpha may aid force generation at low temperature and at low heart rates. Unlike many models of cardiomyopathies where the alpha isoform is replaced by the beta isoform in order to reduce oxygen consumption, ground squirrels demonstrate a potential cardioprotective mechanism to maintain cardiac output during torpor. Received 25 March 2013; Accepted 4 September 2013Key words: hibernation, MyHC, echocardiogram, atrial contraction, cardiac function. Echocardiogram and myosin of hibernatorsThe myosin heavy-chain isoforms (MyHC) are crucial determinants of contractile performance in cardiac muscle t...

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“…Schemes of the cross-bridge cycle with a branched pathway were previously hypothesized (Kawai et al 1987;Smith & Mijailovich 2008;Woledge et al 2009); however, none of them is adequate to account for the different Pi dependence of the number of cross-bridges and ATPase rate in isometric contraction. On the other hand, the idea that the myosin can detach from actin at different stages of the working stroke, allowing rapid termination of the biochemical and structural steps of the actomyosin interaction at high load, probably applies also at physiological [Pi], and thus after the Pi release.…”

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confidence: 99%

A kinetic model that explains the effect of inorganic phosphate on the mechanics and energetics of isometric contraction of fast skeletal muscle

2009

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A conventional five-step chemo-mechanical cycle of the myosin -actin ATPase reaction, which implies myosin detachment from actin upon release of hydrolysis products (ADP and phosphate, Pi) and binding of a new ATP molecule, is able to fit the [Pi] dependence of the force and number of myosin motors during isometric contraction of skeletal muscle. However, this scheme is not able to explain why the isometric ATPase rate of fast skeletal muscle is decreased by an increase in [Pi] much less than the number of motors. The question can be solved assuming the presence of a branch in the cycle: in isometric contraction, when the force generation process by the myosin motor is biased at the start of the working stroke, the motor can detach at an early stage of the ATPase cycle, with Pi still bound to its catalytic site, and then rapidly release the hydrolysis products and bind another ATP. In this way, the model predicts that in fast skeletal muscle the energetic cost of isometric contraction increases with [Pi]. The large dissociation constant of the product release in the branched pathway allows the isometric myosin -actin reaction to fit the equilibrium constant of the ATPase.

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Temperature change as a probe of muscle crossbridge kinetics: a review and discussion

Cited by 34 publications

References 30 publications

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Very low force-generating ability and unusually high temperature-dependency in hummingbird flight muscle fibers

Increase in cardiac myosin heavy-chain (MyHC) alpha protein isoform in hibernating ground squirrels, with echocardiographic visualization of ventricular wall hypertrophy and prolonged contraction.

A kinetic model that explains the effect of inorganic phosphate on the mechanics and energetics of isometric contraction of fast skeletal muscle

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