Nucleotide-Dependent Contractile Properties of Ca2+-Activated Fast and Slow Skeletal Muscle Fibers

Wahr, Philip A.; Cantor, H. C.; Metzger, Joseph M.

doi:10.1016/s0006-3495(97)78716-2

Cited by 23 publications

(37 citation statements)

References 49 publications

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“…In this regard, elevations in P i (from 0 to ϳ15 mM) have been reported to speed the rates of force generation in skeletal (37,38) and cardiac (2) muscle preparations but had minimal effects on unloaded shortening velocity in fast-twitch skeletal muscle fibers (4,26,42). We also found no effect of 5 mM P i on V o in skinned cardiac myocyte preparations (Fig.…”

Section: Discussionsupporting

confidence: 57%

“…Regarding other contractile properties, added P i has been reported to increase k Pi (the rate constant of force decline after rapid increases in solution P i ) to a greater extent in cardiac myocyte preparations than in fast-twitch skeletal muscle fibers (2,41). Additionally, the increase in k tr with added [P i ] (from 0 to 10 mM) was upward of threefold in our skinned cardiac myocyte preparations vs. a 50% increase in fast-twitch skinned skeletal muscle fibers (38). Together these results suggest that contractile properties appear to be more sensitive to elevations in [P i ] in cardiac muscle than skeletal muscle at least over a range of 0 -10 mM added P i .…”

Section: Discussionmentioning

confidence: 49%

“…It is unknown which chemomechanical transitions are most important in determining force and shortening speeds and thus power output at intermediate loads where muscles perform work. Because elevations in P i concentration ([P i ]; from 0 to ϳ15 mM) increase the rate of force development (2,16,37,38) but have no effect on unloaded shortening velocity in skinned fast-twitch skeletal muscle fibers (4,26,42), experiments in the presence of increased [P i ] should indicate at which loads shortening velocities are most influenced by P i transitional states, i.e., those that are associated with weak to strong-binding to force-producing states (steps 3-5, Fig. 1).…”

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confidence: 99%

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Inorganic phosphate speeds loaded shortening in rat skinned cardiac myocytes

Hinken¹,

McDonald²

2004

American Journal of Physiology-Cell Physiology

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Hinken, Aaron C., and Kerry S. McDonald. Inorganic phosphate speeds loaded shortening in rat skinned cardiac myocytes. Am J Physiol Cell Physiol 287: C500 -C507, 2004. First published April 14, 2004 10.1152/ajpcell.00049.2004.-Force generation in striated muscle is coupled with inorganic phosphate (Pi) release from myosin, because force falls with increasing P i concentration ([Pi]). However, it is unclear which steps in the cross-bridge cycle limit loaded shortening and power output. We examined the role of Pi in determining force, unloaded and loaded shortening, power output, and rate of force development in rat skinned cardiac myocytes to discern which step in the cross-bridge cycle limits loaded shortening. Myocytes (n ϭ 6) were attached between a force transducer and position motor, and contractile properties were measured over a range of loads during maximal Ca 2ϩ activation. Addition of 5 mM Pi had no effect on maximal unloaded shortening velocity (V o) (control 1.83 Ϯ 0.75, 5 mM added P i 1.75 Ϯ 0.58 muscle lengths/s; n ϭ 6). Conversely, addition of 2.5, 5, and 10 mM P i progressively decreased force but resulted in faster loaded shortening and greater power output (when normalized for the decrease in force) at all loads greater than ϳ10% isometric force. Peak normalized power output increased 16% with 2.5 mM added P i and further increased to a plateau of ϳ35% with 5 and 10 mM added P i. Interestingly, the rate constant of force redevelopment (ktr) progressively increased from 0 to 10 mM added Pi, with k tr ϳ360% greater at 10 mM than at 0 mM added Pi. Overall, these results suggest that the P i release step in the cross-bridge cycle is rate limiting for determining shortening velocity and power output at intermediate and high relative loads in cardiac myocytes. muscle mechanics; force-velocity relationship; cross-bridge cycle DURING MUSCLE CONTRACTION myosin cross bridges cyclically interact with actin in a process that is driven energetically by hydrolysis of ATP. The chemomechanical states in the crossbridge cycle have been investigated extensively in skinned muscle fiber preparations, and the transition rates between these states are qualitatively similar to rates derived from muscle protein studies in solution (15). A working model for the chemomechanical steps in the cross-bridge cycle is shown in Fig. 1 (40), which is based on extensive work in the field (for reviews see Refs. 3 and 15). According to this model, the transition from weak-binding, non-force-generating cross bridges to strong-binding, forcegenerating states is associated with the release of inorganic phosphate (P i ) (steps 3-5, Fig. 1; Ref. 16). Force generation is maintained through the release of ADP (step 6, Fig. 1; Refs. 6 and 22), which is followed by binding of ATP and subsequent cross-bridge detachment. The binding of ATP and its hydrolysis are thought to be relatively fast processes in skinned fibers (9,14,23). Thus the rate-limiting step in the cross-bridge cycle is thought to occur after ATP hydrolysis, either during an ...

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Section: Discussionsupporting

confidence: 57%

Section: Discussionmentioning

confidence: 49%

mentioning

confidence: 99%

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Inorganic phosphate speeds loaded shortening in rat skinned cardiac myocytes

Hinken¹,

McDonald²

2004

American Journal of Physiology-Cell Physiology

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“…Results from previous studies (e.g. Metzger and Moss, 1990;Wahr et al, 1997;Danieli-Betto et al, 2000) have shown that pCa 4.0 or higher is maximally activating for rat fast and slow fibers.…”

Section: The Journal Of Experimental Biology 216 (12)mentioning

confidence: 74%

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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“…One approach to associating biochemical steps with mechanical events is to use the ability of myosin to hydrolyse a wide variety of divalent cation–nucleotide triphosphate substrates, which power work production in muscle to varying degrees (reviewed by Needham, 1971). In recent years several groups have used this property to relate actomyosin kinetics to muscle mechanics (Burton & Sleep, 1987; Pate et al 1993; White et al 1993; Wahr et al 1997; Regnier et al 1998; Regnier & Homsher, 1998; Seow et al 2001). In this paper we have varied the substrate to compare steady‐state and transient solution kinetics to rates of force recovery and fibre shortening.…”

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confidence: 99%

Kinetics of muscle contraction and actomyosin NTP hydrolysis from rabbit using a series of metal–nucleotide substrates

Burton

White

Sleep

2005

The Journal of Physiology

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Mechanical properties of skinned single fibres from rabbit psoas muscle have been correlated with biochemical steps in the cross-bridge cycle using a series of metal-nucleotide (Me·NTP) substrates (Mn 2+ or Ni 2+ substituted for Mg 2+ ; CTP or ITP for ATP) and inorganic phosphate. Measurements were made of the rate of force redevelopment following (1) slack tests in which force recovery followed a period of unloaded shortening, or (2) ramp shortening at low load terminated by a rapid restretch. The form and rate of force recovery were described as the sum of two exponential functions. Actomyosin-Subfragment 1 (acto-S1) Me·NTPase activity and Me·NDP release were monitored under the same conditions as the fibre experiments. Mn·ATP and Mg·CTP both supported contraction well and maintained good striation order. Relative to Mg·ATP, they increased the rates and Me·NTPase activity of cross-linked acto-S1 and the fast component of a double-exponential fit to force recovery by ∼50% and 10-35%, respectively, while shortening velocity was moderately reduced (by 20-30%). Phosphate also increased the rate of the fast component of force recovery. In contrast to Mn 2+ and CTP, Ni·ATP and Mg·ITP did not support contraction well and caused striations to become disordered. The rates of force recovery and Me·NTPase activity were less than for Mg·ATP (by 40-80% and 50-85%, respectively), while shortening velocity was greatly reduced (by ∼80%). Dissociation of ADP from acto-S1 was little affected by Ni 2+ , suggesting that Ni·ADP dissociation does not account for the large reduction in shortening velocity. The different effects of Ni 2+ and Mn 2+ were also observed during brief activations elicited by photolytic release of ATP. These results confirm that at least one rate-limiting step is shared by acto-S1 ATPase activity and force development. Our results are consistent with a dual rate-limitation model in which the rate of force recovery is limited by both NTP cleavage and phosphate release, with their relative contributions and apparent rate constants influenced by an intervening rapid force-generating transition. An important property of contractile function is force development at the start of contraction or after shortening (Ekelund & Edman, 1982;Brenner & Eisenberg, 1986; K. Burton et al. in preparation), the rate of which is thought to be limited by attachment and detachment reactions of cross-bridges. Identification of the step(s) in the cross-bridge cycle which control this rate is important in the understanding of several properties of active muscle, including stiffness and the curvature of the force-velocity relation.Brenner & Eisenberg (1986) compared the steady-state ATPase of cross-linked actomyosin-S1 over a range of temperatures to rates of force redevelopment under the same conditions in skinned single fibres from rabbit skeletal muscle following isotonic shortening at low load. Shortening was terminated by rapidly restretching the fibre to its original length, a procedure previously shown by Brenner (1983) to inc...

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Nucleotide-Dependent Contractile Properties of Ca2+-Activated Fast and Slow Skeletal Muscle Fibers

Cited by 23 publications

References 49 publications

Inorganic phosphate speeds loaded shortening in rat skinned cardiac myocytes

Inorganic phosphate speeds loaded shortening in rat skinned cardiac myocytes

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

Kinetics of muscle contraction and actomyosin NTP hydrolysis from rabbit using a series of metal–nucleotide substrates

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