Quantitation of Ca ATPase, feet and mitochondria in superfast muscle fibres from the toadfish,Opsanus tau

Appelt, Denah M.; Shen, Vivienne; Franzini‐Armstrong, Clara

doi:10.1007/bf01738442

Cited by 91 publications

(97 citation statements)

References 33 publications

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“…Ultrastructural and biochemical studies suggest that this is achieved by a large increase in the density of SR calcium pumps (SERCAl isoform), an increased concentration of parvalbumin and a short diffusion distance for Ca2+ (-0.15 gm) in the narrow, lamellar-shaped myofibrils (5,7,21,33). There is also an increase in the density of SR Ca2+ release channels in swimbladder fibers (5) and it has been proposed that the channel isoform in this fiber type, the a-ryanodine receptor, abbreviates the time course of Ca2+ release (34). The much larger increase in Ca2+ pump density compared with that of Ca2+ release sites (5) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…A number of modifications appear to underlie this diversity. For example, in locomotory muscle, compared with slow twitch fibers, fast twitch fibers have a faster myosin with a higher maximum velocity of shortening (Vm,,) (2, 3), a greater content of sarcoplasmic reticulum (SR), and its associated Ca2+ pumps (4,5), a different isoform of the SR Ca2+ pump (SERCAl in fast versus SERCA2 in slow) (6,7) and a greater concentration of parvalbumin (a soluble protein that binds both calcium and magnesium) (5,8). There is also evidence that fast fibers have a briefer myoplasmic free Ca2+ concentration ([Ca2+]) transient (9,10) and less sensitive force-pCa relationship (11,12).…”

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confidence: 99%

“…Based on morphological and biochemical evidence from swimbladder of a very large SR Ca2+ pump density, a high density of SR Ca2+ release sites, and a large parvalbumin concentration, it has been proposed that an important modification of these sonic fibers is unusually rapid Ca2+ cycling (5,21). By measuring myoplasmic free [Ca2+], we found that these fibers do indeed have unusual Ca2+ tran-…”

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confidence: 99%

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The whistle and the rattle: the design of sound producing muscles.

Rome

Syme

Hollingworth

et al. 1996

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

226

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Vertebrate sound producing muscles often operate at frequencies exceeding 100 Hz, making them the fastest vertebrate muscles. Like other vertebrate muscle, these sonic muscles are "synchronous," necessitating that calcium be released and resequestered by the sarcoplasmic reticulum during each contraction cycle. Thus to operate at such high frequencies, vertebrate sonic muscles require extreme adaptations. We have found that to generate the "boatwhistle" mating call , the swimbladder muscle fibers of toadfish have evolved (i) a large and very fast calcium transient, (ii) a fast crossbridge detachment rate, and (iii) probably a fast kinetic off-rate of Ca2+ from troponin. The fi'bers of the shaker muscle of rattlesnakes have independently evolved similar traits, permitting tail rattling at '90 Hz.sients-in fact the largest and fastest ever recorded. However, our results showed that a fast Ca2+ transient alone is not sufficient for high frequency operation. By measuring Vmax, an index of crossbridge detachment rate, and the force-pCa relationship in skinned fibers, a possible index of troponin kinetics, we found that rapid activation and relaxation likely also require a modification of the crossbridge kinetic rate, and probably a modification of the kinetics of Ca2+-troponin binding. In reaching these conclusions, we first compared the above measurements in three fiber types from toadfish, ranging from slow twitch swimming fibers to the superfast twitch swimbladder fibers. We then compared the properties of rattlesnake shaker fibers with those of swimbladder.Skeletal muscle fibers perform a wide range of activities, and different fiber types are accordingly designed to operate at different speeds and frequencies (1). A number of modifications appear to underlie this diversity. For example, in locomotory muscle, compared with slow twitch fibers, fast twitch fibers have a faster myosin with a higher maximum velocity of shortening (Vm,,) (2, 3), a greater content of sarcoplasmic reticulum (SR), and its associated Ca2+ pumps (4, 5), a different isoform of the SR Ca2+ pump (SERCAl in fast versus SERCA2 in slow) (6, 7) and a greater concentration of parvalbumin (a soluble protein that binds both calcium and magnesium) (5, 8). There is also evidence that fast fibers have a briefer myoplasmic free Ca2+ concentration ([Ca2+]) transient (9, 10) and less sensitive force-pCa relationship (11,12).To understand the physiological modifications that underlie very rapid contractions, we have studied two of the fastest vertebrate muscles known. Both of these "sonic" muscles are used to produce sounds at the frequency at which the muscle contracts. The "boatwhistle" mating call of the male toadfish (Opsanus tau) is generated by '200 Hz contractions (25°C) of the muscles encircling the fish's gas-filled swimbladder (13-15). The familiar "rattle" of the venomous western diamondback rattlesnake (Crotalus atrox) is generated by "90 Hz contractions (35°C) of the shaker muscles at the base of the tail (16-19). The operational frequ...

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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The whistle and the rattle: the design of sound producing muscles.

Rome

Syme

Hollingworth

et al. 1996

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

226

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“…However, in more highly aerobic muscles, large mitochondrial volume densities would impose severe restrictions on the mount of space available in the sarcoplasm for the other components required for muscle function. In vertebrate muscles and synchronous insect muscles, the fraction of cell volume occupied by sarcoplasmic reticulum would be expected to increase as maximum contraction frequencies become greater (78,79), further limiting the amount of space available for sarcoplasmic enzymes. In toadfish sonic muscles, the sarcoplasmic reticulum accounts for an estimated 30% of muscle volume (79).…”

Section: Mechanistic and Evolutionary Implicationsmentioning

confidence: 99%

Relationships between enzymatic flux capacities and metabolic flux rates: Nonequilibrium reactions in muscle glycolysis

Suarez

Staples²,

Lighton³

et al. 1997

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

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The rules that govern the relationships between enzymatic f lux capacities (V max ) and maximum physiological f lux rates (v) at enzyme-catalyzed steps in pathways are poorly understood. We relate in vitro V max values with in vivo f lux rates for glycogen phosphorylase, hexokinase, and phosphofructokinase, enzymes catalyzing nonequilibrium reactions, from a variety of muscle types in fishes, insects, birds, and mammals. Flux capacities are in large excess over physiological f lux rates in low-f lux muscles, resulting in low fractional velocities (%V max ‫؍‬ v͞V max ؋ 100) in vivo. In high-f lux muscles, close matches between f lux capacities and f lux rates (resulting in fractional velocities approaching 100% in vivo) are observed. These empirical observations are reconciled with current concepts concerning enzyme function and regulation. We suggest that in high-f lux muscles, close matches between enzymatic f lux capacities and metabolic f lux rates (i.e., the lack of excess capacities) may result from space constraints in the sarcoplasm.Studies of structural and functional design in animals have led to valuable insights into the relationships between functional capacities and maximum physiological requirements or loads (1-3). At the biochemical level, biological design has been studied in terms of relationships between protein structure and function (4), pathway stoichiometry (5, 6), and mechanisms of regulation (5, 7). However, the synthesis and turnover of the thousands of metabolic enzymes possessed by each cell type is a costly enterprise (8), and the various compartments in cells appear to be highly crowded (9, 10). Current evidence suggests that there are probably upper limits to the design of biochemical capacities (11,12). Despite this, the rules that govern the design of functional capacities at the biochemical level are poorly understood. What are the relationships between enzymatic capacities for flux and maximum physiological flux rates through pathways? How much enzyme, in Diamond's words (13), is ''enough but not too much?'' Locomotory and cardiac muscles are ideally suited for the examination of capacity͞load relationships at the biochemical level because the maximum rate at which they do mechanical work defines the maximum rate at which ATP is hydrolyzed and, therefore, the maximum rate at which ATP resynthesizing pathways must operate. Herein, we present patterns of relationships, thus far unrecognized, between enzymatic flux capacities at nonequilibrium reactions in glycolysis and rates of glycolytic flux in muscles during exercise. Sources and Analysis of DataData concerning flux rates (v) and flux capacities (enzyme V max values) at three nonequilibrium steps in the glycolytic pathway, the hexokinase, glycogen phosphorylase, and phosphofructokinase reactions, are considered. These are taken from our own studies and published work from other laboratories. Most of the reactions in glycolysis lie close to equilibrium in vivo and are catalyzed by enzymes whose V max values may exceed p...

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“…Contrary to locomotory muscles, drumming muscles possess thin myofibrils and an elaborate development of the sarcoplasmic reticulum (Fawcett and Revel, 1961;Eichelberg, 1977;Ono and Poss, 1981;Bass and Marchaterre, 1989;Fine et al, 1993;Loesser et al, 1997). These features are linked to an unusually rapid calcium cycling necessary for fibers to operate at such high frequencies (Appelt et al, 1991;Rome et al, 1996). Feher et al (1998) relate the extensive sarcoplasmic reticulum to calcium capacity, which allows the muscle to keep contracting even though calcium is not completely recycled.…”

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confidence: 99%

Sound‐generating and ‐detecting motor system in catfish: Design of swimbladder muscles in doradids and pimelodids

Ladich

2001

Anat. Rec.

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Catfishes have evolved a diversity of swimbladder muscles serving in the generation of different sounds and probably other acoustic functions. In order to find out if anatomical and acoustical differences are parallelled by fine structural differences, I examined the sonic muscles of the doradid Platydoras and the pimelodid Pimelodus by gross dissections and ultrastructural methods. In Platydoras, the sound-generating (drumming) muscle (DM) inserts on a dorsal bony plate that vibrates the swimbladder. In pimelodids, the large DM attaches directly on the ventral surface of the swimbladder, whereas the small tensor tripodis muscle (TT) inserts on the rostral surface near the tripus, the most caudal Weberian ossicle. Fibers of all three muscles possess an extensive development of sarcoplasmatic reticulum (SR) in association with very thin myofibrils (MF) but differed widely in their arrangement. In Platydoras, ribbons of MFs are arranged radially around a central core. Mitochondria were found within the core and the peripheral sarcoplasm. Pimelodus does not have a differentiated core and the cross-sectional area of DM-MFs is about 15% larger as determined by stereological measurements. The TT possesses shorter sarcomeres and more mitochondria than DMs, which were primarily found between MFs. This suggests faster contraction properties and greater resistence to fatigue compared with sonic muscles. Data indicate that the higher amount of DM-myofibrils in pimelodids might result in stronger muscle contractions and, presumably, in higher sound intensities. The fine structure of the TT reveals that contractions most likely prevent transmission of swimbladder vibrations to the inner ear via the Weberian ossicles during vocalization.

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Quantitation of Ca ATPase, feet and mitochondria in superfast muscle fibres from the toadfish,Opsanus tau

Cited by 91 publications

References 33 publications

The whistle and the rattle: the design of sound producing muscles.

The whistle and the rattle: the design of sound producing muscles.

Relationships between enzymatic flux capacities and metabolic flux rates: Nonequilibrium reactions in muscle glycolysis

Sound‐generating and ‐detecting motor system in catfish: Design of swimbladder muscles in doradids and pimelodids

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