Energy liberation and chemical change in frog skeletal muscle during single isometric tetanic contractions.

Homsher, Earl; Rall, Jack A.; Wallner, A; Ricchiuti, N. V.

doi:10.1085/jgp.65.1.1

Cited by 45 publications

(42 citation statements)

References 8 publications

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“…It is well established that at the onset of contraction, fast-twitch fibers exhibit a high ATP turnover rate that decreases with time although force is maintained fairly constant (6,7,10,15,42). Similar results were obtained in the present study at higher temperature and lower relative forces.…”

Section: Discussionsupporting

confidence: 90%

Cross bridges account for only 20% of total ATP consumption during submaximal isometric contraction in mouse fast-twitch skeletal muscle

Zhang¹,

Andersson²,

Sandström³

et al. 2006

American Journal of Physiology-Cell Physiology

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It is generally believed that cross bridges account for >50% of the total ATP consumed by skeletal muscle during contraction. We investigated the effect of N-benzyl-p-toluene sulfonamide (BTS), an inhibitor of myosin ATPase, on muscle force production and energy metabolism under near-physiological conditions (50-Hz stimulation frequency at 30 degrees C results in 35% of maximal force). Extensor digitorum longus muscles from mice were isolated and stimulated to perform continuous isometric tetanic contractions. Metabolites of energy metabolism were analyzed with fluorometric techniques. ATP turnover was estimated from the changes in phosphocreatine (PCr), ATP, and lactate (-2DeltaATP - DeltaPCr + [1.5Deltalactate]). During contractions (2-10 s), BTS decreased force production to approximately 5% of control. Under these conditions, BTS inhibited ATP turnover by only 18-25%. ATP turnover decreased markedly and similarly with and without BTS as the duration of contraction progressed. In conclusion, cross bridges (i.e., actomyosin ATPase) account for only a small fraction (approximately 20%) of the ATP consumption during contraction in mouse fast-twitch skeletal muscle under near-physiological conditions, suggesting that ion pumping is the major energy-consuming process.

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Section: Discussionsupporting

confidence: 90%

Cross bridges account for only 20% of total ATP consumption during submaximal isometric contraction in mouse fast-twitch skeletal muscle

Zhang¹,

Andersson²,

Sandström³

et al. 2006

American Journal of Physiology-Cell Physiology

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“…The heat production in excess of that expected from PCr splitting which has been observed during rapid shortening (Rall et al 1976) occurred very early in the tetanus, when a similar 'unexplained' heat production is seen in isometric tetani (Gilbert, Kretzschmar, Wilkie & Woledge, 1971;Curtin & Woledge, 1979;Homsher, Kean, Wallner & Garibian-Sarian, 1979). This ambiguity may be removed by delaying the start of shortening until after 2 sec of isometric contraction, since heat plus work production 424 ENERGETICS OF MUSCLE SHORTENING from sources other than PCr splitting is insignificant after this time in R. pipiens muscles (as calculated by Curtin & Woledge (1978) from the results of Homsher, Rall, Wallner & Ricchiuti (1975) (Rall et al 1976).…”

Section: Introductionmentioning

confidence: 94%

“…These experiments were made over a time span of 9 weeks. The muscle pairs were mounted, thermally equilibrated at 0 'C, aerated, stimulated, and frozen using the hammer apparatus previously described (Homsher et al 1975). The length of the muscle of each pair used for laser diffraction was adjusted to that corresponding to a sarcomere length of 2-6 #m. The length of the contralateral muscle was then adjusted so that both muscles had the same resting tension (mean value 0 04 N).…”

Section: Introductionmentioning

confidence: 99%

“…The thermopile output was amplified by an Astrodata 120 nV amplifier. Calibration of heat values was as described by Homsher et al (1975) following the method of Hill & Woledge (1962). Heat loss from the muscles was exponential with time constants between 10 and 24 see and was determined by the Peltier method (Kretzschmar & Wilkie, 1972) at the muscle lengths used in the heat measurements; the time constants were consistently smaller at greater lengths.…”

Section: Introductionmentioning

confidence: 99%

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High‐energy phosphate metabolism and energy liberation associated with rapid shortening in frog skeletal muscle

Homsher

Irving

Wallner

1981

The Journal of Physiology

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SUMMARY1. High-energy phosphate metabolism and energy liberated as heat and work were measured in 3 sec tetani of frog sartorius muscles at 0 OC.2. Three contraction periods were studied: (a) shortening at near-maximum velocity for 0-3 sec from sarcomere length 2-6 to 18 sum, beginning after 2 sec of isometric stimulation, (b) the 0 7 sec isometric period immediately following such rapid shortening, (c) the period from 2 to 3 sec in an isometric tetanus at sarcomere length 1P8 um.3. There were no significant changes in levels of ATP, ADP or AMP in any contraction period. The observed changes in inorganic phosphate and creatine levels indicated that the only significant reaction occurring was phosphocreatine splitting.4. The mean rate of high-energy phosphate splitting during rapid shortening, 0-48 + 0-24 ,imole/g . sec (mean + S.E. of mean, n = 29; 'g' refers to blotted muscle weight), was not significantly different from that in the 1 sec period in the isometric tetanus, 0-32 +011 smole/g. sec (n = 17). The mean rate in the post-shortening period, 0 71 +0 10 ,umole/g . sec (n = 22), was greater than that in the 1 sec period in the isometric tetanus, and this difference is significant (P < 0-02, t test).5. A large quantity of heat plus work was produced during the rapid shortening period, but less than half of this could be accounted for by simultaneous chemical reactions. The unexplained enthalpy production was 6-5 + 26 mJ/g (mean +S.E. of mean). No significant unexplained enthalpy was produced in the 1 sec period in the isometric tetanus.6. In the post-shortening period the observed enthalpy was less, by 6-2 + 2-6 mJ/g, than that expected from the simultaneous chemical reactions.7. The results are interpreted in terms of an exothermic shift in the population of cross-bridge states during rapid shortening. It is suggested that a relatively slow subsequent step prevents many of these cross-bridges from completing the cycle and splitting ATP until after the end of shortening.

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“…The first concerns a substantial discrepancy between the enthalpy of PCr splitting measured by calorimetry, -8 kcal/mole (Woledge, 1972, see also Mar6chal, 1964) and the value obtained from measurements in muscle of the output of heat plus work divided by the PCr hydrolysed, -11 kcal/mole (Wilkie, 1968;Chaplain & Frommelt, 1972;Homsher, Rall, Wallner & Ricchiuti, 1975). The discrepancy continues and even increases throughout the course of a prolonged tetanus at 200 C (Canfield, Lebacq & Mar6chal, 1973).…”

Section: Introductionmentioning

confidence: 99%

Relationship between initial chemical reactions and oxidative recovery metabolism for single isometric contractions of frog sartorius at 0 degrees C.

Kushmerick¹,

Rutgeerts²

1976

The Journal of Physiology

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SUMMARY1. Measurements of initial chemical changes and recovery oxygen consumption (AG2) were made in unpoisoned aerobic frog sartorius muscles at 00 C to provide independent measures of the chemical energy used for isometric tetani of various durations.2. A02 was measured polarographically and increased in a curvilinear fashion with stimulus duration. For stimulations longer than 4 see AG2 was a linear function of the tension-time integral.3. Measurements of the changes in the content of phosphorylereatine, 'free' creatine and inorganic phosphate were made in muscles rapidly frozen during a tetanus. The average of these quantities, Ai P, was used to measure the initial 'high energy' phosphate utilization. No break-down of 'high-energy' phosphate compounds was detected up to 200 sec after relaxation of tension. Changes in the content of ATP were not observed except for a small decrease (-0 25 + 0.1 pumole/g) in muscles tetanized for 1 sec. 4. A ' P also increase curvilinearly with tetanus duration and, for tetanic durations greater than 4 sec, was a linear function of the tensiontime integral.5. Both A02 and A P were quantitatively related by a constant scaling factor of about 4'3 (A P/AG2) throughout the range of tetanic durations studied. The constancy of this ratio provides evidence against the hypothesis that a significant 'missing reaction' provides energy during any one portion of the tetanus. Several hypothesis may account for the numerical value of the ratio A P/A02.

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Energy liberation and chemical change in frog skeletal muscle during single isometric tetanic contractions.

Cited by 45 publications

References 8 publications

Cross bridges account for only 20% of total ATP consumption during submaximal isometric contraction in mouse fast-twitch skeletal muscle

Cross bridges account for only 20% of total ATP consumption during submaximal isometric contraction in mouse fast-twitch skeletal muscle

High‐energy phosphate metabolism and energy liberation associated with rapid shortening in frog skeletal muscle

Relationship between initial chemical reactions and oxidative recovery metabolism for single isometric contractions of frog sartorius at 0 degrees C.

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