Summary
Three different types of single living muscle fibre were dissected from the iliofibularis muscle ofXenopus laevis. The fibres were mounted in a glass chamber and their rate of oxygen consumption was determined as a function of twitch frequency at 20‡ C. The rate of oxygen consumption increased with twitch frequency until it levelled off and reached a maximum. The maximum rate of oxygen consumption varied between fibres (0.019 to 0.161 nmol O2 s−1 mm−3) and was reached at different twitch frequencies (<0.2 to 5.7 stimuli s−1). After the determination of the maximum rate of oxygen consumption, the succinate dehydrogenase activity in cross sections of the fibre was determined by means of a quantitative histochemical method. A proportional relationship between the maximum rate of oxygen consumption and the succinate dehydrogenase activity was found. The maximum rate of oxygen consumption and the succinate dehydrogenase activity are also proportional to the volume density of mitochrondria in the three fibre types reported by Smith and Ovalle (1973;J. Anat., Lond. 116, 1–24). It is concluded that quantitative histochemistry of succinate dehydrogenase reliably predicts the maximum rate of oxygen consumption of muscle fibres inXenopus laevis and that the maximum rate of oxygen consumption of single muscle fibres is determined by the volume density of mitochondria.
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References
Altman, F. P. (1977) Quantitative microscopy of enzyme reactions.Microsc. Acta 39, 327–34.
Arki, T., Chikamori, K., Sasaki, K., Kawata, S., Minami, S. &Yamada, M. (1987) Topographic estimations by component spectroanalysis of two formazans of nitroblue tetrazolium in tissue sections.Histochemistry 86, 567–72.
Blinks, J. R. (1965) Influence of osmotic strength on cross-section and volume of isolated single muscle fibres.J. Physiol, Lond. 177, 42–57.
Burke, R. E. (1981) Motor units: anatomy, physiology and functional organization. InHandbook of Physiology, The Nervous System, part 1 (edited byBrooks, V. B.) Vol. II, pp. 345–422. Bethesda MD: American Physiological Society.
Butcher, R. G. (1972) Precise cytochemical measurement of neotetrazolium formazan by scanning and integrating cytospectrophotometry.Histochemie 32, 171–90.
Crow, M. T. &Kushmerick, M. J. (1982) Chemical energetics of slow- and fast-twitch muscles of the mouse.J. gen. Physiol. 79, 147–66.
Diegenbach, P. C., Elzinga, G. &Van Der Laarse, W. J. (1988) Maximum rate of oxygen consumption correlates with succinate dehydrogenase activity of single muscle fibres inXenopus laevis. J. Physiol., Lond. 406, 43P.
Edman, K. A. P., Reggiani, C., Schiaffino, S. &Tekronnie, G. (1988) Maximum velocity of shortening related to myosin isoform composition in frog skeletal muscle fibres.J. Physiol., Lond. 395, 679–94.
Elzinga, G. &Van Der Laarse, W. J. (1988) Oxygen consumption of single muscle fibres ofRana temporaria andXenopus laevis at 20‡ C.J. Physiol., Lond. 399, 405–18.
Holloszy, J. O. &Coyle, E. F. (1984) Adaptations of skeletal muscle to endurance exercise and their metabolic consequences.J. appl. Physiol. 56, 831–8.
Hoppeler, H., Hudlicka, O. &Uhlman, E. (1987) Relationship between mitochondria and oxygen consumption in isolated cat muscles.J. Physiol., Lond. 385, 661–75.
Kimmich, H. P. &Kreuzer, F. (1969) Catheter PO2 electrode with low flow dependency and fast response.Progr. Resp. Res. 3, 100–10.
Kugelberg, E. &Lindgren, B. (1979) Transmission and contraction fatigue of rat motor units in relation to SDH activity of motor unit fibres.J. Physiol. Lond. 288, 285–300.
Kushmerick, M. J. (1983) Energetics of muscle contraction. InHandbook of Physiology, section 10, Skeletal Muscle (edited byPeachey, L. D., Adrian, R. H. &Geiger, S. R.), pp. 189–236. Bethesda, MD: American Physiological Society.
LÄnnergren, J. &Hoh, J. F. Y. (1984) Myosin isoenzymes in single muscle fibres ofXenopus laevis: Analysis of five different functional types.Proc. R. Soc. B222, 401–8.
LÄnnergren, J. &Smith, R. S. (1966) Types of muscle fibres in toad skeletal muscle.Acta Physiol. Scand. 68, 263–74.
Pearse, A. G. E. (1980)Histochemistry, Theoretical and Applied. 4th edn pp. 38–44. Edinburgh, London, New York: Churchill Livingstone.
Pette, D., Klingenberg, M. &Bücher, T. H. (1962) Comparable and specific proportions in mitochondrial enzyme activity pattern.Biochem. Biophys. Res. Commun.7, 425–29.
Pool, C. W., Diegenbach, P. C. &Scholten, G. (1979) Quantitative succinate dehydrogenase histochemistry. I. A methodological study on mammalian and fish muscle.Histochemistry 64, 251–62.
Reichmann, H., Hoppeler, H., Mathieu-Costello, O., Von Bergen, F. &Pette, D. (1985) Biochemical and ultrastructural changes of skeletal muscle mitochondria after chronic electrical stimulation in rabbits.Pflügers Arch. ges. Physiol. 404, 1–9.
Saltin, B. &Gollnick, P. D. (1983) Skeletal muscle adaptability: significance for metabolism and performance. InHandbook of Physiology, section 10, Skeletal Muscle (edited byPeachey, L. D., Adrian, R. H. &Geiger, S. R.), 189–236. Bethesda, MD: American Physiological Society.
Schmalbruch, H. (1985)Handbook of Microscopic Anatomy 11/6, Skeletal Muscle, pp. 159–238. Berlin, Heidelberg, New York, Tokyo: Springer Verlag.
Sieck, G. C., Sacks, R. D., Blanco, C. E. &Edgerton, V. R. (1986) SDH activity and cross-sectional area of muscle fibres in cat diaphragm.J. appl. Physiol. 60, 1284–92.
Smith, R. s. &Ovalle, W. K. (1973) Varieties of fast and slow extrafusal fibres in amphibian hind limb muscles.J. Anat., Lond. 116, 1–24.
Sokal, R. R. &Rohlf, F. J. (1981)Biometry, 2nd edn, pp. 454–91. San Fransisco: W. H. Freeman and Company.
Sperry, D. G. (1981) Fibre type composition and postmetamorphic growth of anuran hindlimb muscles.J. Morph. 170, 321–45.
Swatland, H. J. (1984) The radial distribution of succinate dehydrogenase activity in porcine muscle fibres.Histochem. J. 16, 321–9.
Van Der Laarse, W. J. &Diegenbach, P. C. (1988) Method of quenching of muscle fibres affects apparent succinate dehydrogenase activity.Histochem. J. 20, 642–4.
Van Der Laarse, W. J., Diegenbach, P. C. &Maslam, S. (1984) Quantitative histochemistry of three mouse hindlimb muscles: the relationship between calcium-stimulated myofibrillar ATPase and succinate dehydrogenase activities.Histochem. J. 16, 529–41.
Van Der Laarse, W. J., Diegenbach, P. C. &Hemminga, M. A. (1986) Calcium-stimulated myofibrillar ATPase activity correlates with shortening velocity of muscle fibres inXenopus laevis.Histochem. J. 18, 487–96.
Van Noorden, C. J. F., Tas, J. &Sanders, J. A. H. (1981) Quantitative aspects of the cytochemical demonstration of glucose-6-phosphate dehydrogenase with tetrazolium salts studied in a model system of polyacrylamide films.Acta Histochem. Suppl.24, 231–6.
Van Noorden, C. J. F., Tas, J. &Vogels, I. M. C.(1983) Cytophotometry of glucose-6-phosphate dehydrogenase activity in individual cells.Histochem. J. 15, 583–99.
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Van Der Laarse, W.J., Diegenbach, P.C. & Elzinga, G. Maximum rate of oxygen consumption and quantitative histochemistry of succinate dehydrogenase in single muscle fibres ofXenopus laevis . J Muscle Res Cell Motil 10, 221–228 (1989). https://doi.org/10.1007/BF01739812
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DOI: https://doi.org/10.1007/BF01739812