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Relationship among fibre type, myosin ATPase activity and contractile properties

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Summary

At least two types of skeletal muscle myosin have been described which differ in ATPase activity and stability in alkaline or acidic media. Differences in ATPase characteristics distinguish Type I and Type II fibres histochemically. In this study, ATPase activity of myosin from muscles of several species with known histochemical and contractile properties has been determined to test the hypothesis that (1) myosin ATPase activity, (2) histochemical determination of fibre types and (3) maximum shortening velocity, all provide equivalent estimates of contractile properties in muscles of mixed fibre types. Maximum shortening velocity appears to be proportional to ATPase activity as expected from previous reports by Barany. However, both myosin ATPase and the maximum shortening velocity exhibit curvilinear relationships to the fraction of cross-sectional area occupied by Type II fibres. Therefore, we reject the hypothesis and conclude that histochemically determined myofibrillar ATPase does not accurately reflect the intrinsic ATPase activity or shortening velocity in muscles of mixed fibre types. Our data are consistent with the presence of more than two myosin isozymes or with a mixture of isozymes within single muscle fibres.

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References

  • Barany, M. (1967) ATPase activity of myosin correlated with speed of muscle shortening.J. gen. Physiol. 50, 197–216.

    Google Scholar 

  • Barany, M. K., Barany, T., Reckard, T. &Volpe, A. (1965) Myosin of fast and slow muscles of the rabbit.Archs Biochem. Biophys. 109, 185–91.

    Google Scholar 

  • Barnard, R. M., Edgerton, V. R., Furakawa, T., Peter, J. B. (1971) Histochemical, biochemical and contractile properties of red, white and intermediate fibers.Am. J. Physiol. 220, 410–4.

    Google Scholar 

  • Brooke, M. H. &Kaiser, K. K. (1970a) Muscle fiber types: how many and what kind?Arch. Neurol. 23, 369–79.

    Google Scholar 

  • Brooke, M. H. &Kaiser, K. K. (1970b) Three ‘myosin adenosine triphosphatase’ systems: the nature of their pH lability and sulfhydryl dependence.J. Histochem. Cytochem. 18, 670–2.

    Google Scholar 

  • Buller, A. J., Eccles, J. C. &Eccles, R. M. (1960) Differentiation of fast and slow muscles in the cat hind limb.J. Physiol., Lond. 150, 399–416.

    Google Scholar 

  • Buller, A. J. &Lewis, D. M. (1965) Further observations on the differentiation of skeletal muscles in the kitten hind limb.J. Physiol., Lond. 176, 355–70.

    Google Scholar 

  • Burke, R. E. (1967) Motor unit types of cat triceps surae muscleJ. Physiol., Lond. 193, 141–60.

    Google Scholar 

  • Burke, R. E., Levine, P. N., Zajac, F. E. III, Tsairis, P. &Engel, W. K. (1971) Mammalian motor units: physiological correlates of three types in cat gastronemius.Science 174, 709–12.

    Google Scholar 

  • Carlson, H. (1978a) Morphology and contraction properties of cat lumbar back muscles.Acta physiol. scand. 103, 180–97.

    Google Scholar 

  • Carlson, H. (1978b) Histochemical fiber composition of lumbar back muscles in the cat.Acta physiol. scand. 103, 198–209.

    Google Scholar 

  • Close, R. I. (1964) Dynamic properties of fast and slow skeletal muscles of the rat during development.J. Physiol., Lond. 173, 74–95.

    Google Scholar 

  • Close, R. I. (1965) The relation between intrinsic speed of shortening and duration of the active state of muscle.J. Physiol., Lond. 180, 542–59.

    Google Scholar 

  • Close, R. I. (1972) Dynamic properties of mammalian skeletal muscles.Physiol. Rev. 52, 129–97.

    Google Scholar 

  • Cohen, D. M. &Murphy, R. A. (1978) Differences in cellular contractile protein contents among porcine smooth muscles. Evidence for variation in the contractile system.J. gen. Physiol. 72, 369–80.

    Google Scholar 

  • Davies, A. S. &Dunn, H. M. (1972) Histochemical fiber types in the mammalian diaphragm.J. Anat. 112, 41–60.

    Google Scholar 

  • Edgerton, V. R. &Simpson, D. R. (1969) The intermediate fiber of rats and guinea pigs.J. Histochem. Cytochem. 17, 828–38.

    Google Scholar 

  • Eisenberg, B. R. &Kuda, A. M. (1974a) Stereological analysis of mammalian skeletal muscle I. Soleus muscle of the adult guinea pig.J. Cell Biol. 60, 732–54.

    Google Scholar 

  • Eisenberg, B. R. &Kuda, A. M. (1974b) Stereological analysis of mammalian skeletal muscle II. White vastus muscle of the adult guinea pig.J. Cell Biol. 60, 755–65.

    Google Scholar 

  • Faulkner, J. A., Maxwell, L. C., Ruff, J. L. &White, T. P. (1979) The diaphragm as a muscle. Contractile properties.Ann. Rev. Respir. Disease 119, 89–92.

    Google Scholar 

  • Fitts, R. H. &Holloszy, J. O. (1977) Contractile properties of rat soleus muscle: effects of training and fatigue.Am. J. Physiol. Cell Physiol. 2, C86-C91.

    Google Scholar 

  • Fitts, R. H., Winder, W. W., Brooke, M. H., Kaiser, K. K. &Holloszy, J. O. (1980) Contractile, biochemical and histochemical properties of thyrotoxic rat soleus muscle.Am. J. Physiol. 238, C15-C20.

    Google Scholar 

  • Gauthier, G. F. (1967) On the localization of sarcotubular ATPase activity in mammalian skeletal muscle.Histochemie 11, 97–111.

    Google Scholar 

  • Gauthier, G. F. &Lowey, S. (1977) Polymorphism of myosin among skeletal muscle fiber types.J. Cell Biol. 74, 760–79.

    Google Scholar 

  • Gauthier, G. F., Lowey, S. &Hobbs, A. W. (1978) Fast and slow myosin in developing muscle fibres.Nature, Lond. 274, 25–9.

    Google Scholar 

  • Gauthier, G. F. &Lowey, S. (1979) Distribution of myosin isoenzymes among skeletal muscle fiber types.J. Cell Biol. 81, 10–25.

    Google Scholar 

  • Gonyea, W. &Bonde-Petersen, F. (1977) Contraction properties and fiber types of some forelimb and hind limb muscles in the cat.Expl Neurol. 57, 637–44.

    Google Scholar 

  • Gordon, G. &Phillips, C. G. (1949) Slow and rapid components in a flexor muscle.J. Physiol. 110, 6P.

    Google Scholar 

  • Guth, L., &Samaha, F. J. (1972) Erroneous interpretations which may result from application of the ‘myofibrillar ATPase’ histochemical procedure to developing muscle.Expl Neurol. 34, 465–76.

    Google Scholar 

  • Hall-Craggs, E. C. B. (1968) The contraction times and enzyme activity of two rabbit laryngeal muscles.J. Anat. 102, 241–55.

    Google Scholar 

  • Henneman, E. &Olson, C. B. (1965) Relations between structure and function in the design of skeletal muscle.J. Neurophysiol. 28, 581–98.

    Google Scholar 

  • Layne, E. (1957) Spectrophotometric and turbidimetric methods for measuring proteins.Meth. Enzym. 3, 447–54.

    Google Scholar 

  • Lieberman, D. A., Faulkner, J. A., Craig, A. B. Jr &Maxwell, L. C. (1973) Performance and histochemical composition of guinea pig and human diaphragm.J. appl. Physiol. 34, 233–7.

    Google Scholar 

  • Lutz, H., Weber, H. &Jenny, E. (1979) Fast and slow myosin within single skeletal muscle fibers of adult rabbits.Nature, Lond. 281, 142–4.

    Google Scholar 

  • Maxwell, L. C., Barclay, J. K., Mohrman, D. E. &Faulkner, J. A. (1977) Physiological characteristics of skeletal muscles of dogs and cats.Am. J. Physiol. 233, C14–8.

    Google Scholar 

  • Maxwell, L. C., Faulkner, J. A. &Lieberman, D. A. (1973) Histochemical manifestations of age and endurance training in skeletal muscle fibers.Am. J. Physiol. 344, 356–61.

    Google Scholar 

  • McCarter, R. D., Radicke, D. &Yu, B. P. (1977) A model preparation for studying fast mammalian skeletal muscles.Proc. Soc. exp. Biol. Med. 156, 40–5.

    Google Scholar 

  • Murphy, R. A. &Beardsley, A. C. (1974) Mechanical properties of the cat soleus muscle in situ.Am. J. Physiol. 227, 1008–13.

    Google Scholar 

  • Olson, C. B. &Swett, C. P. (1966) A functional and histochemical characterization of motor units in a heterogenous muscle (flexor digitorum longus) of the cat.J. Comp. Neurol. 128, 475–97.

    Google Scholar 

  • Pette, D., Vrbova, G. &Whalen, R. C. (1979) Independent development of contractile properties and myosin light chains in embryonic chick fast and slow muscle.Pflugers Arch. 378, 251–7.

    Google Scholar 

  • Pierobon-Bormioli, S., Sartore, S., Dalla Libera, L., Vitadello, M. &Schiaffino, S. (1981) Fast' isomyosins and fiber types in mammalian skeletal muscle.J. Histochem. Cytochem. 29, 1179–88.

    Google Scholar 

  • Ranatunga, K. W. (1979) Potentiation of the isometric twitch and mechanism of tension recruitment in mammalian skeletal muscle.Expl Neurol. 63, 266–76.

    Google Scholar 

  • Robbins, N., Karpati, G. &Engel, W. K. (1969) Histochemical and contractile properties in the cross innervated guinea pig soleus muscle.Arch. Neurol. 20, 318–26.

    Google Scholar 

  • Rockstein, M. &Herron, P. W. (1951) Colorimetric determination of inorganic phosphate in microgram quantities.Analyt. Chem. 23, 1500–1.

    Google Scholar 

  • Samaha, F. J., Guth, L. &Albers, R. W. (1970) Phenotypic differences between the actomyosin ATPase of the three fiber types of mammalian skeletal muscle.Expl Neurol. 26, 120–5.

    Google Scholar 

  • Sartore, S., Pierobon-Bormioli, S. &Schiaffino, S. (1978) Immunochemical evidence of myosin polymorphism in the chicken heart.Nature, Lond. 274, 82–3.

    Google Scholar 

  • Weeds, A. G., Hall, R. &Spurway, N. C. S. (1975) Characterization of myosin light chains from histochemically identified fibers of rabbit psoas muscle.FEBS Lett. 49, 320–4.

    Google Scholar 

  • Wills, J. H. (1972) Speed of responses of various muscles of cats.Am. J. Physiol. 136, 623–8.

    Google Scholar 

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Maxwell, L.C., Faulkner, J.A. & Murphy, R.A. Relationship among fibre type, myosin ATPase activity and contractile properties. Histochem J 14, 981–997 (1982). https://doi.org/10.1007/BF01005238

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