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.
Similar content being viewed by others
References
Barany, M. (1967) ATPase activity of myosin correlated with speed of muscle shortening.J. gen. Physiol. 50, 197–216.
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.
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.
Brooke, M. H. &Kaiser, K. K. (1970a) Muscle fiber types: how many and what kind?Arch. Neurol. 23, 369–79.
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.
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.
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.
Burke, R. E. (1967) Motor unit types of cat triceps surae muscleJ. Physiol., Lond. 193, 141–60.
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.
Carlson, H. (1978a) Morphology and contraction properties of cat lumbar back muscles.Acta physiol. scand. 103, 180–97.
Carlson, H. (1978b) Histochemical fiber composition of lumbar back muscles in the cat.Acta physiol. scand. 103, 198–209.
Close, R. I. (1964) Dynamic properties of fast and slow skeletal muscles of the rat during development.J. Physiol., Lond. 173, 74–95.
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.
Close, R. I. (1972) Dynamic properties of mammalian skeletal muscles.Physiol. Rev. 52, 129–97.
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.
Davies, A. S. &Dunn, H. M. (1972) Histochemical fiber types in the mammalian diaphragm.J. Anat. 112, 41–60.
Edgerton, V. R. &Simpson, D. R. (1969) The intermediate fiber of rats and guinea pigs.J. Histochem. Cytochem. 17, 828–38.
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.
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.
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.
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.
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.
Gauthier, G. F. (1967) On the localization of sarcotubular ATPase activity in mammalian skeletal muscle.Histochemie 11, 97–111.
Gauthier, G. F. &Lowey, S. (1977) Polymorphism of myosin among skeletal muscle fiber types.J. Cell Biol. 74, 760–79.
Gauthier, G. F., Lowey, S. &Hobbs, A. W. (1978) Fast and slow myosin in developing muscle fibres.Nature, Lond. 274, 25–9.
Gauthier, G. F. &Lowey, S. (1979) Distribution of myosin isoenzymes among skeletal muscle fiber types.J. Cell Biol. 81, 10–25.
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.
Gordon, G. &Phillips, C. G. (1949) Slow and rapid components in a flexor muscle.J. Physiol. 110, 6P.
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.
Hall-Craggs, E. C. B. (1968) The contraction times and enzyme activity of two rabbit laryngeal muscles.J. Anat. 102, 241–55.
Henneman, E. &Olson, C. B. (1965) Relations between structure and function in the design of skeletal muscle.J. Neurophysiol. 28, 581–98.
Layne, E. (1957) Spectrophotometric and turbidimetric methods for measuring proteins.Meth. Enzym. 3, 447–54.
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.
Lutz, H., Weber, H. &Jenny, E. (1979) Fast and slow myosin within single skeletal muscle fibers of adult rabbits.Nature, Lond. 281, 142–4.
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.
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.
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.
Murphy, R. A. &Beardsley, A. C. (1974) Mechanical properties of the cat soleus muscle in situ.Am. J. Physiol. 227, 1008–13.
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.
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.
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.
Ranatunga, K. W. (1979) Potentiation of the isometric twitch and mechanism of tension recruitment in mammalian skeletal muscle.Expl Neurol. 63, 266–76.
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.
Rockstein, M. &Herron, P. W. (1951) Colorimetric determination of inorganic phosphate in microgram quantities.Analyt. Chem. 23, 1500–1.
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.
Sartore, S., Pierobon-Bormioli, S. &Schiaffino, S. (1978) Immunochemical evidence of myosin polymorphism in the chicken heart.Nature, Lond. 274, 82–3.
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.
Wills, J. H. (1972) Speed of responses of various muscles of cats.Am. J. Physiol. 136, 623–8.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01005238