Skip to main content

Discrimination between fast- and slow-twitch fibres of guinea pig skeletal muscle using the relative surface density of junctional transverse tubule membrane

Journal of Muscle Research & Cell Motility volume 9, pages 403–414 (1988)Cite this article

Summary

The black reaction of Golgi was used to infiltrate transverse (T) tubules in fast-twitch glycolytic (FW), fast-twitch oxidative-glycolytic (FR) and slow-twitch (S) type fibres in muscles of guinea pigs. Non-junctional (fT) and junctional (jT) segments of the T-rubule network are clearly demarcated by this technique. Digitized planimetry and direct measurements were used to determine the proportion of T-tubule network forming junctions with the sarcoplasmic reticulum (%L jT ) and to estimate the surface density (surface area per fibre volume) of total and junctional T membrane. From these data, the volume density (number per fibre volume) of junctional feet was calculated. All three types of fibres have approximately equal surface density of T tubules, but the FW and FR fibres have a much higher proportion of jT. The calculated volume density of feet is twice as high in fast-twitch as in slow-twitch fibres.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Akster, H. A. (1985) Morphometry of muscle fiber types in the carp (Cyprinus carpio, L.). Relationship between structural and contractile characteristis.Cell Tissue Res. 241, 193–201.

    PubMed  Google Scholar 

  • Akster, H. A., Granzier, H. L. M. &Ter Keurs, H. E. D. J. (1985) A comparison of quantitative ultrastructural and contractile characteristics of muscle fiber types of the perchPerca fluviatilis.J. Comp. Physiol. 155, 685–91.

    Google Scholar 

  • Ariano, M. A., Armstrong, R. B. &Edgerton, V. R. (1973) Hindlimb muscle fiber populations of five mammals.J. Histochem. Cytochem. 21, 51–5.

    PubMed  Google Scholar 

  • Burke, R. E. (1986) Physiology of motor units. InMyology (edited byEngel, A. G. &Banker, B. Q.), Vol. 1, pp. 419–43. New York: McGraw-Hill.

    Google Scholar 

  • Burke, R. E., Levine, D. N., Tsairis, P. &Zajac., F. E. (1973) Physiological types and histochemical profiles in motor units of the cat gastrocnemiusJ. Physiol. (Lond). 234, 723–48.

    Google Scholar 

  • Burke, R. E. &Tsairis, P. (1974) The correlation of physiological properties with histochemical characteristics in single muscle units.Ann. N.Y. Acad. Sci. 228, 145–59.

    PubMed  Google Scholar 

  • Campbell, K. P., Sharp, A., Strom, M. &Kahl, S. D. (1987) Identification and characterization of the high affinity [3H]ryanodine receptor of the junctional sarcoplasmic reticulum Ca2+ release channelJ. biol. Chem. 262, 6460–3.

    PubMed  Google Scholar 

  • Cullen, M. J., Hollingworth, S. &Marshall, M. W. (1984) A comparative study of the transverse tubular system of the rat extensor digitorum longus and soleus muscles.J. Anat. 138, 297–308.

    PubMed  Google Scholar 

  • Dulhunty, A. F., Gage, P. W. &Lamb, G. D. (1986) Differential effects of thyroid hormone on T-tubules and terminal cisternae in rat muscles: an electrophysiological and morphometric analysis.J. Musc. Res. Cell Motility 7, 225–36.

    Google Scholar 

  • Dulhunty, A. F. &Valois, A. A. (1983) Indentations in the terminal cisternae of amphibian and mammalian skeletal muscle fibers.J. Ultrastruct. Res. 84, 34–49.

    PubMed  Google Scholar 

  • Edstrom, L. &Kugelberg, E. (1968) Histochemical composition, distribution of fibres and fatiguability of single motor units.J. Neurol. Neurosurg. Psychiat. 31, 424–33.

    PubMed  Google Scholar 

  • Eisenberg, B. R. (1983) Quantitative ultrastructure of mammalian skeletal muscle. InHandbook of Physiology: Section 10, Skeletal Muscle (edited byPeachey, L. D., Adrian, R. H. &Geiger, S. R.), pp. 73–112. Bethesda, MD: American Physiological Society.

    Google Scholar 

  • Eisenberg, B. R., Brown, J. M. C. &Salmons, S. (1984) Restoration of fast muscle characteristics following cessation of chronic stimulation. The ultrastructure of slow-to-fast transformation.Cell Tissue Res. 238, 221–30.

    PubMed  Google Scholar 

  • Eisenberg, B. R. &Kuda, A. M. (1975) Stereological analysis of mammalian skeletal muscle. II. White vastus muscle of the adult guinea pig.J. Ultrastruct. Res. 51, 176–87.

    PubMed  Google Scholar 

  • Eisenberg, B. R. &Kuda, A. M. (1976) Discrimination between fiber populations in mammalian skeletal muscle by using ultrastructural parameters.J. Ultrastruct. Res. 54, 76–88.

    PubMed  Google Scholar 

  • Eisenberg, B. R. &Salmons, S. (1981) The reorganization of subcellular structure in muscle undergoing the slow-to-fast type transformation.Cell Tissue Res. 220, 449–71.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Eisenberg, B. R., Dix, D. J., Lin, Z. W. &Wenslroth, M. P. (1987) Relationship of membrane systems in muscle to isomyosin contentCan.J. Physiol. Pharmacol. 65, 598–605.

    Google Scholar 

  • Ferguson, D. G. &Franzini-Armstrong, C. (1988) The Ca2+ ATPase content of slow and fast twitch fibers of guinea pig.Muscle & Nerve. 11, 561–70.

    Google Scholar 

  • Franzini-Armstrong, C. (1976) The comparative structure of intracellular junctions in striated muscle fibers. InPathogenesis of Human Muscular Dystrophies (edited byRowland, L. P.), pp. 612–25. Amsterdam: Excerpta Medica.

    Google Scholar 

  • Franzini-Armstrong, C., Gilly, W. F. &Aladjem, E. (1987) Golgi stain identifies three types of fibers in fish muscle.J. Musc. Res. Cell Motility,8, 418–27.

    Google Scholar 

  • Franzini-Armstrong, C. &Peachey, L. D. (1982) A modified Golgi black reaction method for light and electron microscopy.J. Histochem. Cytochem. 30, 99–105.

    PubMed  Google Scholar 

  • Gauthier, G. F. (1969) On the relationship of ultrastructural and cytochemical features to color in mammalian skeletal muscleZ. Zellforsch. 95, 462–82.

    PubMed  Google Scholar 

  • Gauthier, G. F. (1979) Ultrastructural identification of muscle fiber types by immunocytochemistry.J. Cell Biol. 82, 391–400.

    PubMed  Google Scholar 

  • Gillepsie, C. A., Simpson, D. R. &Edgerton, V. R. (1970) High glycogen content of red as opposed to white skeletal muscle fibers of guinea pig.J. Histochem. Cytochem. 18, 552–8.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Henneman, E., Somjen, G. &Carpenter, D. D. (1965) Functional significance of cell size in spinal motoneurones.J. Neurophysiol. 28, 560–80.

    PubMed  Google Scholar 

  • Inui, M., Saito, A. &Fleischer, S. (1987) Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle.J. Biol. Chem. 262, 1740–1.

    PubMed  Google Scholar 

  • Ishikawa, H. &Tsukita, S. (1983) High voltage electron microscopy of the T system in the mouse diaphragm. InMuscular Dystrophy: Biomedical Aspects (edited byEbashi, S. &Ozawa, E.), pp. 167–76. Berlin: Springer Verlag.

    Google Scholar 

  • Kugelberg, E. &Thornell, L-E. (1983) Contraction time, histochemical type and terminal cisternae volume of rat motor units.Muscle & Nerve 6, 149–53.

    Google Scholar 

  • Lai, F. A., Erickson, H., Block, B. A. &Meissner, G. (1987) Evidence for a junctional feet-ryanodine receptor complex from sarcoplasmic reticulum.Biochem. biophys. Res Commun. 143, 704–9.

    PubMed  Google Scholar 

  • Lowry, O. H., Lowry, C. V., Chi, M. M-Y., Hintz, C. S. &Felder, S. (1980) Enzymological heterogeneity of human muscle fibers. InPlasticity of Muscle (edited byPette, D. pp. 3–18. Berlin: deGruyter.

    Google Scholar 

  • Luff, A. R. &Atwood, H. (1971) Changes in the sarcoplasmic reticulum and transverse tubule system of fast and slow skeletal muscle of the mouse during post-natal development.J. Cell Biol. 51, 369–83.

    PubMed  Google Scholar 

  • Lyons, G. E., Kelly, A. M. &Rubinstein, N. A. (1986) Testosterone-induced changes in contractile protein isoforms in the sexually dimorphic temporalis muscle of the guinea pig.J. Biol. Chem. 261, 13278–84.

    PubMed  Google Scholar 

  • Nemeth, P., Pette, D. &Vrbova, G. (1980) Malate dehydrogenase homogeneity of single fibers of the motor unit. InPlasticity of Muscle (edited byPette, D.), pp. 45–54. Berlin: Walter de Gruyter Co.

    Google Scholar 

  • Nemeth, P. M., Pette, D. &Vrbova, G. (1981) Comparison of enzyme activities among single muscle fibres within defined motor units.J. Physiol (Lond.) 311, 489–95.

    Google Scholar 

  • Nemeth, P. M., Solanki, L., Gordon, D. A., Hamm, T. M., Reinking, R. M. &Stuart, D. G. (1986) Uniformity of metabolic enzymes within individual motor units.J. Neurosci. 6, 892–8.

    PubMed  Google Scholar 

  • Nemeth, P. M. &Turk, W. R. (1984) Biochemistry of rat single muscle fibre in newly assembled motor units following nerve crush.J. Physiol. (Lond.) 355, 547–55.

    Google Scholar 

  • Pellegrino, C. &Franzini, C. (1963) An electron microscopic study of denervation atrophy in red and white skeletal muscle fibres.J. Cell Biol. 17, 327–49.

    Google Scholar 

  • Peter, J. B., Barnard, R. J., Edgerton, V. R., Gillepsie, C. A. &Stempel, K. E. (1972) Metabolic profiles of three fibre types of skeletal muscle in guinea pigs and rabbits.Biochemistry 11, 2627–33.

    PubMed  Google Scholar 

  • Schmalbruch, H. (1979) The membrane systems in different fibre types of the triceps surae muscle of cat.Cell Tissue Res.204, 187–200.

    PubMed  Google Scholar 

  • Sommer, J. R. &Johnson, E. A. (1979) Ultrastructure of cardiac muscle. InHandbook of Physiology, Section 2, The Cardiovascular System (edited byBerne, R. M. &Sperelakis, N.), Vol. 1. Bethesda, MD: The American Physiological Society.

    Google Scholar 

Download references

Author information

Affiliations

  1. Department of Anatomy, University of Pennsylvania, Philadelphia, PA, USA

    C. Franzini-Armstrong

  2. Department of Biology, University of Pennsylvania, Philadelphia, PA, USA

    C. Franzini-Armstrong, D. G. Ferguson & C. Champ

  3. Department of Physiology and Biophysics, University of Cincinnati, College of Medicine, 45267-0576, Cincinnati, OH, USA

    D. G. Ferguson

Authors
  1. C. Franzini-Armstrong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. G. Ferguson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Champ
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Franzini-Armstrong, C., Ferguson, D.G. & Champ, C. Discrimination between fast- and slow-twitch fibres of guinea pig skeletal muscle using the relative surface density of junctional transverse tubule membrane. J Muscle Res Cell Motil 9, 403–414 (1988). https://doi.org/10.1007/BF01774067

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01774067

Keywords

  • Sarcoplasmic Reticulum
  • Surface Density
  • Volume Density
  • Fibre Volume
  • Calculated Volume