Skip to main content
SpringerLink
Log in

Morphological changes in the triads and sarcoplasmic reticulum of rat slow and fast muscle fibres following denervation and immobilization

  • Papers
  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Summary

We observed the morphological features of the membrane systems (sarcoplasmic reticulum, transverse tubules and triads) involved with the excitation-contraction coupling in rat soleus and extensor digitorum longus muscle following two disuse protocols: denervation and immobilization. The immobilized positions were: maximum dorsal flexor (soleus were stretched and extensor digitorum longus were shortened), maximum plantar flexor (soleus were shortened and extensor digitorum longus were stretched), and midway between the dorsal flexor and plantar flexor. The arrangement of the membrane systems was disordered following both disuse conditions. Increases in transverse tubule network were apparent; there were clearly more triads than in normal fibres, and pentadic and heptadic structures (i.e., a close approximation of two or three transverse tubule elements with three or four elements of terminal cisternae of sarcoplasmic reticulum) were frequently appeared following both denervation and immobilization. The most notable difference between the influence of denervation and immobilization on the membrane systems is the time at which the pentads and heptads appeared. They appeared much earlier (1 week after denervation) in denervated than in immobilized (3 or 4 weeks after immobilization) muscle fibres. On the other hand, the frequency of pentads and heptads is clearly related to the fibre type (significantly higher in extensor digitorum longus) and to extent of atrophy. The different influences of immobilization in each leg position suggest that disuse, but with neurotrophic factor(s), influences on the membrane systems were affected by sarcomere length, and the neurotrophic factor(s) and muscle activity were not always necessary to form mew membrane systems in disuse skeletal muscle fibres.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • AL-AMOOD, W. S. & LEWIS, D. M. (1989) A comparison of the effects of denervation on the mechanical properties of rat and guinea-pig skeletal muscle. J. Physiol. 414, 1–16.

    Google Scholar 

  • ALWAY, S. E. (1991) Perpetuation of muscle fibres after removal of stretch in the Japanese quail. Am. J. Physiol. 260 (Cell Physiol. 29), C400–8.

    Google Scholar 

  • ALWAY, S. E. (1994) Force and contractile characteristics after stretch overload in quail anterior latissimus dorsi muscle. J. Appl. Physiol. 77, 135–41.

    Google Scholar 

  • AXELSSON, J. & THESLEFF, S. (1959) A study of super-sensitivity in denervated mammalian skeletal muscle. J. Physiol. 147, 178–93.

    Google Scholar 

  • BOOTH, F. W. (1977) Time course of muscular atrophy during immobilization of hindlimbs in rats. J. Appl. Physiol. 43, 656–61.

    Google Scholar 

  • BOOTH, F. W. (1982) Effect of immobilization on skeletal muscle. J. Appl. Physiol. 52, 1113–18.

    Google Scholar 

  • BOOTH, F. W. & KELSO, J. R. (1973) Production of rat muscle atrophy by cast fixation. J. Appl. Physiol. 34, 404–6.

    Google Scholar 

  • BRENNER, H. R. & RUDIN, W. (1989) On the effect of muscle activity on the end-plate membrane in denervated mouse muscle. J. Physiol. 410, 501–12.

    Google Scholar 

  • DULHUNTY, A. F., GAGE, P. W. & VALOIS, A. A. (1984) Indentation in the terminal cisternae of denervated rat EDL and soleus muscle fibres. J. Ultrastruct. Res. 88, 30–43.

    Google Scholar 

  • EDGE, M. B. (1970) Development of apposed sarcoplasmic reticulum at the T system and sarcolemma and the change in orientation of triads in rat skeletal muscle. Dev. Biol. 28, 634–59.

    Google Scholar 

  • EDGERTON, V. R., BARNARD, R. J., PETER, J. B., MAIER, A. & SIMPSON, D. R. (1975) Properties of immobilized hindlimb muscles of the Galago senegalensis. Exp. Neurol. 46, 115–31.

    Google Scholar 

  • EISENBERG, B. R. & SALMONS, S. (1981) The reorganization of subcellular structure in muscle undergoing fast-to-slow type transformation. A stereological study. Cell Tissue Res. 220, 449–71.

    Google Scholar 

  • EISENBERG, B. R., BROWN, J. M. & 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.

    Google Scholar 

  • ENGEL, A. G. (1994) Quantitative morphological studies of muscle. In Myology (edited by ENGEL, A. G. & FRANZINI-ARMSTRONG, C.) pp. 1081–45. New York: McGraw-Hill, Inc.

    Google Scholar 

  • ENGEL, A. G. & BANKER, B. Q. (1994) Ultrastructural changes in diseased muscle. In Myology (edited by ENGEL, A. G. & FRANZINI-ARMSTRONG, C.) pp. 889–1071. New York: McGraw-Hill, Inc.

    Google Scholar 

  • ENGEL, A. G. & STONNINGTON, H. H. (1974) Morphorogical effects of denervation of muscle. A quantitative ultrastructural study. Ann. New York Acad. Sci. 228, 68–88.

    Google Scholar 

  • FINOL, H. J., LEWIS, D. M. & OWENS, R. (1981) The effects of denervation on contractile properties of rat skeletal muscle. J. Physiol. 319, 81–92.

    Google Scholar 

  • FITTS, R. H., METZGER, J. M., RILEY, D. A. & UNSWORTH, B. R. (1986) Models of disuse: a comparison of hindlimb suspension and immobilization. J. Appl. Physiol. 60, 1946–53.

    Google Scholar 

  • FISCHBACH, G. D. & ROBBINS, N. (1971) Effect of chronic disuse of rat soleus neuromuscular junctions on postsynaptic membrane. J. Neurophysiol. 34, 562–9.

    Google Scholar 

  • FLUCHER, B. E. (1992) Structural analysis of muscle development: transverse tubules, sarcoplasmic reticulum, and triad. Dev. Biol. 154, 245–60.

    Google Scholar 

  • FLUCHER, B. E., ANDREWS, S. B. & DANIELS, M. P. (1994) Molecular organization of transverse tubule/sarcoplasmic reticulum junctions during development of excitation-contraction coupling in skeletal muscle. Mol. Biol. Cell 5, 1105–18.

    Google Scholar 

  • FORBES, M. S., PLANTHOLT, B. A. & SPERELAKIS, N. (1977) Cytochemical staining procedures selective for sarcotubular systems of muscle: modification and applications. J. Ultrastruct. Res. 60, 306–27.

    Google Scholar 

  • FRANZINI-ARMSTRONG, C. (1991) Simultaneous maturation of transverse tubules and sarcoplasmic reticulum during muscle differentiation in the mouse. Dev. Biol. 146, 353–63.

    Google Scholar 

  • FRANZINI-ARMSTRONG, C. & JORGENSEN, A. O. (1994) Structure and development of E-C coupling units in skeletal muscle. Ann. Rev. Physiol. 56, 509–34.

    Google Scholar 

  • KELLY, A. M. (1969) The fine structure of skeletal muscle triads junctions. J. Ultrastruct. Res. 29, 37–49.

    Google Scholar 

  • HOLLY, R. G., BARNETT, J. G., ASHMORE, C. R., TAYLOR, R. G. & MOLE, P. A. (1980) Stretch-induced growth in chicken wing muscles: a new model of stretch hypertrophy. Am. J. Physiol. 238 (Cell Physiol. 7), C62–71.

    Google Scholar 

  • LI, C.-L., SHY, G. M. & WELLS, J. (1957) Some properties of mammalian skeletal muscle fibres with particular reference to fibrillation potentials. J. Physiol. 135, 522–35.

    Google Scholar 

  • MIDRIO, M., CALDESI-VALERI, V., PRINCI, T., RUZZIER, F. & VELUSSI, C. (1977) Differentiatial effects of disuse preceding denervation on the onset and development of fibrillation in fast and slow muscles. Experientia 33, 209–11.

    Google Scholar 

  • NUNZI, M. G. & FRANZINI-ARMSTRONG, C. (1980) Trabecular network in adult skeletal muscle. J. Ultrastruct. Res. 73, 21–6.

    Google Scholar 

  • PELLEGRINO, C. & FRANZINI-ARMSTRONG, C. (1969) 0 Recent contribution of electron microscopy to the study of normal and pathological muscle. In Int. Rev. Exp. Pathol. (edited by RICHTER, G. W. & EPSTEIN, M. A.) pp. 139–226. New York: Academic Press.

    Google Scholar 

  • PETTE, D. & VRBOVA, G. (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev. Physiol. Biochem. Pharmacol. 120, 115–202.

    Google Scholar 

  • SCHIAFFINO, S. & MARGRETH, A. (1969) Coordinated development of the sarcoplasmic reticulum and T system during postnatal differentiation of rat skeletal muscle. J. Cell Biol. 41, 855–75.

    Google Scholar 

  • SCHNEIDER, M. F. (1994) Control of calcium release in functioning skeletal muscle fibers. Ann. Rev. Physiol. 56, 463–84.

    Google Scholar 

  • SCHULTE, L., PETERS, D., TAYLOR, L., NAVARRO, J. & KANDARIAN, S. (1994) Sarcoplasmic reticulum Ca2+ pump expression in denervated skeletal muscle. Am. J. Physiol. 267 (Cell Physiol. 36), C617–22.

    Google Scholar 

  • SOMMER, J. R. & WAUGH, R. A. (1976) The ultrasracture of the mammalian cardiac muscle cell with special emphasis on the tubular membrane system. Am. J. Pathol. 82, 192–232.

    Google Scholar 

  • TAKEKURA, H., SHUMAN, H. & FRANZINI-ARMSTRONG, C. (1993) Differentiation of membrane systems during development of slow and fast skeletal muscle fibres in chicken. J. Muscle Res. Cell Motility 14, 633–45.

    Google Scholar 

  • TAKEKURA, H., SUN, X. & FRANZINI-ARMSTRONG, C. (1994) Development of the excitation-contraction coupling apparatus in skeletal muscle: peripheral and internal calcium release units are formed sequentially. J. Muscle Res. Cell Motility 15, 102–18.

    Google Scholar 

  • TAKEKURA, H., KASUGA, N. & YOSHIOKA, T. (1996) Influences of sarcomere length and selective elimination of myosin filaments for the localization and orientation of triads in rat muscle fibres. J. Muscle Res. Cell Motil. 17, 235–42.

    Google Scholar 

  • WALKER, S. M., SCHRODT, G. R. & BINGHAM, M. (1969) Evidence for connections of the sarcoplasmic reticulum with the sarcolemma and with the Z line in skeletal muscle fibers of fetal and newborn rats. Am. J. Phys. Med. 48, 63–77.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiological Sciences, National Institute of Fitness and Sports, 891-23, Kanoya, Kagoshima, Japan

    Hiroaki Takekura & Kohji Kitada

  2. Department of Health Sciences, Aichi University of Education, 448, Kariya, Aichi, Japan

    Norikatsu Kasuga

  3. Department of Physiology, St. Marianna University School of Medicine, 216, Kawasaki, Kanagawa, Japan

    Toshitada Yoshioka

Authors
  1. Hiroaki Takekura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Norikatsu Kasuga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kohji Kitada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Toshitada Yoshioka
    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

Takekura, H., Kasuga, N., Kitada, K. et al. Morphological changes in the triads and sarcoplasmic reticulum of rat slow and fast muscle fibres following denervation and immobilization. J Muscle Res Cell Motil 17, 391–400 (1996). https://doi.org/10.1007/BF00123356

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00123356

Keywords

Search

Navigation