Skip to main content
SpringerLink
Log in

Ultrastructural comparison of slack and stretched myotendinous junctions, based on a three-dimensional model of the connecting domain

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

Summary

The vertebrate myotendinous junction contains junctional microfibrils, located in the lamina lucida of the basement membrane. The junctional microfibrils are thought to transmit muscular force across the junctional lamina lucida, also called the connecting domain. If true, deformation of the terminal muscle cell processes and connecting domain during force transmission would be detected as a change in spacing and/or orientation of the junctional microfibrils. This study compared connecting domain morphology in frog semitendinosus muscles fixed in two extremes of resting tension, to elucidate the mechanical properties of the myotendinous junction. An initial study of connecting domain ultrastructure revealed that junctional microfibrils are punctate or spinelike in shape, and that they are distributed in a linear, helically-oriented array on the muscle cell surface. The rows in the surface lattice are 10–15 nm in thickness, have a centre-to-centre distance between rows of approximately 24 nm, and are oriented at approximately 41o with respect of the long axis of the muscle fibre. Comparison of slack and highly stretched myotendinous junctions shows no significant changes in spacing or orientation of either individual junctional microfibrils or rows in the helical surface lattice. Thus, both the connecting domain and terminal cell processes at the myotendinous junction are essentially inextensible under the loading conditions used in this study.

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

  • Ajiri, T., Kimura, T., Ito, R. & Inokuchi, S. (1978) Microfibrils in the myotendon junctions. Acta Anat. 102, 433–9.

    Google Scholar 

  • Bartels, H. (1986) Myomuscular junctions in the gill-sac muscle of the atlantic hagfish, Myxine glutinosa: analogy with myotendinous junctions. Cell Tissue Res. 246, 223–5.

    Google Scholar 

  • Bartels, H. (1987) Intramembrane aspects of myotendinous and myomuscular junctions: a freeze-fracture study of the gill sac-muscle of the atlantic hagfish, Myxine glutinosa. Anat. Rec. 218, 249–55.

    Google Scholar 

  • Bonilla, E. (1983) Ultrastructural study of the muscle cell surface. J. Ultrastruct. Res. 82, 341–5.

    Google Scholar 

  • Byers, T. J., Kunkel, L. M. & Watkins, S. C. (1991) The subcellular distribution of dystrophin mouse skeletal, cardiac and smooth muscle. J. Cell Biol. 115, 411–21.

    Google Scholar 

  • Draper, M. H. & Hodge, A. J. (1949) Studies on muscle with the electron microscope. 1. The ultrastructure of toad striated muscle. Austr. J. Exper. Biol. Med. Sci. 27, 465–503.

    Google Scholar 

  • Eisenberg, B. R. & Milton, R. L. (1984) Muscle fiber termination at the tendon in the frog's sartorius: a stereological study. Am. J. Anat. 171, 273–84.

    Google Scholar 

  • Gordon, A. M., Huxley, A. F. & Julian, F. J. (1966) Tension development in highly stretched vertebrate muscle fibres. J. Physiol. 184, 143–69.

    Google Scholar 

  • Hanak, H. & Bock, P. (1971) Die feinstruktur der muskel-sehnen-verbindung von skelett- und herzmuskel. J. Ultrastruct. Res. 36, 68–85.

    Google Scholar 

  • Horwitz, A., Dugan, K., Buck, C., Beckerle, M. C. & Burridge, K. (1986) Interaction of plasma membrane fibronectin receptor with talin—a transmembrane linkage. Nature 320, 531–3.

    Google Scholar 

  • Huxley, A. F. & Peachey, L. D. (1961) The maximum length for contraction in vertebrate striated muscle. J. Physiol. 156, 150–65.

    Google Scholar 

  • Ibraghimov-Beskrovnaya, O., Ervasti, J. M., Leveille, C. J., Slaughter, C. A., Sernett, S. W. & Campbell, K. P. (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355, 696–702.

    Google Scholar 

  • Ishikawa, H. (1965) The fine structure of myo-tendon junction in some mammalian skeletal muscles. Arch. Histol. Jap. 25, 275–96.

    Google Scholar 

  • Korneliussen, H. (1973) Ultrastructure of myotendinous junctions in Myxine and rat: specializations between plasma membrane and the lamina densa. Z. Anat. Entwick.-Gesch. 142, 91–104.

    Google Scholar 

  • Mackay, B., Harrop, T. J. & Muir, A. R. (1969) The fine structure of the muscle tendon junction in the rat. Acta Anat. 73, 588–604.

    Google Scholar 

  • Magid, A. & Law, D. J. (1985) Myofibrils bear most of the resting tension in frog skeletal muscle. Science 230, 1280–2.

    Google Scholar 

  • Mair, W. G. P. & Tomé, F. M. S. (1972) The ultrastructure of the adult and developing human myotendinous junction. Acta Neuropath. (Berlin). 21, 239–52.

    Google Scholar 

  • Nakao, T. (1976) Some observations on the fine structure of the myotendinous junction in myotomal muscles of the tadpole tail. Cell Tissue Res. 166, 241–54.

    Google Scholar 

  • Podolsky, R. J. (1964) The maximum sarcomere length for contraction of isolated myofibrils. J. Physiol. 170, 110–23.

    Google Scholar 

  • Ramsey, R. W. & Street, S. F. (1940) The isometric length-tension diagram of isolated skeletal muscle fibers of the frog. J. Cell. Comp. Physiol. 15, 11–34.

    Google Scholar 

  • Rapoport, S. I. (1972) Mechanical properties of the sarcolemma and myoplasm in frog muscle as a function of sarcomere length. J. Gen. Physiol. 59, 559–85.

    Google Scholar 

  • Rapoport, S. I. (1973) The anisotropic elastic properties of the sarcolemma of the frog semitendinosus muscle fiber. Biophys. J. 13, 14–36.

    Google Scholar 

  • Reedy, M. K., Goody, R. S., Hofmann, W. & Rosenbaum, G. (1983) Co-ordinated electron microscopy and X-ray studies of glycerinated insect flight muscle. I. X-ray diffraction monitoring during preparation for electron microscopy of muscle fibres fixed in rigor, in ATP and AMPPNP. J. Muscle Res. Cell Motil. 4, 25–53; 64.

    Google Scholar 

  • Reedy, M. C., Reedy, M. K. & Tregear, R. T. (1988) Two attached non-rigor crossbridge forms in insect flight muscle. J. Mol. Biol. 204, 357–83.

    Google Scholar 

  • Samitt, C. E. & Bonilla, E. (1990) Immunocytochemical study of dystrophin at the myotendinous junction. Muscle Nerve 13, 493–500.

    Google Scholar 

  • Schmalbruch, H. (1974) The sarcolemma of skeletal muscle fibres as demonstrated by a replica technique. Cell Tissue Res. 150, 377–87.

    Google Scholar 

  • Schwarzacher, H. G. (1960) Untersuchungen uber die skelet-muskel-sehnenverbindung. I. Elektronenmikroskopische und lichtmikroskopische untersuchungen uber den feinbau der muskelfaser-sehnenverbindung. Acta Anat. 40, 59–86.

    Google Scholar 

  • Shear, C. R. & Bloch, R. J. (1985) Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures. J. Cell Biol. 101, 240–56.

    Google Scholar 

  • Shimizu, T., Matsumura, K., Sunada, Y. & Mannen, T. (1989) Dense immunostainings on both neuromuscular and myotendon junctions with an anti-dystrophin monoclonal antibody. Biomed. Res. 10, 405–409.

    Google Scholar 

  • Small, J. V. (1968) Measurement of section thickness. In Proceedings of the 4th European Regional Conference (Rome) on Electron Microsocopy (edited by Bocciarelli, D. S.) pp. 609–10. Rome: Tipografia Poliglotta Vaticana.

    Google Scholar 

  • Sten-Knudsen, O. (1953) Torsional elasticity of the isolated cross striated muscle fibre. Acta Physiol. Scand. 28 (Suppl.), 104.

    Google Scholar 

  • Tidball, J. G. (1983) The geometry of actin filament-membrane associations can modify adhesive strength of the myotendinous junction. Cell Motil. 3, 439–47.

    Google Scholar 

  • Tidball, J. G. (1984) Myotendinous junction: morphological changes and mechanical failure associated with muscle cell atrophy. Exp. Mol. Path. 40, 1–12.

    Google Scholar 

  • Tidball, J. G. & Daniel, T. L. (1986) Myotendinous junctions of tonic muscle cells: structure and loading. Cell Tissue Res. 245, 315–22.

    Google Scholar 

  • Tidball, J. G., O'Halloran, T. & Burridge, K. (1986) Talin at myotendinous junctions. J. Cell Biol. 103, 1465–72.

    Google Scholar 

  • Trotter, J. A. & Baca, J. M. (1987) The muscle-tendon junctions of fast and slow fibres in the garter snake: ultrastructural and stereological analysis and comparison with other species. J. Muscle Res. Cell Motil.. 8, 517–26.

    Google Scholar 

  • Trotter, J. A., Corbett, K. & Avner, B. P. (1981) Structure and function of the murine muscle-tendon junction. Anat. Rec. 201, 293–302.

    Google Scholar 

  • Trotter, J. A., Eberhard, S. & Samora, A. (1983a) Structural domains of the muscle-tendon junction. 1. The internal lamina and the connecting domain. Anat. Rec. 207, 573–91.

    Google Scholar 

  • Trotter, J. A., Eberhard, S. & Samora, A. (1983b) Structural connections of the muscle-tendon junction. Cell Motil. 3, 431–8.

    Google Scholar 

  • Trotter, J. A., HSI, K., Samora, A. & Wofsy, C. (1985) A morphometric analysis of the muscle-tendon junction. anat. Rec. 213, 26–32.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell Biology, Duke University Medical Center, 27710, Durham, NC, USA

    Douglas J. Law

Authors
  1. Douglas J. Law
    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

Law, D.J. Ultrastructural comparison of slack and stretched myotendinous junctions, based on a three-dimensional model of the connecting domain. J Muscle Res Cell Motil 14, 401–411 (1993). https://doi.org/10.1007/BF00121291

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00121291

Keywords

Search

Navigation