Skip to main content
SpringerLink
Log in

Some observations on the fine structure of the myotendinous junction in myotomal muscles of the tadpole tail

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Myotendinous junctions in the myotomal tail muscles of the tadpole of Rana rugosa were examined by electron microscopy. At the site of the myotendinous junction, the sarcolemma is covered on its sarcoplasmic aspect by the connecting filament layer and the attachment layer, and on the extracellular aspect by the intermediary layer and the external lamina, with associated collagen fibrils. The intermediary layer consists of filamentous structures which closely resemble “microfibrils” (Hanak and Böck, 1971), “spine-like or thread-like profiles” (Korneliussen, 1973) and “intermediary layer” (Nakao, 1975a, b) in the myotendinous junctions of other vertebrate skeletal muscles.

Particularly interesting is the fact that all the coverings and linings of the sarcolemma, including the external lamina, are completely absent in the terminal segment of the finger-like sarcolemmal invagination characteristic of the myotendinous junction. Furthermore, special types of coupling between a sac of sarcoplasmic reticulum and a part of the sarcolemmal invagination are frequently observed. These couplings always occur along the region of the sarcolemma where the external lamina is absent. The couplings show features similar to those of the triad, such as “ SR feet ”, “scalloped SR membranes” and “granular content of the SR sac”, suggesting that they are analogous and functionally similar to the triad and other equivalent structures.

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

  • Bennett, H.S.: Modern concepts of structure of striated muscle. Amer. J. Phys. Med. 34, 46–67 (1955)

    Google Scholar 

  • Beringer, T., Hadek, R.: Ultrastructure of sinus venosus innervation in Petromyzon marinus. J. Ultrastruct. Res. 42, 312–323 (1973)

    Google Scholar 

  • Cavey, M.J., Cloney, R.A.: Fine structure and differentiation of ascidian muscle. I. Differentiated caudal musculature of Distaplia occidentalis tadpole. J. Morph. 138, 349–374 (1972)

    Google Scholar 

  • Cavey, M.J., Cloney, R.A.: Fine structure and differentiation of ascidian muscle. II. Morphometrics and differentiation of the caudal muscle cells of Distaplia occidentalis tadpoles. J. Morph. 144, 23–70 (1974)

    Google Scholar 

  • Couteaux, R.: Sur le mode de terminaison des myofibrilles et leurs connexions avec la membrane sarcoplasmique au niveau de la jonction musculotendineuse. C.R. Acad. Sci. (Paris) 246, 307–309 (1958)

    Google Scholar 

  • Couteaux, R.: Observations sur L-ultrastructure de la jonction musculotendineuse. C.R. Acad. Sci. (Paris) 249, 964–966 (1959)

    Google Scholar 

  • Devine, C.E., Somlyo, A.V., Somlyo, A.P.: Sarcoplasmic reticulum and excitation-contraction coupling in mammalian smooth muscles. J. Cell Biol. 52, 690–718 (1972)

    Google Scholar 

  • Edwards, G.A., Ruska, H., de Sonza, S.P., Vallejo-Freire, A.: Comparative cytophysiology of striated muscle with special reference to the role of the endoplasmic reticulum. J. biophys. biochem. Cytol. 2 (Suppl.), 143–156 (1956)

    Google Scholar 

  • Fawcett, D.W., McNutt, N.S.: The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J. Cell Biol. 42, 1–45 (1969)

    Google Scholar 

  • Forbes, M.S., Sperelakis, N.: Ultrastructure of lizard ventricular muscle. J. Ultrastruct. Res. 34, 439–451 (1971)

    Google Scholar 

  • Forbes, M.S., Sperelakis, N.: Spheroid bodies in the junctional sarcoplasmic reticulum of lizard myocardial cells. J. Cell Biol. 60, 602–615 (1974)

    Google Scholar 

  • Forssmann, W.G., Girardier, L.: A study of the T system in rat heart. J. Cell Biol. 44, 1–19 (1970)

    Google Scholar 

  • Franzini-Armstrong, C.: Studies of triad. I. Structure of the junction in frog twitch fibers. J. Cell Biol. 47, 488–499 (1970)

    Google Scholar 

  • Gelber, D., Moore, D.H., Ruska, H.: Observations of the myotendon junction in mammalian skeletal muscle. Z. Zellforsch. 52, 396–400 (1960)

    Google Scholar 

  • Gilai, A., Parnas, I.: Electromechanical coupling in tubular muscle fibers. I. The organization of tubular muscle fibers in the scorpion Leiurus quinquestriatus. J. Cell Biol. 52, 626–638 (1972)

    Google Scholar 

  • Hagiwara, S., Henkart, M.P., Kidokoro, Y.: Excitation-contraction coupling in Amphioxus muscle cells. J. Physiol. (Lond.) 219, 233–251 (1971)

    Google Scholar 

  • Hanak, H., Böck, P.: Die Feinstruktur der Muskel-Sehnenverbindung von Skelett- und Herzmuskel. J. Ultrastruct. Res. 36, 68–85 (1971)

    Google Scholar 

  • Ishikawa, H.: The fine structure of myo-tendon junction in some mammalian skeletal muscles. Arch, histol. jap. 25, 275–296 (1965)

    Google Scholar 

  • Jewett, P.H., Leonard, S.D., Sommer, J.R.: Chicken cardiac muscle. Its elusive extended junctional sarcoplasmic reticulum and sarcoplasmic reticulum fenestration. J. Cell Biol. 56, 595–600 (1973)

    Google Scholar 

  • Jewett, P.H., Sommer, J.R., Johnson, E.A.: Cardiac muscle. Its ultrastructure in the finch and hummingbird with special reference to the sarcoplasmic reticulum. J. Cell Biol. 49, 50–65 (1971)

    Google Scholar 

  • Johnson, E.A., Sommer, J.R.: A strand of cardiac muscle. Its ultrastructure and the electrophysiological implications of its geometry. J. Cell Biol. 3, 103–129 (1967)

    Google Scholar 

  • Kelly, D.E.: Fine structural analysis of muscle triad junctions. J. Cell Biol. 35 (2), 66 A (Abstract) (1967)

  • Kelly, D.E., Cahill, M.A.: Skeletal muscle triad junction fine structure; new observation regarding dimples of the sarcoplasmic reticulum terminal cisternae. J. Cell Biol. 43 (2), 66 A (Abstract) (1969)

  • Korneliussen, H.: Ultrastructure of myotendinous junctions in Myxine and rat. Specializations between the plasma membrane and the lamina densa. Z. Anat. Entwickl.-Gesch. 142, 91–101 (1973)

    Google Scholar 

  • Luft, J.H.: Ruthenium red staining of the striated muscle cell membrane and the myotendinous junction. In: Electron microscopy, vol. II, p. 65–66 (R. Uyeda, ed.). Tokyo: Maruzen Co., Ltd. 1966

    Google Scholar 

  • Luft, J.H.: Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat. Rec. 171, 369–416 (1971)

    Google Scholar 

  • Mackay, B., Muir, A.R., Peters, A.: Observations on the terminal innervation of segmental muscle fibers in Amphibia. Acta anat. (Basel) 40, 1–12 (1960)

    Google Scholar 

  • McNutt, N.S., Fawcett, D.W.: The ultrastructure of the cat myocardium. II. Atrial muscle. J. Cell Biol. 42, 46–67 (1969)

    Google Scholar 

  • Muir, A.R.: Observations on the attachment of myofibrils to the sarcolemma at the muscle-tendon junction. In: Electron microscopy in anatomy. (J.D. Boyd, F.R. Johnson and J.D. Lever, eds.), p. 267–277. Baltimore: The Williams and Wilkins Co. 1961

    Google Scholar 

  • Nakao, T.: Fine structure of the myotendinous junction and “terminal coupling” in the skeletal muscle of the lamprey, Lampetra japonica. Anat. Rec. 182, 321–338 (1975a)

    Google Scholar 

  • Nakao, T.: Some observations on the fine structure of the myotomes of larval lamprey, Lampetra japonica. Acta Anat. Nippon, (in press) (Abstract) (1975b)

  • Page, S.G., Niedergerke, R.: Structures of physiological interest in the frog heart ventricle. J. Cell Biol. 11, 179–203 (1972)

    Google Scholar 

  • Porter, K.R.: The myo-tendon junction in larval forms of Amblystoma punctatum. Anat. Rec. 118, 342 (Abstract) (1954)

    Google Scholar 

  • Porter, K.R., Palade, G.E.: Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. biophys. biochem. Cytol. 3, 269–300 (1957)

    Google Scholar 

  • Revel, J.P.: The sarcoplasmic reticulum of the bat cricothyroid muscle. J. Cell Biol. 12, 571–588 (1962)

    Google Scholar 

  • Rosenbluth, J.: Sarcoplasmic reticulum of an unusually fast-acting crustacean muscle. J. Cell Biol. 42, 534–547 (1969a)

    Google Scholar 

  • Rosenbluth, J.: Ultrastructure of diads in muscle fibers of Ascaris lumbricoides. J. Cell Biol 42, 817–825 (1969b)

    Google Scholar 

  • Schiaffino, S., Margreth, A.: Coordinated development of the sarcoplasmic reticulum and T system during postnatal differentiation of rat skeletal muscle. J. Cell Biol. 41, 855–875 (1969)

    Google Scholar 

  • Schubert, D., Harris, A.J., Devine, C.E., Heinemann, S.: Characterization of a unique muscle cell line. J. Cell Biol. 61, 398–413 (1974)

    Google Scholar 

  • Schwarzacher, H.G.: Untersuchungen über der Feinbau der Muskelfaser-Sehnenverbindung. Acta anat. (Basel) 40, 59–86 (1960)

    Google Scholar 

  • Scott, T.M.: The ultrastructure of ordinary and Purkinje cells of the fowl heart. J. Anat. (Lond.) 110, 259–273 (1971)

    Google Scholar 

  • Smith, D.S.: The organization of flight muscle in an aphid, Megoura viciae (Homoptera). J. Cell Biol. 27, 379–393 (1965)

    Google Scholar 

  • Smith, D.S.: The organization of flight muscle fibers in Odonata. J. Cell Biol. 28, 109–126 (1966a)

    Google Scholar 

  • Smith, D.S.: The structure of intersegmental muscle in an insect, Periplaneta americana. J. Cell Biol. 29, 449–459 (1966b)

    Google Scholar 

  • Somlyo, A.P., Devine, C.E., Somlyo, A.V., North, S.R.: Sarcoplasmic reticulum and the temperature-dependent contraction of smooth muscle in calcium-free solutions. J. Cell Biol. 51, 722–741 (1971)

    Google Scholar 

  • Soomer, J.K., Johnson, E.A.: Cardiac muscle. A comparative study of Purkinje fibers and ventricular fibers. J. Cell Biol. 36, 497–526 (1968)

    Google Scholar 

  • Sommer, J.K., Johnson, E.A.: Comparative ultrastructure of cardiac cell membrane specializations. A review. Amer. J. Cardiol. 25, 184–194 (1970)

    Google Scholar 

  • Spray, T.L., Waugh, R.A., Sommer, J.R.: Peripheral couplings in adult vertebrate skeletal muscle. Anatomical observation and functional implications. J. Cell Biol. 62, 223–227 (1974)

    Google Scholar 

  • Taylor, A.C., Kollros, J.J.: Stages in the normal development of Rana pipiens larvae. Anat. Rec. 94, 7–23 (1946)

    Google Scholar 

  • Yamada, E.: The fine structure of the gall bladder epithelium of the mouse. J. biophys. biochem. Cytol. 1, 445–458 (1955)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Akita University School of Medicine, Akita, Japan

    Taisuke Nakao

Authors
  1. Taisuke Nakao
    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

Nakao, T. Some observations on the fine structure of the myotendinous junction in myotomal muscles of the tadpole tail. Cell Tissue Res. 166, 241–254 (1976). https://doi.org/10.1007/BF00227045

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227045

Key words

Search

Navigation