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Quantitative morphological study of smooth muscle cells of the guinea-pig taenia coli

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A quantitative study of muscle cells of the guinea-pig taenia coli is reported. Stereological methods were used on electron micrographs and phase contrast micrographs. Smooth muscle cells of taeniae fixed under 1 gram load were about 515 μm long. Muscle cell volume was about 3,500 μm3 and cell surface 5,300 μm2. About 168,000 caveolae were found at the surface of each muscle cell, covering about 29 percent of its surface. They produced a 73 percent increase of the cell membrane compared to a smooth-surfaced cell. The ratio surface-to-volume is about 1∶0.67 if the geometrical surface is considered, or 1∶0.39 if the total surface of the cell membrane (including the caveolae) is considered. Mitochondria constituted 3.5–4 percent of the cell volume. A few nexuses were observed, both between two muscle cells and between a muscle cell and an interstitial cell. In serial sections septa of connective tissue and groups of muscle cells were found to disappear within few tens of microns or to merge with other septa, and the taenia did not appear to be divided into clear-cut muscle cell bundles. Bundles of smooth muscle cells were seen passing from the taenia to the underlying circular muscle. The transverse sectional area of the taenia ranged between 0.14 and 0.39 mm2; it showed about 526 blood vessels · mm-2.

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References

  • Barr, L., Berger, W., Dewey, M.M.: Electrical transmission at the nexus between smooth muscle cells. J. gen. Physiol. 51, 347–369 (1968)

    Google Scholar 

  • Bennett, H.S.: The structure of striated muscle as seen by the electron microscope. In: Structure and function of muscle, Vol. 1 (G.H. Bourne, ed.), pp. 137–150. New York: Academic Press 1960

    Google Scholar 

  • Bennett, M.R., Burnstock, G.: Electrophysiology of the innervation of intestinal smooth muscle. In: Handbbok of Physiology, Sec. 6, Vol. 4 (C.F. Code, ed.), pp. 1709–1732. Washington: American Physiological Society 1968

    Google Scholar 

  • Bennett, M.R., Rogers, D.C.: A study of the innervation of the taenia coli. J. Cell Biol. 33, 573–596 (1967)

    Google Scholar 

  • Brading, A.F., Widdicombe, J.H.: An estimate of sodium/potassium pump activity and the number of pump sites in the smooth muscle of the guinea-pig taenia coli, using [3H] ouabain. J. Physiol. (Lond.) 238, 235–249 (1974)

    Google Scholar 

  • Bülbring, E.: Membrane potentials of smooth muscle fibres of the taenia coli of the guinea-pig. J. Physiol. (Lond.) 125, 302–315 (1954)

    Google Scholar 

  • Bülbring, E.: Physiology and pharmacology of intestinal smooth muscle. Lectures on Scientific Basis of Medicine 7, 374–397 (1957)

    Google Scholar 

  • Bülbring, E., Hooton, I.N.: Smooth muscle potentials recorded with intracellular electrodes. J. Physiol. (Lond.) 120, 8–9 (1953)

    Google Scholar 

  • Burnstock, G., Prosser, C.L.: Conduction in smooth muscles: comparative electrical properties. Amer. J. Physiol. 199, 553–559 (1960)

    Google Scholar 

  • Casteels, R.: The relation between the membrane potential and the ionic distribution in smooth muscle cells. In: Smooth muscle (E. Bülbring, A.F. Brading, A.W. Jones and T. Tomita, eds.), pp. 70–99. London: Arnold 1970

    Google Scholar 

  • Cobb, J.L.S., Bennett, T.: A study of nexuses in visceral smooth muscle. J. Cell Biol. 41, 287–297 (1969)

    Google Scholar 

  • Cooke, P.H., Fay, F.S.: Correlation between fiber length, ultrastructure, and the length-tension relationship in mammalian smooth muscle. J. Cell Biol. 52, 105–116 (1972)

    Google Scholar 

  • Devine, C.E., Rayns, D.G.: Freeze-fracture studies of membrane systems in vertebrate muscle. II. Smooth muscle. J. Ultrastruct. Res. 51, 293–306 (1975)

    Google Scholar 

  • Devine, C.E., Simpson, F.O., Bertaud, W.S.: Surface features of smooth muscle cells from the mesenteric artery and vas deferens. J. Cell Sci. 8, 427–443 (1971)

    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 

  • Dewey, M.M., Barr, L.: A study of the structure and distribution of the nexus. J. Cell Biol. 23, 553–585 (1964)

    Google Scholar 

  • Dulhunty, A.F., Franzini-Armstrong, C.: The relative contribution of the folds and caveolae to the surface membrane of frog skeletal muscle fibres at different sarcomere lengths. J. Physiol. (Lond.) 250, 513–539 (1975)

    Google Scholar 

  • Franzini-Armstrong, C.: Membrane systems in muscle fibres. In: The structure and function of muscle, 2nd ed., Vol. 1 (G.H. Bourne, ed.), pp. 532–617. New York: Academic Press 1973

    Google Scholar 

  • Freeman-Narrod, M., Goodford, P.J.: Sodium and potassium content of the smooth muscle of the guinea-pig taenia coli at different temperatures and tensions. J. Physiol. (Lond.) 163, 399–410 (1962)

    Google Scholar 

  • Gabella, G.: Fine structure of smooth muscle. Phil. Trans. roy. Soc. B 265, 7–16 (1973)

    Google Scholar 

  • Gabella, G.: Special muscle cells and their innervation in the mammalian small intestine. Cell Tiss. Res. 153, 63–77 (1974a)

    Google Scholar 

  • Gabella, G.: The sphincter pupillae of the guinea-pig: structure of muscle cells, intercellular relations and density of innervation. Proc. roy. Soc. B 186, 369–386 (1974b)

    Google Scholar 

  • Geisweid, G., Wermbter, G.: Die Feinstruktur des Nexus zwischen glatten Muskelzellen der Taenia coli im Gefrierätzbild. Cytobiol. 9, 121–130 (1974)

    Google Scholar 

  • Goodford, P.J.: Ion movements in smooth muscle. In: Membranes and ion transport (E. Bittar, ed.), pp. 33–74. New York: Wiley 1970

    Google Scholar 

  • Goodford, P.J., Hermansen, K.: Sodium and potassium movements in the unstriated muscle of the guinea-pig taenia coli. J. Physiol. (Lond.) 158, 426–448 (1961)

    Google Scholar 

  • Henderson, R.M.: Cell-to-cell contacts. In: Methods in pharmacology (E.E. Daniel and D.M. Paton, ed.), pp. 47–77. New York: Plenum Press 1975

    Google Scholar 

  • Henderson, R.M., Duchon, G., Daniel, E.E.: Cell contacts in duodenal smooth muscle layers. Amer. J. Physiol. 221, 564–574 (1971)

    Google Scholar 

  • Imaizumi, M., Hama, K.: An electron microscopic study on the interstitial cells of the gizzard in love-bird (Uroloncha domestica). Z. Zellforsch. 97, 351–357 (1969)

    Google Scholar 

  • Irwin, D.A.: The anatomy of the Auerbach's plexus. Amer. J. Anat. 49, 141–166 (1931)

    Google Scholar 

  • Ishikawa, H., Fukuda, Y., Yamada, E.: Freeze-replica observations on frog sartorius muscle. I. Sarcolemmal specialization J. Electr. Micr. 24, 97–107 (1975)

    Google Scholar 

  • McGeachie, J.K.: Smooth muscle regeneration. Monographs Develop. Biol. 9, 1–90 (1975)

    Google Scholar 

  • Merrillees, N.C.R.: The nervous environment of individual smooth muscle cells of the guinea-pig vas deferens. J. Cell Biol. 37, 794–817 (1968)

    Google Scholar 

  • Mobley, B.A., Eisenberg, B.R.: Sizes of components in frog skeletal muscle measured by methods of stereology. J. gen. Physiol. 66, 31–45 (1975)

    Google Scholar 

  • Nagasawa, J., Suzuki, T.: Electron microscopic study on the cellular interrelationships in the smooth muscle. Tohoku J. exp. Med. 91, 299–313 (1967)

    Google Scholar 

  • Nishihara, H.: Some observations on the fine structure of the guinea-pig taenia coli in hypertonic solution, with special reference to the nexus. J. Anat. (Lond.) 107, 101–114 (1970)

    Google Scholar 

  • Prosser, C.L., Burnstock, G., Kahn, J.: Conduction in smooth muscle: comparative structural properties. Amer. J. Physiol. 199, 545–552 (1960)

    Google Scholar 

  • Rayns, D.G., Simpson, F.O., Bertaud, W.S.: Surface features of striated muscle. I. Guinea-pig cardiac muscle. J. Cell Sci. 3, 467–474 (1968)

    Google Scholar 

  • Schofield, G.C.: Anatomy of muscular and neural tissues in the the alimentary canal. In: Handbook of physiology, Sect. 6, Vol. 4 (C.F. Code, ed.), pp. 1579–1627. Washington: American Physiological Society

  • Taxi, J.: Contribution a l'étude des connexions des neurones moteurs du système nerveux autonome. Ann. Sci. Nat. Zool. 7, 413–674 (1965)

    Google Scholar 

  • Verity, M.A., Bevan, J.A.: Fine structural study of the terminal effector plexus, neuromuscular and intermuscular relationships in the pulmonary artery. J. Anat. (Lond.) 103, 49–63 (1968)

    Google Scholar 

  • Watanabe, H., Yamamoto, T.Y.: Freeze-etch of smooth muscle cells from vas deferens and taenia coli. J. Anat. (Lond.) 117, 553–564 (1974)

    Google Scholar 

  • Wootton, G.S., Goodford, P.J.: The ratio of smooth muscle cell volume to cell surface area measured by electron microscopy with corrections for shrinkage. Cell Tiss. Res. 162, 75–82 (1975)

    Google Scholar 

  • Yamauchi, A.: Electron microscopic studies on the autonomic neuromuscular junction in the taenia coli of the guinea-pig. Acta anat. nipp. 39, 22–38 (1964)

    Google Scholar 

  • Yamauchi, A., Burnstock, G.: Post-natal development of smooth muscle cells in the mouse vas deferens. A fine structural study. J. Anat. (Lond.) 104, 1–15 (1969)

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, University College London, England

    Giorgio Gabella

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  1. Giorgio Gabella
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I thank Professors G. Burnstock and E.G. Gray, F.R.S., for critical comments on the manuscript, and Miss E.M. Franke and Mr. S.J. Sarsfield for excellent technical assistance. This work is supported by grants from the Medical Research Council and the Central Research Funds of the University of London

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Gabella, G. Quantitative morphological study of smooth muscle cells of the guinea-pig taenia coli. Cell Tissue Res. 170, 161–186 (1976). https://doi.org/10.1007/BF00224297

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