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Thick filaments in vertebrate smooth muscle

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Summary

Smooth muscle cells of the mouse vas deferens fixed with 5% glutaraldehyde contained three types of filaments, namely, thin (50–80 Å) filaments, intermediate (100 Å) filaments and thick (120–180 Å) filaments. However, in 2 out of 16 experiments, under identical conditions, the cells did not contain thick filaments. With OsO4 fixation, thin filaments were not prominent, the most obvious being thick (120–250 Å) and intermediate (100 Å) filaments.

After soaking in a modified Ringer solution under no applied tension for one hour, thick filaments (120–180 Å) appeared prominently in smooth muscle cells of the mouse vas deferens and thin filaments were in ordered bundles. By 4 hours, thick filaments had increased in size and density, with thin filaments distributed randomly around them. After 8 hours in Ringer, thin filaments were diffuse and difficult to discern, while thick filaments were large (up to 300 Å) and electron-dense. Intermediate (100 Å) filaments were present in association with dark bodies. Physiological experiments indicated that the intracellular components responsible for the development of a mechanical response were still functional at this time.

The presence of “thick filaments” is also reported in degenerating smooth muscle cells of the guinea-pig vas deferens in tissue culture.

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References

  • Bárány, M., Bárány, K., Gaertens, E., Bailin, G.: Chicken gizzard myosin. Arch. Biochem. Biophys. 113, 205–221 (1966)

    Google Scholar 

  • Bauer, H., Goodford, P. J., Hüter, J.: The calcium content and 45calcium uptake of the smooth muscle of the guinea-pig taenia coli. J. Physiol. (Lond.) 176, 163–179 (1965)

    Google Scholar 

  • Burnstock, G.: Structure of smooth muscle and its innervation. In: Smooth muscle, eds. E. Bülbring, A. Brading, A. Jones and T. Tomita, p. 1–69. London: Edward Arnold Ltd. 1970

    Google Scholar 

  • Campbell, G. R., Chamley, J. H., Burnstock, G.: Development of smooth muscle cells in tissue culture. J. Anat. (Lond.) 117, 295–312 (1974)

    Google Scholar 

  • Campbell, G. R., Uehara, Y., Malmfors, T., Burnstock, G.: Degeneration and regeneration of smooth muscle transplants in the anterior eye chamber. An ultrastructural study. Z. Zellforsch. 117, 155–175 (1971)

    Google Scholar 

  • Campbell, G. R., Uehara, Y., Mark, G., Burnstock, G.: Fine structure of smooth muscle cells grown in tissue culture. J. Cell Biol. 49, 21–34 (1971)

    Google Scholar 

  • Carsten, M. E.: Tropomyosin from smooth muscle of the uterus. Biochemistry (Wash.) 7, 960–967 (1968)

    Google Scholar 

  • Carsten, M. E.: Uterine smooth muscle: Troponin. Arch. Biochem. Biophys. 147, 353–357 (1971)

    Google Scholar 

  • Chamley, J. H., Campbell, G. R., Burnstock, G.: Dedifferentiation, redifferentiation and bundle formation of smooth muscle cells in tissue culture. The influence of cell number and nerve fibres. J. Embryol. exp. Morph. 32, 297–323 (1974)

    Google Scholar 

  • Choi, J. K.: Fine structure of the smooth muscle of the chicken's gizzard. In: Proc. 5th Int. Cong. Electron Microscopy, Philadelphia, ed. S. S. Breese, Jr., M-9. New York: Academic Press 1962

    Google Scholar 

  • Cooke, P. H., Chase, R. H.: Potassium chloride-insoluble myofilaments in vertebrate smooth muscle cells. Exp. Cell Res. 66, 417–425 (1971)

    Google Scholar 

  • Cooke, P. H., Chase, R. H., Cortés, J. M.: Thick filaments resembling myosin in electrophoretically-extracted vertebrate smooth muscle. Exp. Cell Res. 60, 237–246 (1970)

    Google Scholar 

  • Cooke, P. H., Fay, F. S.: Thick myofilaments in contracted and relaxed mammalian smooth muscle cells. Exp. Cell Res. 71, 265–272 (1972)

    Google Scholar 

  • Devine, C. E., Somlyo, A. P.: Thick filaments in vascular smooth muscle. J. Cell Biol. 49, 636–649 (1971)

    Google Scholar 

  • Ebashi, S., Iwakura, H., Nakajima, H., Nakamura, R., Ooi, Y.: New structural proteins from dog heart and chicken gizzard. Biochem. Z. 345, 201–211 (1966)

    Google Scholar 

  • Enerson, D. M.: Cellular swelling. I. Hypothermia graded hypoxia, and the osmotic effects of low molecular weight dextran on isolated tissues. Ann. Surg. 163, 169–174 (1966)

    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 

  • Furness, J. B.: The excitatory input to a single smooth muscle cell. Pflügers Arch. 314, 1–13 (1970)

    Google Scholar 

  • Garamvölgyi, N., Vizi, E. S., Knoll, J.: The regular occurrence of thick filaments in stretched mammalian smooth muscle. J. Ultrastruct. Res. 34, 135–143 (1971)

    Google Scholar 

  • Gröschel-Stewart, U.: Comparative studies of human smooth and striated muscle myosins. Biochim. biophys. Acta (Amst.) 229, 322–334 (1971)

    Google Scholar 

  • Hamoir, G.: Extractability and properties of the contractile proteins of vertebrate smooth muscle. Phil. Trans. B 265, 169–181 (1973)

    Google Scholar 

  • Hamoir, G., Laszt, L.: La tropomyosine B de carotides de bovidé. Biochim. biophys. Acta (Amst.) 59, 365–375 (1962a)

    Google Scholar 

  • Hamoir, G., Laszt, L.: Tonomyosin of arterial muscle. Nature (Lond.) 193, 682–684 (1962b)

    Google Scholar 

  • Hanson, J., Lowy, J.: The problem of the location of myosin in vertebrate smooth muscle. Proc. roy. Soc. B 160, 523–524 (1964)

    Google Scholar 

  • Heumann, H.-G,: Smooth muscle: contraction hypothesis based on the arrangement of actin and myosin filaments in different states of contraction. Phil. Trans. B 265, 213–217 (1973)

    Google Scholar 

  • Huriaux, F., Pechère, J. F., Hamoir, G.: Propriétés et composition de la tonomyosine de carotides de bovidé. Angiologica 2, 15–43 (1965)

    Google Scholar 

  • Huxley, H. E.: Molecular basis of contraction in cross-striated muscles. In: Structure and function of muscle, ed. G. Bourne, vol. 1, 2nd ed., p. 302–388. New York: Academic Press 1972

    Google Scholar 

  • Kaminer, B.: Synthetic myosin filaments from vertebrate smooth muscle. J. molec. Biol. 39, 257–264 (1969)

    Google Scholar 

  • Kelly, R. E., Arnold, J. W.: Myofilaments of the pupillary muscles of the iris fixed in situ. J. Ultrastruct. Res. 40, 532–545 (1972)

    Google Scholar 

  • Kelly, R. E., Rice, R. V.: Localization of myosin filaments in smooth muscle. J. Cell Biol. 37, 105–116 (1968)

    Google Scholar 

  • Kelly, R. E., Rice, R. V.: Ultrastructural studies on the contractile mechanism of smooth muscle. J. Cell Biol. 42, 683–694 (1969)

    Google Scholar 

  • Kerényi, T., Jellinek, H.: Fibrin deposition in smooth muscle cells of muscular type small arteries under temporary conditions of hypoxia. Exp. molec. Path. 17, 1–5 (1972)

    Google Scholar 

  • Keyserlingk, D. G.: Ultrastruktur glycerinextrahierter Dünndarmuskelzellen der Ratte vor und nach Kontraktion. Z. Zellforsch. 111, 559–571 (1970)

    Google Scholar 

  • Lane, B. P., Rhodin, J. A. G.: Fine structure of the lamina muscularis mucosae. J. UItrastruct. Res. 10, 489–497 (1964)

    Google Scholar 

  • Lowy, J., Poulsen, F. R., Vibert, P. H.: Myosin filaments in vertebrate smooth muscle. Nature (Lond.) 225, 1053–1054 (1970)

    Google Scholar 

  • Lowy, J., Small, J. V.: The organization of myosin and actin in vertebrate smooth muscle. Nature (Lond.) 227, 46–51 (1970)

    Google Scholar 

  • Lowy, J., Vibert, P. J., Haselgrove, J. C., Poulsen, F. R.: The structure of the myosin elements in vertebrate smooth muscles. Phil. Trans. B 265, 191–196 (1973)

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961)

    Google Scholar 

  • Needham, D. M., Shoenberg, C. F.: The biochemistry of the myometrium. In: Cellular biology of the uterus, ed. R. M. Wynn, p. 291–352. New York: Appleton-Century-Crofts Inc. 1967

    Google Scholar 

  • Needham, D.M., Williams, J. M.: Proteins of the uterine contractile mechanism. Biochem. J. 89, 552–561 (1963)

    Google Scholar 

  • Nonomura, Y.: Myofilaments in smooth muscle of guinea pig's taenia coli. J. Cell Biol. 39, 741–745 (1968)

    Google Scholar 

  • Panner, B. J., Honig, C. R.: Filament ultrastructure and organization in vertebrate smooth muscle. Contraction hypothesis based on localization of actin and myosin. J. Cell Biol. 35, 303–321 (1967)

    Google Scholar 

  • Panner, B. J., Honig, C. R.: Locus and state of aggregation of myosin in tissue sections of vertebrate smooth muscle. J. Cell Biol. 44, 52–61 (1970)

    Google Scholar 

  • Pease, D. C.: Structural features of unfixed mammalian smooth and striated muscle prepared by glycol dehydration. J. Ultrastruct. Res. 23, 280–303 (1968)

    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 

  • Rice, R. V., Brady, A. C.: Biochemical and ultrastructural studies on vertebrate smoothmuscle. In: The mechanism of muscle contraction. Cold Spr. Harb. Symp. quant. Biol. 37, 429–438 (1973)

    Google Scholar 

  • Rice, R. V., McManus, G. M., Devine, C. R., Somlyo, A. P.: Regular organization of thick filaments in mammalian smooth muscle. Nature (Lond.) New Biol. 231, 242–243 (1971)

    Google Scholar 

  • Rice, R. V., Moses, J. A., McManus, G. M., Brady, A. C., Blasik, L. M.: The organization ofcontractile filaments in a mammalian smooth muscle. J. Cell Biol. 47, 183–196 (1970)

    Google Scholar 

  • Rosenbluth, J.: Myosin-like aggregates in trypsin-treated smooth muscle cells. J. Cell Biol. 48, 174–188 (1971)

    Google Scholar 

  • Schirmer, R. H.: Die Besonderheiten des contractilen Proteins der Arterien. Biochem. Z. 343, 269–282 (1965)

    Google Scholar 

  • Shoenberg, C. F.: An electron microscope study of the influence of divalent ions on myosin filament formation in chicken gizzard extracts and homogenates. Tissue and Cell 1, 83–96 (1969)

    Google Scholar 

  • Shoenberg, C. F.: The influence of temperature on the thick filaments of vertebrate smooth muscle. Phil. Trans. B 265, 197–202 (1973)

    Google Scholar 

  • Shoenberg, C. F., Goodford, P. J., Wolowyk, M. W., Wootton, G. S.: Ionic changes during smooth muscle fixation for electron microscopy. J. Mechanochem. Cell Motility 2, 69–82 (1973)

    Google Scholar 

  • Small, J. V.: Contractile units in vertebrate smooth muscle cells. Nature (Lond.) 249, 324–327 (1974)

    Google Scholar 

  • Small, J. V., Squire, J. M.: Structural basis of contraction in vertebrate smooth muscle. J. molec. Biol. 67, 117–149 (1972)

    Google Scholar 

  • Somlyo, A. P., Devine, C. E., Somlyo, A. V.: Thick filaments in unstretched mammalian smooth muscle. Nature (Lond.) New Biol. 233, 218–219 (1971)

    Google Scholar 

  • Somlyo, A. P., Devine, C. E., Somlyo, A. V., Rice, R. V.: Filament organization in vertebrate smooth muscle. Phil. Trans. B 265, 223–229 (1973)

    Google Scholar 

  • Somlyo, A. P., Somlyo, A. V.: Vascular smooth muscle. I. Normal structure, pathology, biochemistry and biophysics. Pharmacol. Rev. 20, 197–272 (1968)

    Google Scholar 

  • Stehbens, W. E.: The ultrastructure of the anastomosed vein of experimental arteriovenous fistulae in sheep. Amer. J. Path. 76, 377–400 (1974)

    Google Scholar 

  • Takebayashi, S.: Ultrastructural studies on arteriolar lesions in experimental hypertension. J. Electron microscopy 19, 17–31 (1970)

    Google Scholar 

  • Uehara, Y., Campbell, G. R., Burnstock, G.: Cytoplasmic filaments in developing and adult vertebrate smooth muscle. J. Cell Biol. 50, 484–497 (1971)

    Google Scholar 

  • Venable, J. H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965)

    Google Scholar 

  • Wachsberger, P., Kaldor, G.: Studies on uterine myosin A and actomyosin. Arch. Biochem. Biophys. 143, 127–137 (1971)

    Google Scholar 

  • Yamaguchi, M., Miyazawa, Y., Sekine, T.: Preparation and properties of smooth muscle myosin from horse oesophagus. Biochim. biophys. Acta (Amst.) 216, 411–421 (1970)

    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 Zoology, University of Melbourne, Parkville, Vic., Australia

    G. R. Campbell & J. H. Chamley

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  1. G. R. Campbell
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  2. J. H. Chamley
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Additional information

We are extremely grateful for the collaboration, helpful advice and guidance of Professor Yasuo Uehara. We would also like to thank Dr. P. Berger for performing the organ-bath studies and Professor G. Burnstock for the use of laboratory facilities. G. R. Campbell and J. H. Chamley are holders of post-doctoral research fellowships from the National Heart Foundation of Australia and the Life Insurance Medical Research Fund of Australia and New Zealand respectively.

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Campbell, G.R., Chamley, J.H. Thick filaments in vertebrate smooth muscle. Cell Tissue Res. 156, 201–216 (1975). https://doi.org/10.1007/BF00221803

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