Skip to main content
Log in

New views of smooth muscle structure using freezing, deep-etching and rotary shadowing

  • Reviews
  • Published:
Experientia Aims and scope Submit manuscript

Summary

Freezing, deep-etching and rotary shadowing techniques have been applied to study smooth muscle ultrastructure. The results show some new aspects of intracellular and extracellular connections, interior views of the sarcoplasmic reticulum showing a luminal content, coated pits and vesicles, contractile filaments and other organelles in smooth muscle.

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

Access this article

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

  1. Ashton, F. T., Somlyo, A. V., and Somlyo, A. P., The contractile apparatus of vascular smooth muscle: Intermediated high voltage stereo electron microscopy. J. molec. Biol.98 (1975) 17–29.

    Article  CAS  PubMed  Google Scholar 

  2. Bond, M., Kitazawa, T., Somlyo, A. P., and Somlyo, A. V., Release and recycling of calcium by the sarcoplasmic reticulum in guinea pig portal vein smooth muscle. J. Physiol., Lond., in press.

  3. Bond, M., and Somlyo, A. V., Dense bodies and actin polarity in vertebrate smooth muscle. J. Cell Biol.95 (1982) 403–413.

    Article  CAS  PubMed  Google Scholar 

  4. Burke, J. M., and Ross, R., Synthesis of connective tissue macromolecules by smooth muscle. Int. Rev. Connect. Tissue Res.,8 (1979) 119–157.

    Article  CAS  PubMed  Google Scholar 

  5. Campbell, G. R., and Chamley, J. H., Thick filaments in vertebrate smooth muscle. Cell Tissue Res.156 (1975) 201–216.

    Article  CAS  PubMed  Google Scholar 

  6. Chen, K., and Wight, T. N., Proteoglycans in arterial smooth muscle cell cultures: An ultrastructural histochemical analysis. J. Histochem. Cytochem.32 (1984) 347–357.

    Article  CAS  PubMed  Google Scholar 

  7. Chen, W.-T., and Singer, S. J., Immunoelectron microscopic studies of the sites of cell-substratum and cell-cell contacts in cultured fibroblasts. J. Cell Biol.95 (1982) 205–222.

    Article  CAS  PubMed  Google Scholar 

  8. Craig, R., and Megerman, J., Assembly of smooth muscle myosin into side-polar filaments. J. Cell Biol.75 (1977) 990–996.

    Article  CAS  PubMed  Google Scholar 

  9. Craig, R., Smith, R., and Kendrick-Jones, J., Light chain phosphorylation controls the conformation of vertebrate non-muscle and smooth muscle myosin molecules. Nature302 (1983) 436–439.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Endo, M., Kitazawa, T., Yagi, S., Iino, M., and Kakuta, T., Some properties of chemically skinned smooth muscle fibers, in: Excitation-Contraction in Smooth Muscle, pp. 199–210. Eds R. Casteels, T. Godfraind and J. C. Rüegg. Elsevier/North-Holland, Amsterdam 1977.

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Franzini-Armstrong, C., and Nunzi, G., Junctional feet and particles in the triads of a fast-twitch muscle fibre. J. Muscle Res. Cell Motility4 (1983) 233–252.

    Article  CAS  Google Scholar 

  15. Gabella, G., The force generated by a visceral smooth muscle, J. Physiol., Lond.263 (1976) 199–213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gabella, G., Structure of smooth muscles, in: Smooth Muscle: An Assessment of Current Knowledge, pp. 1–46. Eds. E. Bülbring, A. F. Brading, A. W. Jones and T. Tomita. University of Texas Press, Austin 1981.

    Google Scholar 

  17. Geiger, B., Dutton, A. H., Tokayasu, T., and Singer, S. J., Immunoelectron microscope studies of membrane-microfilament interaction: Distributions of alpha-actinin, tropomyosin, and vinculin in intestinal epithelial brush border and chicken gizzard smooth muscle cells. J. Cell Biol.91 (1981) 614–628.

    Article  CAS  PubMed  Google Scholar 

  18. Goldstein, J. L., Anderson, R. G. W., and Brown, M. S., Coated pits, coated vesicles and receptor-mediated endocytosis. Nature279 (1979) 679–685.

    Article  CAS  PubMed  Google Scholar 

  19. Heuser, J. E., Three-dimensional visualization of coated vesicle formation in fibroblasts. J. Cell Biol.84 (1980) 560–583.

    Article  CAS  PubMed  Google Scholar 

  20. Heuser, J. E., Structure of the myosin crossbridge lattice in insect flight muscle. J. molec. Biol.169 (1983) 123–154.

    Article  CAS  PubMed  Google Scholar 

  21. Heuser, J. E., and Cooke, R., Actin-myosin interactions visualized by the quick-freeze deep-etch replica technique. J. molec. Biol.169 (1983) 97–122.

    Article  CAS  PubMed  Google Scholar 

  22. Heuser, J. E., and Kirshner, M. W., Filament organization revealed in platinum replicas of freeze-dried cytoskeletons. J. Cell Biol86 (1980) 212–234.

    Article  CAS  PubMed  Google Scholar 

  23. Heuser, J. E., Reese, T. S., Dennis, M. J., Jan, L., and Evans, L., Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol.81 (1979) 275–300.

    Article  CAS  PubMed  Google Scholar 

  24. Hirokawa, N., Glicksman, M. A., and Willard, M. B., Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J. Cell Biol.98 (1984) 1523–1536.

    Article  CAS  PubMed  Google Scholar 

  25. Hirokawa, N., and Tilney, L. G., Interactions between actin filaments and between actin filaments and membranes in quick-frozen and deeply etched hair cells of the chick ear. J. Cell Biol95 (1982) 149–261.

    Article  Google Scholar 

  26. Ishikawa, H., Bischoff, R., and Holtzer, H., Formation of arrowhead complexes with HMM in a variety of cell types. J. Cell Biol7 (1969) 281–308.

    Google Scholar 

  27. Jorgensen A. O., Kalnins, V., and MacLennan, D. H., Localization of sarcoplasmic reticiulum proteins in rat skeletal muscle by immunofluorescence. J. Cell Biol.80 (1979) 372–384.

    Article  CAS  PubMed  Google Scholar 

  28. Junker, J. L., and Sommer, J. R., Calsequestrin localization in rabbit and frog skeletal muscle by immunofluorescence. J. Cell Biol.83 (1979) 384a (abstr.).

    Google Scholar 

  29. Kanaseki, T., and Kadota, K., The ‘vesicle in a basket’: A morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. J. Cell Biol.42 (1969) 202–220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Montesano, R., Perrelet, A., Vassali, P., and Orci, L., Absence of filipin-sterol complexes from large coated pits on the surface of culture cells. Proc. natn. Acad. Sci. USA76 (1979) 6391–6395.

    Article  CAS  Google Scholar 

  31. Ohtsuki, I., Manzi, R. M., Palade, G. E., and Jamieson, J. D., Entry of macromolecular tracers into cells fixed with low concentrations of aldehydes. Biol. cell.31 (1978) 119–126.

    Google Scholar 

  32. Pearse, B. M. F., Coated vesicles from pig brain: Purification and biochemical characterization. J. molec. Biol.97 (1975) 93–98.

    Article  CAS  PubMed  Google Scholar 

  33. Pearse, B. M. F., Clathrin: A unique protein associated with intracellular transfer membrane by coated vesicles. Proc. natn. Acad. Sci. USA73 (1976) 1255–1259.

    Article  CAS  Google Scholar 

  34. Poole, A. P., Pidoux, I., Reiner, A., and Rosenberg, L., An immunoelectron microscope study of the organization of proteoglycan monomer, link protein, and collagen in the matrix of articular cartilage. J. Cell Biol.93 (1982) 921–937.

    Article  CAS  PubMed  Google Scholar 

  35. Robinson, T. F., and Winegrad, S., A variety of intercellular connections in heart muscle. J. molec. cell. Cardiol.13 (1981) 185–195.

    Article  CAS  Google Scholar 

  36. Rogus, E., and Zierler, K. L., Sodium and water contents of sarcoplasm and sarcoplasmic reticulum in rat skeletal muscle: Effects of anisotonic media, ouabain and external sodium. J. Physiol., Lond.233 (1973) 227–270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ross, R., Connective tissue cells, cell proliferation and synthesis of extracellular matrix: A review. Phil. Trans. R. Soc. Lond. (B) 271 (1975) 247–259.

    CAS  Google Scholar 

  38. Roth, T. F., and Porter, K. R., Yolk protein uptake in the oocyte of the mosquito,Aedes aegypti. J. Cell Biol.2 (1964) 313–316.

    Article  Google Scholar 

  39. Salisbury, J. L., Condeelis, J. S., Maihle, N. J., and Satir, P., Receptor-mediated endocytosis by clathrin-coated vesicles: Evidence for a dynamic pathway. Cold Spring Harb. Symp. quant. Biol.46 (1982) 733–741.

    Article  PubMed  Google Scholar 

  40. Schollmeyer, J. E., Furcht, L. T., Goll, D. E., Robson, R. M., and Stromer, M. H., Localization of contractile proteins in smooth muscle cells and in normal and transformed fibroblasts, in: Cell Motility, vol. 3a, pp. 361–388. Eds R. Goldman, T. Pollard and J. Rosenbaum, Cold Spring Harbor Laboratories, Cold Spring Harbor 1976.

    Google Scholar 

  41. Small, J. V., and Sobieszek, A., The contractile apparatus of smooth muscle. Int. Rev. Cytol.64 (1980) 241–306.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  44. Somlyo, A. P., and Somlyo, A. V., Ultrastructure of smooth muscle, in: Methods in Pharmacology, vol. 3, pp. 3–45. Eds E. E. Daniel and D. M. Paton. Plenum Press, New York 1975.

    Google Scholar 

  45. Somlyo, A. P., and Somlyo, A. V., Ultrastructure of the contractile apparatus: Controversies resolved and questions remaining, in: Excitation-Contraction Coupling in Smooth Muscle, pp. 317–322. Eds R. Casteels, T. Godfraind and J. C. Rüegg. Elsevier/North Holland, Amsterdam 1977.

    Google Scholar 

  46. Somlyo, A. P., Wasserman, A. J., Kitazawa, T., Bond, M., Shuman, H., and Somlyo, A. V., Calcium and sodium distribution and movements in smooth muscle. Experientia, in press 1985.

  47. Somlyo, A. V., Bridging structures spanning the junctional gap at the triad of skeletal muscle. J. Cell Biol.81 (1979) 743–750.

    Article  Google Scholar 

  48. Somlyo, A. V., Ultrastructure of vascular smooth muscle, in: The Handbook of Physiology: The Cardiovascular System, vol. 2, Vascular Smooth Muscle, pp. 33–67. Eds D. F. Bohr, A. P. Somlyo and H. V. Sparks. American Physiological Society, Bethesda 1980.

    Google Scholar 

  49. Somlyo, A. V., Butler, T. M., Bond, M., and Somlyo, A. P., Myosin filaments have nonphosphorylated light chains in relaxed smooth muscle. Nature294 (1981) 567–570.

    Article  CAS  PubMed  Google Scholar 

  50. Somlyo, A. V., Gonzalez-Serratos, H., Shuman, H., McClellan, G., and Somlyo, A. P., Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: An electron probe study. J. Cell Biol.90 (1981) 577–594.

    Article  CAS  PubMed  Google Scholar 

  51. Somlyo, A. V., Shuman, H., and Somlyo, A. P., Elemental distribution in striated muscle and effects of hypertonicity: Electron probe analysis of cryo sections. J. Cell Biol.74 (1977) 828–857.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sommer, J. R., and Johnson, E. A., Ultrastructure of cardiac muscle, in: The Handbook of Physiology: The Cardiovascular System, vol. 1,The Heart, pp. 113–186. Ed. R. M. Berne. American Physiological Societ, Bethesda 1979.

    Google Scholar 

  53. Suzuki, H., Onishi, H., Takahashi, K., and Watanabe, S., Structure and function of chicken gizzard myosin. J. Biochem., Tokyo84 (1978) 1529–1542.

    Article  CAS  PubMed  Google Scholar 

  54. Trybus, K. M., Huiatt, T. W., and Lowey, S., A bent monomeric conformation of myosin from smooth muscle. Proc. natn. Acad. Sci. USA79 (1982) 6151–6155.

    Article  CAS  Google Scholar 

  55. Trybus, K. M., and Lowey, S., Conformation and assembly of smooth muscle myosin. Biophys. J.41 (1983) 299a.

    Google Scholar 

  56. Ungewickell, E., and Branton, D., Assembly of clathrin coats. Nature289 (1981) 420–424.

    Article  CAS  PubMed  Google Scholar 

  57. Varriano-Marston, E., and Franzini-Armstrong, C., Crossbridges in deep-etched vertebrate striated muscle. J. Cell Biol.95 (1982) (2, pt 2), 1368a (abstr.).

    Google Scholar 

  58. Varriano-Marston, E., Franzini-Armstrong, C., and Hazelgrove, J., The structure and disposition of crossbridges in deep-etched vertebrate striated muscle. J. Muscle Res. Cell Motility5 (1984) 363–386.

    Article  CAS  Google Scholar 

  59. Wakabayashi, T., and Toyoshima, C., Three-dimensional image analysis of the complex of thin filaments and myosin molecules from skeletal muscle: II. The multi-domain structure of actin-myosin S1 complex. J. Biochem., Tokyo90 (1981) 683–701.

    Article  CAS  PubMed  Google Scholar 

  60. Wight, T. N., and Hascall, V. C., Preteoglycans in primate arteries: III. Characterization of the proteoglycans synthesized by arterial smooth muscle cells in culture. J. Cell Biol.96 (1983) 167–176.

    Article  CAS  PubMed  Google Scholar 

  61. Wight, T. N., and Ross, R., Proteoglycans in primate arteries: I. Ultrastructural localization and distribution in the intima. J. Cell Biol.67 (1975) 660–674.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Somlyo, A.V., Franzini-Armstrong, C. New views of smooth muscle structure using freezing, deep-etching and rotary shadowing. Experientia 41, 841–856 (1985). https://doi.org/10.1007/BF01970000

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01970000

Key words

Navigation