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The Contractile Mechanism and Ultrastructure of the Myometrium

  • C. F. Shoenberg

Abstract

It is usual to stress the resemblance between vertebrate smooth muscles and other muscles (striated and cardiac muscles of vertebrates, and invertebrate smooth muscles). An actomyosin can be extracted from vertebrate smooth muscles in solutions of high ionic strength (Csapo, 1948), which has properties closely resembling those of skeletal muscles (see review by Needham and Shoenberg, 1967). The muscles appear to contract by a sliding filament mechanism (Shoenberg, 1962, 1969b) and develop tensions comparable to those developed by skeletal muscles (Herlihy and Murphy, 1974; Murphy et al 1974). There exist, however, very striking differences between vertebrate smooth muscles and skeletal muscles, and there are some aspects in which these muscles resemble much more closely nonmuscle cells, fibroblasts in particular. Particular emphasis will be placed in this chapter on the different ways in which smooth muscles resemble nonmuscle cells. Most of our knowledge on the structure and function of muscles is derived from studies on skeletal muscles; therefore, these are briefly described before approaching the subject of smooth muscles.

This chapter is dedicated to Dr. Dorothy M. Needham on the occasion of her eightieth birthday.

Keywords

Sarcoplasmic Reticulum Dense Body Thin Filament Dense Patch Thick Filament 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adelstein, R. S., Pollard, T. D., and Kuehl, W. M., 1971, Isolation and characterization of myosin and two myosin fragments from human blood platelets, Proc. Natl. Acad. Sci. USA 68:2703– 2707.Google Scholar
  2. Althoff, R. W., and Albert, E. N., 1970, Ultrastructural changes in mouse myometrium during pregnancy, Am. J. Obstet. Gynecol. 108: 1224–1233.PubMedGoogle Scholar
  3. Ashton, T., Somlyo, A. V., and Somlyo, A. P., 1975, The contractile apparatus of vascular smooth muscle: Intermediate high voltage stereo electron microscopy,. Mol. Biol. 98: 17–30.Google Scholar
  4. Bagby, R. M., Young, A. M., Dotson, R. S., Fisher, B. A., and McKinnon, K., 1971, Contraction of single smooth muscle cells from Bufo marinus stomach, Nature (London) 234: 351–352.PubMedGoogle Scholar
  5. Batra, S. C., 1973, The role of mitochondrial calcium uptake in contraction and relaxation of the human myometrium, Biochim. Biophys. Acta 305: 428–432.PubMedGoogle Scholar
  6. Bauer, H., Goodford, P. J., and Hiiter, J., 1965, The calcium content and calcium uptake of the smooth muscle of the guinea-pig taenia coli,J. Physiol. (London) 176: 163–179.Google Scholar
  7. Behnke, O., Kristensen, B. I., and Engdahl Nielsen, L., 1971, Electron microscopical observations on actinoid and myosinoid filaments in blood platelets, Ultrastruct. Res. 37: 351–369.Google Scholar
  8. Bertaud, W. S., Rayns, D. G., and Simpson, F. O., 1970, Freeze-etch studies on fish skeletal muscle, J. Cell Sci. 6: 537–557.PubMedGoogle Scholar
  9. Biberfeld, P., Ericsson, J. L. E., Perlmann, P., and Raftell, M., 1965, Increased occurrence of cytoplasmic filaments in vitro propagated rat liver epithelial cells, Exp. Cell Res. 39:301– 305.Google Scholar
  10. Bruns, R. R., and Palade, G. E., 1968, Studies on blood capillaries. I. General organization of blood capillaries in muscle,/. Cell Biol. 37: 244–276.Google Scholar
  11. Burridge, K., 1974, A comparison of fibroblast and smooth muscle myosins, FEBS Lett. 45: 14–17.PubMedGoogle Scholar
  12. Campbell, G. R., and Chamley, J. H., 1975, Thick filaments in vertebrate smooth muscle, Cell. Tiss. Res. 156: 2–16.Google Scholar
  13. Choi, J. K., 1962, Fine structure of the smooth muscle of chicken gizzard, in: Fifth International Congress for Electron Microscopy, Philadelphia M9, Academic Press, New York.Google Scholar
  14. Cooke, P. H., and Chase, R. H., 1971, Potassium chloride insoluble myofilaments in vertebrate smooth muscle cells, Exp. Cell Res. 66: 417–425.PubMedGoogle Scholar
  15. Cooke, P. H., and Fay, F. S., 1972a, Correlation between fiber length, ultrastructure, and the length-tension relationship of mammalian smooth muscle, Cell Biol. 52: 105–116.Google Scholar
  16. Cooke, P. H., and Fay, F. S., 1972b, Thick myofilaments in contracted and relaxed mammalian smooth muscle cells, Exp. Cell Res. 71: 265–272.PubMedGoogle Scholar
  17. Csapo, A., 1948, Actomyosin content of the uterus, Nature (London) 162: 218–219.PubMedGoogle Scholar
  18. De Petris, S., Karlsbad, G., and Pernis, B., 1962, Filamentous structures in the cytoplasm of normal mononuclear phagocytes,/. Ultrastruct. Res. 7: 39–55.Google Scholar
  19. Dessouky, A. D., 1968, Electron microscopic studies of the myometrium of the guinea pig: The smooth muscle cell of the myometrium before and during pregnancy, Am. J. Obstet. Gynecol. 100: 1117–1123.Google Scholar
  20. Dessouky, A. D., 1971, Myometrial changes in postpartum uterine involution, Am. J. Obstet. 110: 318–329.Google Scholar
  21. Devine, C. E., and Somylo, A. P., 1971, Thick filaments in vascular smooth muscle, Cell Biol. 49: 636–649.Google Scholar
  22. Devine, C. E., Simpson, F. O., and Bertaud, W. S., 1971, Surface features of smooth muscle cells from the mesenteric artery and vas deferens, Cell Biol. 8: 427–443.Google Scholar
  23. Devine, C. E., Somlyo, A. V., and Somlyo, A. P., 1972, Sarcoplasmic reticulum and excitation contraction coupling in mammalian smooth muscles, Cell Biol. 52: 690–718.Google Scholar
  24. Devine, C. E., Somlyo, A. V., and Somyo, A. P., 1973, Sarcoplasmic reticulum and mitochondria as cation accumulation sites in smooth muscle, Philos. Trans. R. Soc. London Ser. B 265: 17–23.Google Scholar
  25. Dewey, M. M., and Barr, L., 1968, Structure of vertebrate intestinal muscle, in: Handbook of Physiology, Sect. 6: Alimentary Canal, Vol. 4 ( O. F. Code, ed.), pp. 1629–1654, American Physiological Society, Washington, D.C.Google Scholar
  26. Ebashi, S., and Endo, M., 1968, Calcium ion and muscle contraction, Prog. Biophys. Mol. Biol. 18: 123–183.PubMedGoogle Scholar
  27. Ebashi, E., Endo, M., and Ohtsuki, I., 1969, Control of muscle contraction, Q. Rev. Biophys. 2: 351–384.Google Scholar
  28. Elliott, G. F., 1964, X-ray diffraction studies on striated and smooth muscles, Proc. R. Soc. London Ser. B 160: 467–472.Google Scholar
  29. Elliott, G. F., 1967, Variations of the contractile apparatus in smooth and striated muscles: X-ray diffraction studies at rest and in contraction,/. Gen. Physiol. 50: 171–184.Google Scholar
  30. Elliott, G. F., and Lowy, J., 1968, Organization of actin in a mammalian smooth muscle, Nature (London) 219: 156–157.PubMedGoogle Scholar
  31. Fawcett, D. W., 1966, The Cell: An Atlas of Fine Structure, p. 255, Saunders, Philadelphia.Google Scholar
  32. Fay, F. S., and Cooke, P. H., 1973, Reversible disaggregation of myofilaments in vertebrate smooth muscles, Cell Biol. 56: 399–411.Google Scholar
  33. Forssman, W. G., and Girardier, L., 1970, A study of the T system in rat heart, Cell Biol. 44: 1–19.Google Scholar
  34. Franzini-Armstrong, C., and Porter, K. R., 1964, Sarcolemmal invaginations and the T-system in fish skeletal muscle, Nature (London) 202: 355–357.Google Scholar
  35. Frederici, H. H. R., and DeCloux, R. J., 1968, The early response of immature rat myometrium to estrogenic stimulation,/. Ultrastruct. Res. 22: 402–412.Google Scholar
  36. Freeman-Narrod, M., and Goodford, P. J., 1962, Sodium and potassium content of the smooth muscle of guinea-pig taenia coli at different temperatures and tensions, Physiol. (London) 163: 399–410.Google Scholar
  37. Gabella, G., 1971, Caveolae intracellulars and sarcoplasmic reticulum in smooth muscle, Cell Sci. 8: 601 - 609.Google Scholar
  38. Gabella, G., 1973, Fine structure of smooth muscle, Philos. Trans. R. Soc. London Ser. B 265: 7–16.Google Scholar
  39. Garamvôlgyi, N., Vizi, E. S., and Knoll, J., 1971, The regular occurrence of thick filaments in stretched mammalian smooth muscle, Ultrastruct. Res. 34: 135–143.Google Scholar
  40. Gorski, J., and Nelson, N. J., 1965, Ribonucleic acid synthesis in the rat uterus and its early response to estrogen, Arch. Biochem. Biophys. 110: 284–290.PubMedGoogle Scholar
  41. Grôschel-Stewart, U., Chamley, J. H., McConnell, J., and Burnstock, G., 1975, Comparison of the reaction of cultured smooth and cardiac muscle cells and fibroblasts to specific antibodies to myosin, Histochemistry 43: 215–224.Google Scholar
  42. Gupta, B. L., and Little, C., 1975, Ultrastructure, phylogeny and Pogonophora, Z. Zool. Syst. Evolutionsforsch. Suppl., p. 45.Google Scholar
  43. Hanson, J., and Huxley, H. E., 1955, The structural basis of contraction in striated muscles, Symp. Soc. Exp. Biol. 9: 228–264.Google Scholar
  44. Hanson, J., and Lowy, J., 1964, The structure and the origin of the axial periodicity in the I substance of vertebrate striated muscles, Proc. R. Soc. London Ser. B 160: 449–460.Google Scholar
  45. Hanson, J., and Lowy, J., 19646, The problem of the location of myosin in vertebrate smooth muscle, Proc. R. Soc. London Ser. B 160: 523–524.Google Scholar
  46. Herlihy, J. T., and Murphy, R. A., 1974, Force-velocity and series elastic characteristics of smooth muscle from the hog carotid artery, Circ. Res. 34: 461–466.PubMedGoogle Scholar
  47. Heumann, H. G., 1969, Localization of myosin and actin in vertebrate smooth muscle, Zool. Anz. (Suppl. BD 33 Verh. Zool.), pp. 416–424.Google Scholar
  48. Heumann, H. G., 1970, A regular actin filament lattice in a vertebrate smooth muscle, Experientia 26: 1131.PubMedGoogle Scholar
  49. Heumann, H. G., 1971, Mechanism of smooth muscle contraction: An electron microscope study of the mouse large intestine, Cytobiologie 3: 259–281.Google Scholar
  50. Heumann, H. G., 1973, Smooth muscle: Contraction hypothesis based on the arrangement of actin and myosin filaments in different states of contraction, Philos. Trans. R. Soc. London Ser. B 265: 213–217.Google Scholar
  51. Huxley, H. E., 1957, The double array of filaments in cross-striated muscles, Biophys. Biochem. Cytol. 3: 631–649.Google Scholar
  52. Huxley, H. E., 1963, Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle,/. Mol. Biol. 7: 281–308.Google Scholar
  53. Huxley, H. E., 1964, Evidence for continuity between the central elements of the triads and extracellular space in frog sartorius muscle, Nature (London) 202: 1067–1071.PubMedGoogle Scholar
  54. Huxley, H. E., 1969, The mechanism of muscular contraction, Science 164: 1356–1366.PubMedGoogle Scholar
  55. Huxley, H. E., 1971, The structural basis of muscular contraction, Proc. R. Soc. London Ser. B 178: 131–149.Google Scholar
  56. Huxley, H. E., and Brown, W., 1967, The low angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor, Mol. Biol. 30: 383–434.Google Scholar
  57. Huys, J., 1961, Isolement et propriétés de la tonoactomosine dutérus de vache, Arch. Int. Physiol. Biochim. 69: 677–700.PubMedGoogle Scholar
  58. Ishikawa, H., Bischoff, R., and Holtzer, H., 1968, Mitosis and intermediate filaments in developing skeletal muscle,/. Cell Biol. 38: 538–555.Google Scholar
  59. Ishikawa, H., Bischoff, R., and Holtzer, H., 1969, Formation of arrowhead complexes with heavy meromyosin in a variety of cell types, Cell Biol. 43: 312–328.Google Scholar
  60. Jervell, K. F., Diniz, C. R., and Mueller, G. C., 1958, Early effects of estradiol on nucleic acid metabolism in the rat myometrium,/. Biol. Chem. 231: 945.Google Scholar
  61. Jones, A. W., Somlyo, A. P., and Somlyo, A. V., 1973, Potassium accumulation in smooth muscle and associated ultrastructural changes, Physiol. (London) 232: 247–273.Google Scholar
  62. Kaminer, B., 1969, Synthetic myosin filaments from vertebrate smooth muscle, J. Mol. Biol. 39: 257–264.PubMedGoogle Scholar
  63. Kao, K.-Y. T., Hitt, W. E., Bush, A. T., and McGavack, T. H., 1964, Connective tissue. XII. Stimulating effects of estrogens on collagen synthesis in rat uterine slices, Proc. Soc. Exp. Biol. Med. 117: 86–97.PubMedGoogle Scholar
  64. Kelly, R. E., and Arnold, J. W., 1972, Myofilaments of the papillary muscles of the iris fixed in situ, J. Ultrastruct. Res. 40: 532–545.Google Scholar
  65. Kelly, R. E., and Rice, R. V., 1968, Localization of myosin filaments in smooth muscle, Cell Biol. 37: 105–116.Google Scholar
  66. Kendrick-Jones, J., 1973, The sub-unit structure of gizzard myosin, Philos. Trans. R. Soc. London Ser. B 265: 183–189.Google Scholar
  67. Keyserlingk, D. G., 1970, Ultrastruktur glycerinextrahierter Dunndarm-muskelzellen der Ratte vor und nach Kontraktion, Z. Zellforsch. Mikrosk. Anat. 111: 559–571.Google Scholar
  68. Krames, B., and Page, E., 1968, Effects of electron microscopic fixatives on cell membranes of the perfused rat heart, Biochim. Biophys. Acta 150: 24–31.Google Scholar
  69. Kristensen, B. I., Nielsen, L. E., and Rostgaard, J., 1971, A two filament system and interaction of heavy meromyosin (HMM) with thin filaments in smooth muscle, Z. Zellforsch. 122: 350–356.Google Scholar
  70. Laguens, R., 1964, Effect of estrogen upon the fine structure of uterine smooth muscle cell of the rat, Ultrastruct. Res. 10: 578 - 584.Google Scholar
  71. Laguens, R., and Lagrutta, J., 1964, Fine structure of human uterine muscle in pregnancy, Am. J. Obstet. Gynecol. 89: 1040–1049.PubMedGoogle Scholar
  72. Laszt, L., and Hamoir, G., 1961, Etude par électrophorèse et ultracentrifugation de la composition protéinique de la couche musculaire des carotides de bovidé, Biochim. Biophys. Acta 50: 430–449.PubMedGoogle Scholar
  73. Lowey, S., and Cohen, C., 1962, Studies on the structure of myosin Mol. Biol. 4: 293–308.Google Scholar
  74. Lowey, S., Slayter, H. S., Weeds, A. G., and Baker, H., 1969, The substructure of the myosin molecule. I. Subfragments of myosin by enzymic degradation,/. Mol. Biol. 42: 1–29.Google Scholar
  75. Lowy, J., and Small, J. V., 1970, The organization of myosin and actin in vertebrate smooth muscle, Nature (London) 227: 1–6.Google Scholar
  76. Lowy, J., Poulson, F. R., and Vibert, P. J., 1970, Myosin filaments in vertebrate smooth muscle, Nature (London) 225: 1053–1054.PubMedGoogle Scholar
  77. Lowy, J., Vibert, P. J., Haselgrove, J. C., and Poulson, F. R., 1973, The structure of the myosin elements in vertebrate smooth muscle, Philos. Trans. R. Soc. London Ser. B 265: 191–196.Google Scholar
  78. Lowy, J., Poulson, F. R., and Pedersen, J., 1974, personal communication.Google Scholar
  79. McCullagh, K. A., and Balian, G., 1975, Collagen characterisation and cell transformation in human atherosclerosis, Nature (London) 258: 73–75.PubMedGoogle Scholar
  80. Moore, P. B., Huxley, H. E., and DeRosier, D. J., 1970, Three-dimensional reconstruction of F- actin, thin filaments and decorated thin filaments, Mol. Biol. 50: 279–295.Google Scholar
  81. Murphy, R. A., Herlihy, J. T., and Megerman, J., 1974, Force-generating capacity and contractile protein content of arterial smooth muscle, Gen. Physiol. 64(6): 691–705.Google Scholar
  82. Nachmias, V. T., 1972, Filament formation by purified Physarum myosin, Proc. Natl. Acad. Sci. USA 60: 2011–2014.Google Scholar
  83. Needham, D. M., 1971, Machina Carnis pp. 545–577, Cambridge University Press, Cambridge.Google Scholar
  84. Needham, D. M., and Shoenberg, C. F., 1964, Proteins of the contractile mechanism of mammalian smooth muscle and their possible location in the cell, Proc. R. Soc. London Ser. B 148: 517–522.Google Scholar
  85. Needham, D. M., and Shoenberg, C. F., 1967, The biochemistry of the myometrium, in: Cellular Biology of the Uterus ( R. M. Wynn, ed.), pp. 291–352, Appleton-Century-Crofts, New York.Google Scholar
  86. Needham, D. M., and Shoenberg, C. F., 1968, Proteins of the contractile mechanism in vertebrate smooth muscle, in: Handbook of Physiology, Sect. 6: Alimentary Canal, Vol. 4 ( O. F. Code, ed.), pp. 1793–1810, American Physiological Society, Washington, D.C.Google Scholar
  87. Needham, D. M., and Williams, J. M., 1959, Some properties of uterus actomyosin and myofilaments, Biochem. J. 73: 171 - 181.PubMedGoogle Scholar
  88. Nonomura, Y., 1968, Myofilaments in smooth muscle of guinea pigs taenia coli,. Cell Biol. 39: 741–745.Google Scholar
  89. Panner, B. J., and Honig, C. R., 1967, Filament ultrastructure and organization in vertebrate smooth muscle: Contraction hypothesis based on localization of actin and myosin, Cell Biol. 35: 303–321.Google Scholar
  90. Panner, B. J., and Honig, C. R., 1970, Locus and state of aggregation of myosin in tissue sections of vertebrate smooth muscle,/. Cell Biol. 44: 52–61.Google Scholar
  91. Parker, F., and Odland, G. F., 1966, A light microscope, histochemical and electron microscope study of experimental atherosclerosis in rabbit coronary artery and a comparison with rabbit aorta atherosclerosis, Am. Pathol 48: 451–481.Google Scholar
  92. Peachey, L. D., 1965, The sarcoplasm reticulum and transverse tubules of the frog sartorius, Cell Biol. 25: 209–232.Google Scholar
  93. Pollard, T. D., and Ito, S., 1974, The role of filaments in consistency changes and movement, Cell Biol. 46: 267–289.Google Scholar
  94. Pollard, T. D., and Weihing, R. R., 1974, Actin and myosin and cell movement, CRC Crit. Rev. Biochem. 2: 1–65.PubMedGoogle Scholar
  95. Popescu, L. M., and Ionescu, N., 1970, On the equivalence between dense bodies and Z bands, Experientia 26: 624–643.Google Scholar
  96. Porter, K. R., and Palade, G. E., 1957, Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells, Biophys. Biochem. Cytol. 3: 269–300.Google Scholar
  97. Rice, R. V., Moses, J. A., McManus, G. M., Brady, A. C., and Blasik, L. M., 1970, The organization of contractile filaments in a mammalian smooth muscle, Cell Biol. 47: 183–196.Google Scholar
  98. Rosenbluth, J., 1965, Smooth muscle on ultrastructural basis for the dynamics of its contraction, Science 148: 1337–1339.PubMedGoogle Scholar
  99. Rosenbluth, J., 1971, Myosin-like aggregates in trypsin-treated smooth muscle cells, Cell Biol. 48: 174–188.Google Scholar
  100. Ross, R., and Klebanoff, S. J., 1967, Fine structural changes in uterine smooth muscle and fibroblasts in response to estrogen, Cell Biol. 32: 155–167.Google Scholar
  101. Shoenberg, C. F., 1958, An electron microscope study of smooth muscle in pregnant uterus of rabbit, Biophys. Biochem. Cytol. 4: 609–614.Google Scholar
  102. Shoenberg, C. F., 1962, Some electron microscope observations on the contraction mechanism in vertebrate smooth muscle, in: Fifth International Congress for Electron Microscopy, Philadelphia M8, Academic Press, New York.Google Scholar
  103. Shoenberg, C. F., 1967, Abst. Br. Biophys. Soc. Muscle Meeting p. 8.Google Scholar
  104. Shoenberg, C. F., 1969«, An electron microscope study of the influence of divalent ions on myosin filament formation in chicken gizzard extracts and homogenates, Tissue Cell 1: 83–96.Google Scholar
  105. Shoenberg, C. F., 19696, A study of myosin filaments in extracts and homogenates of vertebrate smooth muscle, Angiologica 6: 233–246.Google Scholar
  106. Shoenberg, C. F., 1973, The influence of temperature on thick filaments of vertebrate smooth muscle, Philos. Trans. R. Soc. London Ser. B 265: 197–202.Google Scholar
  107. Shoenberg, C. F., and Haselgrove, J. C., 1974, Filaments and ribbons in vertebrate smooth muscle, Nature (London) 249: 152–154.PubMedGoogle Scholar
  108. Shoenberg, C. F., and Needham, D. M., 1976, A study of the mechanism of contraction in vertebrate smooth muscle, Biol. Rev. 1976: 53–104.Google Scholar
  109. Shoenberg, C. F., Goodford, P. J., Wolowyk, M. W., and Wootton, G. S., 1973, Ion changes during smooth muscle fixation for electron microscopy, Mechanochem. Cell Motility 2: 69–82.Google Scholar
  110. Small, J V., 1974, Contractile units in vertebrate smooth muscle, Nature (London) 249:324–327.Google Scholar
  111. Small, J. V., 1976, The contractile apparatus of the smooth muscle cell: Structure and composition, (in press).Google Scholar
  112. Small, J. V., and Sobieszek, A., 1973, The core component of the myosin containing elements of vertebrate smooth muscle, Cold Spring Harbor Symp. Quant. Biol. 37: 439–442.Google Scholar
  113. Small, J. V., and Squire, J. M., 1972, Structural basis of contraction in vertebrate smooth muscle, Mol. Biol. 67: 117–149.Google Scholar
  114. Sobieszek, A., 1972, Cross-bridges on self assembled smooth muscle myosin, Mol. Biol. 70: 741–744.Google Scholar
  115. Sobieszek, A., and Small, J. V., 1973a, The assembly of ribbon-shaped structures in low ionic strength extracts obtained from vertebrate smooth muscle, Philos. Trans. R. Soc. London Ser. B 265: 203–212.Google Scholar
  116. Sobieszek, A., and Small, J. V., 19736, Filaments from purified smooth muscle myosin, Cold Spring Harbor Symp. Quant. Biol 37: 109–112.Google Scholar
  117. Somlyo, A. P., Devine, C. E., Somlyo, A. V., and North, S. R., 1971a, Sarcoplasmic reticulum and temperature dependent contraction of smooth muscle in calcium free solution, J. Cell Biol 51: 722–741.PubMedGoogle Scholar
  118. Somlyo, A. P., Somlyo, A. V., Devine, C. E., and Rice, R. V., 19716, Aggregation of thick filaments into ribbons in mammalian smooth muscle, Nature (London) New Biol 231: 243–246.Google Scholar
  119. Somylo, A. P., Devine, C. E., Somlyo, A. V., and Rice, R. V., 1973, Filament organization in vertebrate smooth muscle, Philos. Trans. R. Soc. London Ser. B 265: 223–229.Google Scholar
  120. Somylo, A. V., and Somlyo, A. P., 1971, Strontium accumulation by sarcoplasmic reticulum and mitochondria in vascular smooth muscle, Science 174: 955–958.Google Scholar
  121. Somylo, A. V., Devine, C. E., and Somlyo, A. P., 1971, Thick filaments in unstretched mammalian smooth muscle, Nature (London) New Biol. 233: 218–219.Google Scholar
  122. Tanaka, Y., 1964, Fibrillar structures in the cells of blood forming organs, Natl. Cancer Inst. 33: 467–486.Google Scholar
  123. Thomas, W. A., Jones, R., Scott, R. F., Morrison, E., Goodale, F., and Imai, H., 1963, Production of early atherosclerotic lesions in rats characterized by proliferation of modified smooth muscle cells, Exp. Mol. Pathol. Suppl. 1: 40–48.Google Scholar
  124. Tregear, R. T., and Squire, J. M., 1973, Myosin content and filament structure in smooth and striated muscle, Mol. Biol. 77: 279 - 290.Google Scholar
  125. Uehara, Y., Campbell, G. R., and Burnstock, G., 1971, Cytoplasmic filaments in developing and adult vertebrate smooth muscle, Cell Biol. 50: 484–497.Google Scholar
  126. Vibert, P. J., Haselgrove, J. C., Lowy, J., and Poulson, P. R., 1972, Structural changes in actin- containing filaments of muscle, Mol. Biol. 71: 757–767.Google Scholar
  127. Wachsberger, P. R., and Pepe, F. A., 1974, Purification of uterine myosin and synthetic filament formation, Mol. Biol. 88: 385–391.Google Scholar
  128. Wells, G. S., and Wolowyk, M. W., 1971, Freeze-etch observations on membrane structure in smooth muscle of guinea-pig taenia coli, Physiol. (London) 218: 11–13 P.Google Scholar
  129. Winegrad, S., 1965, (1) Autoradiographic studies of intracellular calcium in frog skeletal muscle, Gen. Physiol. 48: 455 - 479.Google Scholar
  130. Yamauchi, A., and Burnstock, G., 1967, Post-natal development of smooth muscle cells in the mouse vas deferens: A fine structural study. Anat. 104: 1–15.Google Scholar
  131. Yohro, T., and Burnstock, G., 1973, Filament bundle and contractility of endothelial cells in coronary arteries, Z. Zellforsch. Mikrosk. Anat. 138: 85–95.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1977

Authors and Affiliations

  • C. F. Shoenberg
    • 1
  1. 1.Department of AnatomyUniversity of CambridgeCambridgeEngland

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