Ultrastructure of Smooth Muscle

  • A. P. Somlyo
  • Avril V. Somlyo


Identification of the anatomical sources of the increased intracellular free calcium that activates contraction in smooth muscle has been a major objective of cell pharmacology. The extracellular fluid, the space between the basement membrane and the plasma membrane, the plasma membrane itself, and intracellular organelles each has been considered as a possible source and sink of calcium during, respectively, excitation and inhibition (for reviews see Bohr, 1964; Daniel, 1965; Goodford, 1965; A. P. Somlyo and Somlyo, 1968; 1970; Hurwitz and Suria, 1971; Johansson, 1971). In the striated (twitch skeletal) muscles the sarcosplasmic reticulum is the intracellular “site” that accumulates calcium during relaxation and from which the calcium that activates contraction is released by the action potential (for reviews see Bianchi, 1968; A. F. Huxley, 1971). Recent studies have shown that some smooth muscles can be stimulated to contract even if the extracellular calcium concentration is reduced below the levels that can activate contraction (Bozler, 1969; A. P. Somlyo and Somlyo, 1970; A. P. Somlyo et al., 1971b; Devine, Somlyo, and Somlyo, 1972; Keatinge, 1972), indicating the existence of an intracellular source of activator calcium. Recent electron microscopic studies have therefore been directed toward determining whether there is in smooth muscles a sarcoplasmic reticulum that may serve as an intracellular calcium storage site.


Smooth Muscle Sarcoplasmic Reticulum Intermediate Filament Thin Filament 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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aikawa, M. and Koletsky, S. 1970. Arteriosclerosis of the mesenteric arteries of rats and renal hypertension. Am. J. Pathol., 61:293–304.PubMedGoogle Scholar
  2. Altura, B. M. and Altura, B. T. 1970. Differential effects of substrate depletion on drug-induced contractions of rabbit aorta. Am. J. Physiol., 219:1698–1705.PubMedGoogle Scholar
  3. Appleton, T. C. 1972. “Dry” ultra-thin frozen sections for electron microscopy and x-ray microanalysis: the cryostat approach. Micron, 3: 101–105.CrossRefGoogle Scholar
  4. April, E. W., Brandt, P. W., and Elliott, G. F. (1972). The myofilament lattice: studies on isolated fibers. II. The effects of osmotic strength, ionic concentration, and pH upon the unit-cell volume. J. Cell Biol.,55: 53–65.CrossRefGoogle Scholar
  5. Arvill, A., Johansson, B., and Jonsson, O. 1969. Effects of hyperosmolarity on the volume of vascular smooth muscle cells and the relation between cell volume and muscle activity. Acta Physiol. Scand., 75:484–495PubMedCrossRefGoogle Scholar
  6. Barr, L., Berger, W., and Dewey, M. M. 1968. Electrical transmission at the nexus between smooth muscle cells. Gen. Physiol., 51:347–368CrossRefGoogle Scholar
  7. Beaman, D. R. and Isasi, J. A. 1972. Electron Beam Microanalysis. Am. Soc. Test. Mater. Spec. Tech. Publ. 506.Google Scholar
  8. Bergman, R. 1968. Uterine smooth muscle fibers in castrate and estrogen-treated rats. J. Cell Biol.,36:639–648.PubMedCrossRefGoogle Scholar
  9. Bhagwat, A. G. and Wong, P. 1972. Effect ofpH in direct OSO4 fixation on glycogen staining as shown by electron microscopy. Stain Technology,, 47:3940.Google Scholar
  10. Bianchi, C. P. 1968. Cell Calcium. Appleton-Century-Crofts, New York.Google Scholar
  11. Bo, W. J., Odor, D. L., and Rothrock, M. 1968. The fine structure of uterine smooth muscle of the rat uterus at various time intervals following a single injection of estrogen. Am. J. Anat., 123: 369–384.PubMedCrossRefGoogle Scholar
  12. Bohr, D. F. 1964. Electrolytes and smooth muscle contraction. Pharmacol. Rev.,, 76:85–111.Google Scholar
  13. Bone, Q. and Denton, E. J. 1971. The osmotic effects of electron microscope fixatives. Cell Biol., 49:517–581.CrossRefGoogle Scholar
  14. Borle, A. B. 1970. Kinetic analyses of calcium movements in cell cuhures. IV. Effects of phosphate and parathyroid hormone in kidney cells. Endocrinol., 56:1389–1393.CrossRefGoogle Scholar
  15. Bozler, E. 1969. Role of calcium in initiation of activity of smooth muscle. Am. J. Physiol., 216.611–674.Google Scholar
  16. Brading, A. F. 1970. Osmotic phenomena in smooth muscle. In: Smooth Muscle, pp. 166–196. Ed. by Bülbring, E., Brading, A. F., Jones, A. W., and Tomita, T. Edward Arnold, London.Google Scholar
  17. Brading, A. F. and Setekleiv, J. 1968. The effect of hypo- and hypertonic solutions on volume and ion distribution of smooth muscle of guinea-pig taenia coli. J. Physiol. (Lond.), 195 107–118.Google Scholar
  18. Brandt, P. W., Lopez, E., Reuben, J. P., and Grundfest, H. 1967. The relationship between myofilament packing density and sarcomere length in frog striated muscle. J. Cell Biol, 33: 255–264.PubMedCrossRefGoogle Scholar
  19. Brayser, M., Casley-Smith, J. R., and Green, B. 1971. A new small molecular tracer for permeability studies with the electron microscope. Experientia, 27:115–116.PubMedCrossRefGoogle Scholar
  20. Burnstock, G. 1970. Structure of smooth muscle and its innervation. In: Smooth Muscle, pp. 1–69. Ed. by Bülbring, E., Brading, A. F., Jones, A. W., and Tomita, T. Edward Arnold, London.Google Scholar
  21. Burnstock, G. 1974. This volume, Part II, Chapter 5.Google Scholar
  22. Busson-Mabillot, S. 1971. Influence de la fixation chimique sur les ultrastructures. I. Etude sur les organites du follicule Ovarien d’un poisson teleosteen. J. de Microscopic, 72:317–348.Google Scholar
  23. Campbell, G. R., Uehara, Y., Malmfors, T., and Burnstock, G. 1971a. Degeneration and regeneration of smooth muscle transplants in the anterior eye chamber. Z. Zellforsch., 117:155–175.PubMedCrossRefGoogle Scholar
  24. Campbell, G. R., Uehara, Y., Mark, G., and Burnstock, G. 1971b. Fine structure of smooth muscle cells grown in tissue culture. J. Cell Biol.,49:21–34.PubMedCrossRefGoogle Scholar
  25. Chau-Wong, M. and Seeman, P. 1971. The control of membrane-bound Ca2+ by ATP. Biochim. Biophys. Acta, 241:473–482PubMedCrossRefGoogle Scholar
  26. Christensen, A. K. 1971. Frozen thin sections of fresh tissue for electron microscopy, with a description of pancreas and liver. J. Cell Biol.,57:772–804.CrossRefGoogle Scholar
  27. Cliff, W. J. 1971, The ultrastructure of aortic elastica as revealed by prolonged treatment with OSO4. Exp. Mol Pathol, 75:220–229.CrossRefGoogle Scholar
  28. Cobb, J. L. S. and Bennett, T. 1969. A study of nexuses in visceral smooth muscle. J. Cell Biol.,41:287–297.PubMedCrossRefGoogle Scholar
  29. Conti, G., Haenni, B., Laszt, L., and Rouiller, Ch. 1964. Structure et ultrastructure de la cellule musculaire lisse de la paroi carotidienne a I’etat de repos et a I’etat de contraction. Angiologica, 1:119–140.PubMedGoogle Scholar
  30. Cooke, P. H. and Chase, R. H. 1971. Potassium chloride-insoluble myofilaments in vertebrate smooth muscle cells. Exp. Cell Res., 66:417–425.PubMedCrossRefGoogle Scholar
  31. Cooke, P. H. and Fay, F. S. 1972. Thick myofilaments in contracted and relaxed mammalian smooth muscle cells. Exp. Cell Res., 77:265–272.CrossRefGoogle Scholar
  32. Daniel, E. E. 1963. On roles of calcium, strontium and barium in contraction and excitability of rat uterine muscle. Arch. Int. Pharmacodyn., 746:298–349.Google Scholar
  33. Daniel, E. E. 1965. Attempted synthesis of data regarding divalent ions in muscle function. In: Muscle., pp. 295–313. Ed. by Paul, W. M., Daniel, E. E., Kay, C. M., and Monckton, G. Pergamon Press, London.Google Scholar
  34. Dessouky, D. A. 1968. Electron microscopic studies of the myometrium of the guinea pig. Am. J. Obst. Gynecol., 700:30–41.Google Scholar
  35. Devine, C. E., Simpson, F. O., and Bertaud, W. S. 1971. Surface features of smooth muscle cells from the mesenteric artery and vas deferens. J. Cell Sci., 8:427–443.PubMedGoogle Scholar
  36. Devine, C. E. and Somlyo, A. P. 1971. Thick filaments in vascular smooth muscle. J. Cell Biol.,49:636–649.PubMedCrossRefGoogle Scholar
  37. Devine, C. E., Somlyo, A. V., and Somlyo, A. P. 1972. Sarcoplasmic reticulum and excitation-contraction coupling in mammalian smooth muscles. J. Cell Biol.,52:690–718.PubMedCrossRefGoogle Scholar
  38. Devine, C. E., Somlyo, A. V., and Somlyo, A. P. 1973. Sarcoplasmic reticulum and mitochondria as cation accumulating sites in smooth muscle. Phil Trans. R. Soc. B., 265:17–23.PubMedCrossRefGoogle Scholar
  39. Ebashi, S. 1971. Comparative aspect of structural proteins of muscle with particular reference to regulatory proteins. In: Vascular Neuroeffector Systems., pp. 190–201. Ed. by Bevan, J. A., Furchgott, R. F., Maxwell, R. A., and Somlyo, A. P. Basel, S. Karger.Google Scholar
  40. Elias, H., Hennig, A., and Schwartz, D. E. 1971. Stereology: applications to biomedical research. Physiol. Rev., 57:158–200.Google Scholar
  41. Elliott, G. F. and Lowy, J. 1968. Organization of actin in a mammalian smooth muscle. Nature., 219: 156–157.PubMedCrossRefGoogle Scholar
  42. Feder, N. 1971. Microperoxidase. An ultrastructural tracer of low molecular weight. J. Cell Biol., 51:339–343.PubMedCrossRefGoogle Scholar
  43. Franzini-Armstrong, C. and Porter, K. R. 1964. Sarcolemmal invaginations constituting the T-system in fish muscle fibers. J. Cell Biol., 22:675–696.PubMedCrossRefGoogle Scholar
  44. Gabella, G. 1971. Caveolae intracellulares and sarcoplasmic reticulum in smooth muscle. J. Cell Sci., 5:601–609.Google Scholar
  45. Garamvölgyi, N., Vizi, E. S., and Knoll, J. 1971. The regular occurrence of thick filaments in stretched mammalian smooth muscle. J. Ultrastruct. Res., 8: 135–143.CrossRefGoogle Scholar
  46. Goodford, P. J. 1965. The distribution of calcium in intestinal smooth muscle. In: Muscle., pp. 219–228. Ed. by Paul, W. M., Daniel, E. E., Kay, C. M., and Monckton, G. Pergamon Press, London.Google Scholar
  47. Goodford, P. J. 1967. The calcium content of the smooth muscle of the guinea-pig taenia coli. J. Physiol., 792:145–157.Google Scholar
  48. Goodford, P. J. and Wolowyk, M. W. 1972. Localization of cation interactions in the smooth muscle. J. Physiol. (Lond.), 224:521.Google Scholar
  49. Grantham, J., Cuppage, F. E., and Fanestil, D. 1971. Direct observation of toad bladder response to vasopressin. J. Cell Biol., 48:695–699.PubMedCrossRefGoogle Scholar
  50. Hackenbrock, C. R. 1972. Energy-linked ultrastructural transformations in isolated liver mitochondria and mitoplasts. Preservation of configurations by freeze-cleaving compared to chemical fixation. J. Cell Biol., 53:450–465.PubMedCrossRefGoogle Scholar
  51. Hall, T. A. 1971. The microprobe assay of chemical elements. In: Physical Techniques in Biological Research, 2nd ed. Vol. I A, p. 158. Ed. by G. Oster. Academic Press, New York.Google Scholar
  52. Hall, T. A. 1974. Preparation of frozen-hydrated tissue sections for x-ray microanalysis in the scanning electron microscope. Nature., 247:113–115.PubMedCrossRefGoogle Scholar
  53. Hama, K. and Porter, K. R. 1969. An application of high voltage electron microscopy to the study of biological materials. J. Microscopie, 8:149–158.Google Scholar
  54. Hammersen, F. Personal communication.Google Scholar
  55. Hanson, J. and Lowy, J. 1963. The structure of F-actin and of actin filaments isolated from muscle. J. Mol. Biol, 6:46–60.CrossRefGoogle Scholar
  56. Hanson, J. and Lowy, J. 1964. Discussion. Proc. Roy. Soc. B, 160:523.CrossRefGoogle Scholar
  57. Harrison, R. G. Lowey, S., and Cohen, C. 1971. Assembly of myosin. J. Mol. Biol., 59:531–535.PubMedCrossRefGoogle Scholar
  58. Henderson, R. M. 1974. Cell-to-cell contacts. This volume. Part I, Chapter 2.Google Scholar
  59. Henderson, R. M., Duchon, G., and Daniel, E. E. 1971. Cell contacts in duodenal smooth muscle layers. Am. J. Physiol., 227:564–574.Google Scholar
  60. Heumann, H.-G. 1970. A regular actin filament lattice in a vertebrate smooth muscle. Experientia, 26:1131–1132.PubMedCrossRefGoogle Scholar
  61. Hoff, H. F. and Gottlob, R. 1969. Studies on the pathogenesis of atherosclerosis with experimental model systems. II. An electron microscopy study on the uptake of egg lipoproteins by endothelial and smooth muscle cells of the doubly-ligated rabbit carotid artery. Virchows Arch. Abt. A. Path. Anat., 348:77–88.CrossRefGoogle Scholar
  62. Hülsemann, J. 1971. Innervation of the umbilical vessels. Electron microscopic studies on the guinea-pig. Z. Zellforsch., 120:137–150.PubMedCrossRefGoogle Scholar
  63. Hurwitz, L. and Suria, A. 1971. The link between agonist action and response in smooth muscle. Ann. Rev. Pharmacol, 11:313–326.CrossRefGoogle Scholar
  64. Huxley, A. F. 1964. Muscle. Ann. Rev. Physiol. 26:131–152.CrossRefGoogle Scholar
  65. Huxley, A. F. 1971. The Croonian Lecture, 1967. The activation of striated muscle and its mechanical response. Proc. Roy. Soc. B, 178:1–27.CrossRefGoogle Scholar
  66. Huxley, H. E. 1957. The double array of filaments in cross-striated muscle. J. Biophys. Biochem. Cytol., 5:631–648.CrossRefGoogle Scholar
  67. Huxley, H. E. 1963. Electron microscope studies on the structure of natural and synthetic filaments from striated muscle. J. Mol. Biol., 7:281–308.PubMedCrossRefGoogle Scholar
  68. Huxley, H. E. 1964. Evidence for continuity between the central elements of the triads and extracellular space in frog sartorius muscle. Nature., 202:1067–1071.PubMedCrossRefGoogle Scholar
  69. Huxley, H. E. 1971. Some new developments in specimen preparation techniques. Phil. Trans. R. Soc. B, 267:119.CrossRefGoogle Scholar
  70. Huxley, H. E. and Brown, W. 1967. The low-angle x-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J. Mol. Biol., 50:383–434.CrossRefGoogle Scholar
  71. Huxley, H. E., Page, S., and Wilkie, D. R. 1963. An electron microscopic study of muscle in hypertonic solutions. J. Physiol. (Lond.) 169:312–329.Google Scholar
  72. Ishikawa, H. 1968. Formation of elaborate networks of T-system tubules in cultured skeletal muscle with special reference to the T-system formation. J. Cell Biol., 55:51–66.CrossRefGoogle Scholar
  73. Ishikawa, H., Bischoff, R., and Holtzer, H. 1968. Mitosis and intermediate-sized filaments in developing skeletal muscle. Cell Biol., 55:538–555.CrossRefGoogle Scholar
  74. Ishikawa, H., Bischoff, R., and Holtzer, H. 1969. Formation of arrowhead complexes with heavy mero- myosin in a variety of cell types. J. Cell Biol.,45:312–328.Google Scholar
  75. Jard, S., Bourguet, J., Carasso, N., and Favard, P. 1966. Action de divers fixateurs sur la permeabilite et I’ultrastructure de la vessie de grenouille. J. Microscopie, 5:31–50.Google Scholar
  76. Johansson, B. 1971. Electromechanical and mechanoelectrical coupling in vascular smooth muscle. Angiologica, 8:129–143.PubMedGoogle Scholar
  77. Jones, A. W., Somlyo, A. P., and Somlyo, A. V. 1973. Potassium accumulation in smooth muscle and associated ultrastructural changes. J. Physiol (Lond), 252:247–273.Google Scholar
  78. Kalt, M. R. and Tandler, B. 1971. A study of fixation of early amphibian embryos for electron microscopy. J. Ultrastruct. Res., 36:633–645.PubMedCrossRefGoogle Scholar
  79. Kaminer, B. 1969. Synthetic myosin filaments from vertebrate smooth muscle. J. Mol. Biol., 59:257–264.CrossRefGoogle Scholar
  80. Karnovsky, M. J. 1967. The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol., 55:213–236.CrossRefGoogle Scholar
  81. Karnovsky, M. J. and Rice, D. F. 1969. Exogenous cytochrome c as an ultrastructure tracer. J. Histochem. Cytochem., 77:751–753.CrossRefGoogle Scholar
  82. Kay, D. H. 1965. Techniques for Electron Microscopy. F. A. Davis, Philadelphia.Google Scholar
  83. Keatinge, W. R. 1972. Ca concentration and flux in Ca-deprived arteries. J. Physiol. (Lond.), 224:35–59.Google Scholar
  84. Kelly, R. E. and Arnold, J. W. 1972. Myofilaments of the pupillary muscles of the iris fixed in situ. J. Ultrastruct. Res., 40:532.PubMedCrossRefGoogle Scholar
  85. Kendrick-Jones, J., Szent-Györgyi, A. G., and Cohen, C. 1971. Segments from vertebrate smooth muscle myosin rods. J. Mol. Biol., 59:527–529.PubMedCrossRefGoogle Scholar
  86. Kosek, J. C., Chartrand, C., Hurley, E. J., and Lower, R. R. 1969. Arteries in canine cardiac homografts. Ultrastructure during acute rejection. Lab. Invest., 27:328–335.Google Scholar
  87. Krames, B. and Page, E. 1968. Effects of electron microscopic fixatives on cell membranes of the perfused rat heart. Biochim. Biophys. Acta, 750:24–31, 1968.Google Scholar
  88. Kuriyama, H., Ohshima, K., and Sakamoto, Y. 1971. The membrane properties of the smooth muscle of the guinea-pig portal vein in isotonic and hypertonic solutions. J. Physiol., 217:179–199.PubMedGoogle Scholar
  89. Laguens, R. 1964. Effect of estrogen upon the fine structure of the uterine smooth muscle cell of the rat. Ultrastruct. Res., 70:578–584.CrossRefGoogle Scholar
  90. Lee, K. T., Lee, K. J., Lee, S. K., Imai, H., and O’Neal, R. M. 1970. Poorly differentiated subendothelial cells in swine aortas. Exp. Mol. Pathol., 75:118–129.CrossRefGoogle Scholar
  91. Loud, A. V. 1968. A quantitative stereological description of the ultrastructure of normal rat liver parenchymal cells. J. Cell Biol., 57:27–46.CrossRefGoogle Scholar
  92. Lowy, J. and Small, J. V. 1970. The organization of myosin and actin in vertebrate smooth muscle. Nature., 227:46–51.PubMedCrossRefGoogle Scholar
  93. Lowy, J., Poulsen, F. R., and Vibert, P. J. 1970. Myosin filaments in vertebrate smooth muscle. Nature., 225:1053–1054.PubMedCrossRefGoogle Scholar
  94. Luciano, L., Junger, E., and Reale, E. 1968. Glykogen in glatten Muskelzellen der Gefäßwand von Säugetieren. Histochemie, 75:219–228.Google Scholar
  95. Manasek, F. J. 1969. Myocardial cell death in the embryonic chick ventricle. J. Embryol. Exp. Morphol, 27:271–284.Google Scholar
  96. Maunsbach, A. B. 1967. Cited in: Electron Microscopy of Cells and Tissues. Volume I. Instrumentation and Techniques. F. S. Sjöstrand. Academic Press, London.Google Scholar
  97. McGeachie, J. K. 1971. Ultra-structural specificity in regenerating smooth muscle. Experientia, 27:436.CrossRefGoogle Scholar
  98. Millonig, G. 1962. Further observations on a phosphate buffer for osmium solutions in tixation. In: Electron Microscopy, Vol. II, p-8. Fifth International Congress, Philadelphia, Pennsylvania, 1962. Ed. by Breese, Jr., S. S. Academic Press, New York.Google Scholar
  99. Morel, F. M. M., Baker, R. F., and Wayland, H. 1971. Quantitation of human red blood cell fixation by glutaraldehyde. 7. Cell Biol., 48:91–100.PubMedCrossRefGoogle Scholar
  100. Moss, N. S. and Benditt, E. P. 1970a. Spontaneous and experimentally induced arterial lesions. I. An ultrastructural survey of the normal chicken aorta. Lab. Invest., 22:166–183.PubMedGoogle Scholar
  101. Moss, N. S. and Benditt, E. P. 1970b. The ultrastructure of spontaneous and experimentally induced arterial lesions. III. The cholesterol-induced lesions and the effect of a cholesterol and oil diet on the preexisting spontaneous plaque in the chicken aorta. Lab. Invest., 25:521–535.Google Scholar
  102. Needham, D. M. and Shoenberg, C. F. 1967. The biochemistry of the myometrium. In: Cellular Biology of the Uterus, pp. 291–352. Ed. by Wynn, R. M. Appleton-Century-Crofts, New York.Google Scholar
  103. Nishihara, H. 1970. Some observations on the fine structure of the guinea-pig taenia coli after incubation in hypertonic solution. J. Anat., 107:101–114.PubMedGoogle Scholar
  104. Nonomura, Y. 1968. Myofilaments in smooth muscle of guinea pig’s taenia coli. J. Cell Biol., 59:741–745.CrossRefGoogle Scholar
  105. Northover, B. J. 1968. The effect of drugs on the constriction of isolated depolarized blood vessels in response to calcium or barium. Br. J. Pharmacol., 34:417–428.PubMedGoogle Scholar
  106. Peachey, L. D., Personal communication.Google Scholar
  107. Peachey, L. D. 1965. Electron microscopy of tilted biological sections. Sci. Instrum. (News), 70:7–12.Google Scholar
  108. Pease, D. C. 1964. Histological Techniques for Electron Microscopy. Academic Press, New York.Google Scholar
  109. Pease, D. C. 1968. Structural features of unfixed mammalian smooth and striated muscle prepared by glycol dehydration. J. Ultrastruct. Res., 25:280–303.CrossRefGoogle Scholar
  110. Pease, D. C. and Molinari, S. 1960. Electron microscopy of muscular arteries; pial vessels of the cat and monkey. J. Ultrastruct. Res., 5:447–468.CrossRefGoogle Scholar
  111. Pepe, F. A. 1971. Structural components of the striated muscle fibril. In: Biological Macromolecules Series. Subunits in Biological Systems. Vol. V, Part A, pp. 323–353. Ed. by Timasheff, S. N. and Fasman, G. D. Marcel Dekker, New York.Google Scholar
  112. Prosser, C. L., Burnstock, G., and Kahn, J. 1960. Conduction in smooth muscle: comparative structural properties. Am. J. Physiol., 799:545–582.Google Scholar
  113. Rappoport, S. I. and Bidinger, J. M. 1972. Effect of stretch on survival and ionic content of frog sartorius muscle in vitro. Fed. Proc., 31:324Abs.Google Scholar
  114. Reale, E. and Ruska, H. 1965. Die Feinstruktur der Gefäßwände. Angiologica, 2:314–366.PubMedGoogle Scholar
  115. Reedy, M. K. 1968. Ultrastructure of insect flight muscle. I. Screw sense and structural grouping in the rigor cross-bridge lattice. J. Mol. Biol., 57:155–176.CrossRefGoogle Scholar
  116. Revel, J. P. and Kamovsky, M. J. 1967. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell. Biol, 55: 7.CrossRefGoogle Scholar
  117. Revel, J. P., Napolitano, L., and Fawcett, D. W. 1960. Identification of glycogen in electron micrographs of thin tissue sections. J. Biophys. Biochem. Cytol., 5:575–589.CrossRefGoogle Scholar
  118. Rhodin, J. A. G. 1962. Fine structure of vascular walls in mammals. With special reference to smooth muscle component. Physiol. Rev., 42:48–81.Google Scholar
  119. Rice, R. V. and Brady, A. C. 1972. Biochemical and ultrastructural studies on vertebrate smooth muscle. In: Proc. Cold Spring Harbor Laboratory’s 37 th Ann. Symp. on the Mechanism of Muscle Contraction (in press).Google Scholar
  120. Rice, R. v., Brady, A. C., Depue, R. H., and Kelly, R. E. 1966. Morphology of individual macromolecules and their ordered aggregates by electron microscopy. Biochem. Z., 55:370–394.Google Scholar
  121. 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. J. Cell Biol., 47:183–196.PubMedCrossRefGoogle Scholar
  122. Rice, R. v., McManus, G. M., Devine, C. E., and Somlyo, A. P. 1971. A regular organization of thick filaments in mammalian smooth muscle. Nature. (New Biol.), 257:242–243.Google Scholar
  123. Rome, E. 1968. X-ray diffraction studies of the filament lattice of striated muscle in various bathing media. J. Mol. Biol., 57:331–344.CrossRefGoogle Scholar
  124. Rosenbluth, J. 1971. Myosin-like aggregates in trypsin-treated smooth muscle cells. J. Cell Biol.,48:174–188.PubMedCrossRefGoogle Scholar
  125. Ross, R. 1971. The smooth muscle cell. II. Growth of smooth muscle in culture and formation of elastic fibers. J. Cell Biol., 50:172–186.PubMedCrossRefGoogle Scholar
  126. Ross, R. and Klebanoff, S. J. 1967. Fine structural changes in uterine smooth muscle and fibroblasts in response to estrogen. J. Cell Biol.,32:155–167.PubMedCrossRefGoogle Scholar
  127. Ross, R. and Klebanoff, S. J. 1971. The smooth muscle cell. I. In vivo synthesis of connective tissue proteins. J.CellBiol.,50:159–171.PubMedCrossRefGoogle Scholar
  128. Royal Society. 1972. Discussion meeting on recent developments in vertebrate smooth muscle physiology.Google Scholar
  129. Russ, J. 1972. Resolution and sensitivity of X-ray microanalysis in biological sections by scanning and conventional transmission electron microscopy. Proceedings of the Fifth Annual Scanning Electron Microscope Symposium. Illinois Institute of Technology Research Institute, Chicago, I 11, 73.Google Scholar
  130. Sachs, E. S. and Daems, W.Th. 1966. Microtubules in human aortic intimal cells. Z. Zellforsch., 71:553–558.Google Scholar
  131. Sandborn, E. B., Cote, M. G., Roberge, J., and Bois, P. 1967. Microtubules et filaments cytoplasmiques dans le muscle de mammiferes. J. Microscopie, 6:169–178.Google Scholar
  132. Sanger, J. W. 1971. Formation of synthetic myosin filaments: influence of pH, ionic strength, cation substitution, dielectric constant and method of preparation. Cytobiologie, 450–466.Google Scholar
  133. Shoenberg, C. F. 1958. An electron microscope study of smooth muscle in pregnant uterus of the rabbit. Biophys. ßiochem. Cytol 4, 609–614.CrossRefGoogle Scholar
  134. Shoenberg, C. E. 1969. An electron microscope study of the influence of divalent ions on myosin filament formation in chicken gizzard extracts and homogenates. Tissue and Cell, 7:83–96.CrossRefGoogle Scholar
  135. Shoenberg, C. F. 1973. The influence of temperature on the thick filaments of vertebrate smooth muscle. Phil Trans. R. Soc. B., 265:197–202.PubMedCrossRefGoogle Scholar
  136. Sjöstrand, F. S. 1967. Electron Microscopy of Cells and Tissues. Volume I. Instrumentation and Techniques. Academic Press, London.Google Scholar
  137. Small, J. V. and Squire, J. M. 1972. Structural basis of contraction in vertebrate smooth muscle. J. Mol. Biol., 57:117–149.CrossRefGoogle Scholar
  138. Smetana, K., Gyorkey, F., Gyorkey, P., and Busch, H. 1970. Studies on the ultrastructure of nucleoli in human smooth muscle cells. Exp. Cell Res., 60:175–184.PubMedCrossRefGoogle Scholar
  139. Somlyo, A. P. 1972. Excitation-contraction coupling in vertebrate smooth muscle: correlation of ultra- structure with function. The Physiologist, 75:338–348.Google Scholar
  140. Somlyo, A. P. 1973. Discussion. Symposium on recent developments in vertebrate smooth muscle physiology. Phil. Trans. R. Soc. B, 265:210–212.CrossRefGoogle Scholar
  141. Somlyo, A. P. and Somlyo, A. V. 1968. Vascular smooth muscle. I. Normal structure, pathology, biochemistry and biophysics. Pharmacol. Rev.,, 20:197–272.PubMedGoogle Scholar
  142. Somlyo, A. P. and Somlyo, A. V. 1970. Vascular smooth muscle. II. Pharmacology of normal and hypertensive vessels. Pharmacol. Rev.,, 22:249–353.PubMedGoogle Scholar
  143. Somlyo, A. P., Devine, C. E., and Somlyo, A. V. 1971a. Thick filaments in unstretched mammalian smooth muscle. Nature. (New Biol.), 233:218–219.Google Scholar
  144. Somlyo, A. P., Devine, C. E., Somlyo, A. V., and North, S. R. 1971b. Sarcoplasmic reticulum and the tem-perature-dependent contraction of smooth muscle in calcium-free solutions. J. Cell Biol., 51:722–741.PubMedCrossRefGoogle Scholar
  145. Somlyo, A. V. and Somlyo, A. P. 1968. Electromechanical and pharmacomechanical coupling in vascular smooth muscle. J. Pharmacol. Exp. Ther., 159:129–145.PubMedGoogle Scholar
  146. Somlyo, A. V. and Somlyo, A. P. 1971. Strontium accumulation by sarcoplasmic reticulum and mitochondria in vascular smooth muscle. Science, 174:955–958.PubMedCrossRefGoogle Scholar
  147. Somlyo, A. V., Vinall, P., and Somlyo, A. P. 1969. Excitation-contraction coupling and electrical events in two types of vascular smooth muscle. Microvasc. Res., 28:1634–1642.Google Scholar
  148. Somlyo, A. P., Somlyo, A. V., Devine, C. E., and Rice, R. V. 1971c. Aggregation of thick filaments into ribbons in mammalian smooth muscle. Nature. (New Biol.), 231:242–246.Google Scholar
  149. Somlyo, A. P., Devine, C. E., and Somlyo, A. V. 1972a. Sarcoplasmic reticulum, mitochondria and filament organization in vascular smooth muscle. In: Vascular Smooth Muscle, A Symposium, pp. 119–121. Ed. by Betz, E. Springer-Verlag, Heidelberg.CrossRefGoogle Scholar
  150. Somlyo, A. P., Somlyo, A. V., and Smiesko, V. 1972b. Cyclic AMP and vascular smooth muscle. In: Advances in Cyclic Nucleotide Research, Vol. 1, pp. 175–194. Ed. by Paoletti, R. and Robinson, G. A. Raven Press, New York.Google Scholar
  151. Somlyo, A. P., Devine, C. E., Somlyo, A. V., and Rice, R. V. 1973. Filament organization in vertebrate smooth muscle. Phil. Trans. R. Soc. B, 265:223–229.PubMedCrossRefGoogle Scholar
  152. Somlyo, A. P., Somlyo, A. V, Devine, C. E., Peters, P. D., and Hall, T. A. 1974. Electron microscopy and electron probe analysis of mitochondrial cation accumulation in smooth muscle. J. Cell Biol., 57:723–742.CrossRefGoogle Scholar
  153. Sperelakis, N. and Rubio, R. 1971. Ultrastructural changes produced by hypertonicity in cat cardiac muscle. J. Mol. Cell. Cardiol., 3:139–156.PubMedCrossRefGoogle Scholar
  154. Spurr, A. R. 1969. A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res 26:31–43PubMedCrossRefGoogle Scholar
  155. Stein, O., Eisenberg, S., and Stein, Y. 1971. Morphologic and biochemical changes in smooth muscle cells of aortas in growth-restricted rats. Lab. Invest., 25:149–157.PubMedGoogle Scholar
  156. Tahmisian, T. N. 1964. Use of the freezing point method to adjust the tonicity of fixing solutions. J. Ultrastruct. Res., 70:182–188. Cited in: Pease, D. C. 1964. Histological Techniques for Electron icroscopy.,Academic Press, New York.CrossRefGoogle Scholar
  157. Uehara, Y. and Burnstock, G. 1970. Demonstration of “gap junctions” between smooth muscle cells. J. Cell Biol., 44:215–217.PubMedCrossRefGoogle Scholar
  158. Uehara, Y., Campbell, G. R., and Burnstock, G. 1971. Cytoplasmic filaments in developing and adult vertebrate smooth muscle. J. Cell Biol., 50:484–497.PubMedCrossRefGoogle Scholar
  159. Vibert, P. J., Haselgrove, J. C., Lowy, J., and Poulsen, F. R. 1972. Structural changes in actin-containing filaments of muscle. Nature., 215:182–183.Google Scholar
  160. Vye, M. V. and Fischman, D. A. 1970. The morphological alteration of particulate glycogen by en bloc staining with uranyl acetate. J. Ultrastruct. Res., 33: 278–291.PubMedCrossRefGoogle Scholar
  161. Weibel, E. R. 1972. The value of stereology in analysing structure and function of cells and organs. J. Microscopy, 95:3–13.CrossRefGoogle Scholar
  162. Wuerker, R. B. 1970. Neurofilaments and glial filaments. Tissue and Cell, 2:1–9.PubMedCrossRefGoogle Scholar
  163. Yamauchi, A. and Burnstock, G. 1969. Postnatal development of smooth muscle cells in the mouse vas deferens. A fine structural study. J. Anat., 104:1–15.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1975

Authors and Affiliations

  • A. P. Somlyo
    • 1
    • 2
  • Avril V. Somlyo
    • 1
    • 2
  1. 1.Department of PathologyPresbyterian University of Pennsylvania Medical CenterPhiladelphiaUSA
  2. 2.Departments of Physiology and Pathology, School of MedicineUniversity of PennsylvaniaUSA

Personalised recommendations