Ultrastructure and Calcium Stores in the Myometrium

  • Ray Broderick
  • Karen A. Broderick


This chapter is designed to provide the nonspecialist with an introduction to and an overview of uterine smooth muscle ultrastructure, particularly as it pertains to the development and transmission of force. A detailed description of intracellular calcium storage sites has been included along with a discussion of the release and recycling of activatable calcium in smooth muscle. Because of the paucity of information available in these areas with respect to uterine muscle, much of what is conveyed herein is a generalized summary of data from other visceral muscles as well as vascular smooth muscle, with specific reference to uterine muscle whenever possible. This is not meant to contend that all smooth muscles are alike; however, most points of ultrastructure are consistent among the muscle types, and, in fact, all salient features discussed are demonstrated with electron micrographs of uterine smooth muscle prepared specifically for this text. Although direct electron-optical quantitation of intracellular calcium stores and demonstration of calcium release/recycling has been made only in vascular muscle, it is hypothesized, based on the similarities in ultrastructure and physiological responses, that this information is applicable to uterine as well as other visceral smooth muscles. Resolution of these questions in myometrial muscle has lagged somewhat, partly because of a concentration of effort on its “wealthier” cousin vascular smooth muscle, and further research is required.


Smooth Muscle Smooth Muscle Cell Sarcoplasmic Reticulum Calcium Store Cytoplasmic Calcium 
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  1. 1.
    Osa, T., and Katase, T., 1975, Physiological comparison of the longitudinal and circular muscles of the pregnant rat uterus, Jpn. J. Physiol 25:153–164PubMedGoogle Scholar
  2. 2.
    Massman, H. W., 1980, Comparative morphology of the endometrium, in: The Endometrium F. A. Kimball, ed.), Spectrum Publications, New York, pp. 3–23.Google Scholar
  3. 3.
    Ross, R., and Klebanoff, S. J., 1971, The smooth muscle cell. I. In vivo synthesis of connective tissue proteins, J. Cell Biol 50:159–171.Google Scholar
  4. 4.
    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.PubMedGoogle Scholar
  5. 5.
    Wight, T. N., and Ross, R., 1975, Glycosaminoglycans in primate arteries II. Synthesis and secretion by arterial smooth muscle cells in culture, J. Cell Biol 67:675–686.PubMedGoogle Scholar
  6. 6.
    Law, R. O., 1982, Techniques and application of extracellular space determination in mammalian tissues, Experientia 38:411–420.PubMedGoogle Scholar
  7. 7.
    Casteels, R. J., and Kuriyama, H., 1965, Membrane potential and ionic content in pregnant and nonpregnant rat myometrium, J. Physiol. (London 177:263–287.Google Scholar
  8. 8.
    Jones, A. W., 1968, Influence of oestrogen and progesterone on electrolyte accumulation in the rabbit myometrium, J. Physiol. (London 197:19–20.Google Scholar
  9. 9.
    Csapo, A. I., 1962, Smooth muscle as a contractile unit, Physiol. Rev.42Suppl. 5 ): 7—33.Google Scholar
  10. 10.
    Finn, C. A., and Porter, D. G., 1975, The Uterus, Elek Science, London.Google Scholar
  11. 11.
    Cole, W. C., Garfield, R. E., and Kirkaldy, S. J., 1985, Gap junctions and direct intracellular communication between rat uterine smooth muscle cells, Am. J. Physiol 249:C20 - C31.PubMedGoogle Scholar
  12. 12.
    Kyozuka, M., Crankshaw, J., Berezin, I., Collins, S. M., and Daniels, E. E., 1987, Calcium and contractions of isolated smooth muscle cells from rat myometrium, Can.J. Physiol. Pharmacol 65:1966–1975.Google Scholar
  13. 13.
    Gabella, G., 1981, Structure of smooth muscles, in: Smooth Muscle: An Assessment of Current Knowledge E. Bulbring, A. F., Brading, A. W. Jones, and T. Tomita, eds.), Arnold, London, pp. 1–46.Google Scholar
  14. 14.
    Singer, S. J., and Nicolson, G. L., 1972, The fluid mosaic model of the structure of cell membranes, Science 175:720.PubMedGoogle Scholar
  15. 15.
    Luft, J. H., 1976, The structure and properties of the cell surface coat, Int. Rev. Cytol 45:291–382.PubMedGoogle Scholar
  16. 16.
    Kefalides, N. A., Alper, R., and Clark, C. C., 1979, Biochemistry and metabolism of basement membranes, Int. Rev. Cytol 61:167–228.PubMedGoogle Scholar
  17. 17.
    Gabella, G., 1984, Structural apparatus for force transmission in smooth muscle, Physiol. Rev 64:455–477.PubMedGoogle Scholar
  18. 18.
    Somlyo, A. V., and Franzini-Armstrong, C., 1985, New views of smooth muscle structure using freezing, deep-etching and rotary shadowing, Experientia 41:841–856.PubMedGoogle Scholar
  19. 19.
    Garfield, R. E., and Somlyo, A. P., 1985, Structure of smooth muscle, in: Calcium and Contractility A. K. Grover and E. E. Daniel, eds.), Humana Press, Clifton, N.J., pp. 1–36.Google Scholar
  20. 20.
    Devine, C. E., and Rayns, D. G., 1975, Freeze-fracture studies of membrane systems in vertebrate muscle. II. Smooth muscle, J. Ultrastruct. Res 51:293–306.PubMedGoogle Scholar
  21. 21.
    Wells, G. S., and Wolowyk, M. W., 1971, Freeze-etch observations on membrane structure in the smooth muscle of the guinea-pig taenia coli, J. Physiol. (London 218:11P–13PGoogle Scholar
  22. 22.
    Gabella, G., 1976, Quantitative morphological study of smooth muscle cells of the guinea-pig taenia coli. Structural changes in smooth muscle cells during isotonic contraction, Cell Tissue Res.170:161–201.PubMedGoogle Scholar
  23. 23.
    Gabella, G., and Blundell, D., 1978, Effect of stretch and contraction on caveolae of smooth muscle cells, Cell Tissue Res.190:255–271.PubMedGoogle Scholar
  24. 24.
    Goodford, P. J., 1966, The extracellular space of the smooth muscle of the guinea-pig taenia coli, J. Physiol. (London 186:1–10.Google Scholar
  25. 25.
    Verity, M. A., and Bevan, J. A., 1966, Plurivesicular nerve endings in the pulmonary artery, Nature 211:537–538.PubMedGoogle Scholar
  26. 26.
    Prosser, C. L., Burnstock, G., and Kahn, J., 1960, Conduction in smooth muscle: Comparative structural properties, Am. J. Physiol 199:545–552.PubMedGoogle Scholar
  27. 27.
    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
  28. 28.
    Muggli, R., and Baumgartner, H. R., 1972, Pattern of membrane invaginations at the surface of smooth muscle cells of rabbit arteries, Experientia 28:1212–1214.PubMedGoogle Scholar
  29. 29.
    Orci, L., and Perrelet, A., 1973, Membrane–associated particles: Increases at site of pinocytosis demonstrated by freeze-etching, Science 181:868–869.PubMedGoogle Scholar
  30. 30.
    Garfield, R. E., and Daniel, E. E., 1977, Relation of membrane vesicles to volume control and sodium transport in smooth muscle: Studies on sodium rich tissues, J. Mechanochem. Cell Motil 4:157–176.PubMedGoogle Scholar
  31. 31.
    Garfield, R. E., and Daniels, E. E., 1977, Relation of membrane vesicles to volume control and sodium transport in smooth muscle: Effect of metabolic and transport inhibition on fresh tissue, J. Mechanochem. Cell Motil 4:115–157.Google Scholar
  32. 32.
    Goodford, P. J., and Wolowyk, M. W., 1972, Localization of cation interactions in the smooth muscle of the guinea-pig taenia coli, J. Physiol. (London 224:521–535.Google Scholar
  33. 33.
    Devine, C. E., Somlyo, A. V., and Somlyo, A. P., 1972, Sarcoplasmic reticulum and excitation- contraction coupling in mammalian smooth muscle, J. Cell Biol 52:690–718.PubMedGoogle Scholar
  34. 34.
    Brown, M. S., and Goldstein, J. L., 1976, Receptor-mediated control of cholesterol metabolism, Science 191:150–154.PubMedGoogle Scholar
  35. 35.
    Schollmeyer, J. E., Furcht, L. T., Goll, D. E., Robson, R. M., and Stromer, M. E., 1976, Localization of contactile proteins in smooth muscle cells and in normal and transformed fibroblasts, in: Cell Mobility, Volume A ( R. Goldman, T. Pollard, and J. Rosenbaum, eds.), Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp. 361–388.Google Scholar
  36. 36.
    Schollmeyer, J. E., Goll, D. E., Robson, R. M., and Stromer, M. H., 1973, Localization of α- actinin and tropomyosin in different muscles, J. Muscle Res. Cell Motil.59:306a.Google Scholar
  37. 37.
    Geiger, B., 1979, A 130K protein from chicken gizzard: Its localization at termini of microfilament bundles in cultured chicken cells, Cell 18:193–205.PubMedGoogle Scholar
  38. 38.
    Staehelin, L. A., and Hull, B. E., 1978, Junctions between living cells, Sci. Am 238:140–152.PubMedGoogle Scholar
  39. 39.
    Ikeda, M., Shibata, Y., and Yamamoto, T., 1987, Rapid formation of myometrial gap junctions during parturition in the unilaterally implanted rat uterus, Cell Tissue Res.248:297–303.PubMedGoogle Scholar
  40. 40.
    Shoenberg, C. F., and Stewart, M. J., 1980, Filament formation in muscle homogenates, J. Muscle Res. Cell Motil 1:117–126.PubMedGoogle Scholar
  41. 41.
    Somlyo, A. V., Butler, T. M., Bond, M., and Somlyo, A. P., 1981, Myosin filaments have phosphorylated light chains in relaxed smooth muscle, Nature 294:567–570.PubMedGoogle Scholar
  42. 42.
    Ashton, F. T.,Somlyo, A. V., and Somlyo, A. P., 1975, The contractile apparatus of vascular smooth muscle: Intermediate high voltage stereo electron microscopy, J. Mol. Biol 98:17–29.PubMedGoogle Scholar
  43. 43.
    Lowy, J., Poulsen, F. R., and Vibert, P. J., 1970, Myosin filaments in vertebrate smooth muscle, Nature 225:1053–1054.PubMedGoogle Scholar
  44. 44.
    Shoenberg, C. F., and Haselgrove, J. C., 1974, Filaments and ribbons in vertebrate smooth muscle, Nature 249:152–154.PubMedGoogle Scholar
  45. 45.
    Spudich, J. A., Huxley, H. E., and Finch, J. T., 1972, Regulation of skeletal muscle contraction. II. Structural studies of the interaction of the tropomyosin-troponin complex with actin, J. Mol. Biol 72:619–632.PubMedGoogle Scholar
  46. 46.
    Groschel-Stewart, U., Schreiber, J., Mahl-Meister, C., and Weber, K., 1976, Production of specific antibodies to contractile proteins, and their use in immunofluorescence microscopy. I. Antibodies to smooth and striated chicken myosin, Histochemie 46:229–236.Google Scholar
  47. 47.
    Adelstein, R. S., and Eisenberg, E., 1980, Regulation and kinetics of the actin-myosin-ATP interaction, Annu. Rev. Biochem 49:921–956.PubMedGoogle Scholar
  48. 48.
    Kamm, K. E., and Stull, J. T., 1985, The function of myosin and myosin light chain kinase phosphorylation in smooth muscle, Annu. Rev. Pharmacol. Toxicol. 25: 593–620.PubMedGoogle Scholar
  49. 49.
    Hartshorne, D. J., 1987, Biochemistry of the contractile process in smooth muscle, in: Physiology of the Gastrointestinal Tract, ( L. R. Johnson, ed.), Raven Press, New York, pp. 423–482.Google Scholar
  50. 50.
    Sommerville, L. E., and Hartshorne, D. J., 1987, Intracellular calcium and smooth muscle contraction, Cell Calcium 75–6):353–364Google Scholar
  51. 51.
    Murphy, R. A., Driska, S. P., and Cohen, D. M., 1977, Variations in actin to myosin ratios and cellular force generation in vertebrate smooth muscle, in: Excitation-Contraction Coupling in Smooth Muscle R. Casteels, T. Godfraind, and J. C. Ruegg, eds.), Elsevier/North-Holland, Amsterdam, pp. 417–424.Google Scholar
  52. 52.
    Smith, R. C., Cande, W. Z., Craig, R., Tooth, P. J., Scholey, J. M., and Kendrik-Jones, J., 1983, Regulation of myosin filament assembly by light-chain phosphorylation, Philos. Trans. R. Soc. London Ser. B 302:73–82.Google Scholar
  53. 53.
    Suzuki, H., Kamata, T., Onishi, H., and Watanabe, S., 1982, ATP induced reversible change in the conformation of chicken gizzard myosin and HMM, J. Biochem 91:1699–1705.PubMedGoogle Scholar
  54. 54.
    Trybus, K. M., Huiatt, T. W., and Lowey, S., 1982, A bent monomelic conformation of myosin from smooth muscle, Proc. Natl. Acad. Sci. USA 79:6151–6155.PubMedGoogle Scholar
  55. 55.
    Somlyo, A. P., and Somlyo, A. V., 1986, Smooth muscle structure and function, in: The Heart and the Cardiovascular System H. A. Fozzard, ed.), Raven Press, New York, pp. 845–864.Google Scholar
  56. 56.
    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.PubMedGoogle Scholar
  57. 57.
    Somlyo, 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
  58. 58.
    Ebashi, S., and Kodama, A., 1966, Interaction of troponin with F-actin in the presence of tropomyosin, J. Biochem 59:425–426.PubMedGoogle Scholar
  59. 59.
    Cohen, D. M., and Murphy, R. A., 1979, Cellular thin filament protein contents and force generation in porcine arteries and veins, Circ. Res 45:661–665.PubMedGoogle Scholar
  60. 60.
    Carsten, M. E., 1968, Tropomyosin from smooth muscle of the uterus, Biochemistry 7:960–967.PubMedGoogle Scholar
  61. 61.
    Cooke, P., 1976, A filamentous cytoskeleton in vertebrate smooth muscle fibers, J. Cell Biol 48:539–556.Google Scholar
  62. 62.
    Bennett, G. S., Fellini, S. A., Croop, J. M., Otto, J. J., Bryans, J., and Holtzer, H., 1976, Differences among 100 A-filament subunits from different cell types, Proc. Natl. Acad. Sci. USA 73:4364–4368.Google Scholar
  63. 63.
    Frank, E. D., and Warren, L., 1981, Aortic smooth muscle cells contain vimentin instead of desmin, Proc. Natl. Acad. Sci. USA 78:3020–3024.PubMedGoogle Scholar
  64. 64.
    Gabbiani, G., Schmid, E., Winter, S., Chaponnier, C., Dechastonay, C., Vandekerckhove, J., Weber, K., and Franke, W. W., 1981, Vascular smooth muscle cells differ from other smooth muscle cells: Predominance of vimentin filaments and a specific α-type actin, Proc. Natl. Acad. Sci. USA 78:298–302.PubMedGoogle Scholar
  65. 65.
    Bond, M., and Somlyo, A. V., 1982, Dense bodies and actin polarity in vertebrate smooth muscle, J. Cell Biol 95:403–413.PubMedGoogle Scholar
  66. 66.
    Fay, F. S., and Delise, C. M., 1973, Contraction of isolated smooth muscle cells. Structural changes, Proc. Natl. Acad. Sci. USA 70:641–645.PubMedGoogle Scholar
  67. 67.
    Fisher, B. A., and Bagby, R. M., 1977, Reorientation of myofilaments during contraction of a vertebrate smooth muscle, Am. J. Physiol 232:C5–C14.PubMedGoogle Scholar
  68. 68.
    Murphy, R. A., Herlihy, J. T., and Megerman, J., 1974, Force-generating capacity and contractile protein content of arterial smooth muscle, J. Gen. Physiol 64:691–705.PubMedGoogle Scholar
  69. 69.
    Driska, S. P., and Murphy, R. A., 1978, Estimation of cellular force generation in an arterial smooth muscle with a high actin: myosin ratio, Blood Vessels 15:26–32.PubMedGoogle Scholar
  70. 70.
    Devine, C. E., and Somlyo, A. P., 1971, Thick filaments in vascular smooth muscle, J. Cell Biol 49:636–649.PubMedGoogle Scholar
  71. 71.
    Gabella, G., 1979, Smooth muscle cell junctions and structural aspects of contraction, Br. Med. Bull 35:213–218.PubMedGoogle Scholar
  72. 72.
    Dingemans, K. P., Janses, N., and Becker, A. E., 1981, Ultrastructure of the normal aortic media, Virchows Arch. A 392:199–216.Google Scholar
  73. 73.
    Engvall, E. Ruoslahti, E., and Miller, E. J., 1978, Affinity of fibronectin to collagen of different genetic types and to fibrinogen, J. Exp. Med 147:1584–1595.PubMedGoogle Scholar
  74. 74.
    Perkins, M. E., Ji, T. H., and Hynes, R. O., 1979, Cross-linking of fibronectin to sulfated proteoglycans at the cell surface, Cell 16:941–952.PubMedGoogle Scholar
  75. 75.
    Schlessinger, J., Barak, L. S., Hammes, G. G., Yamada, K. M., Pastan, I., Webb, W. W., and Elson, E. L., 1977, Mobility and distribution of a cell surface glycoprotein and its interaction with other membrane components, Proc. Natl. Acad. Sci. USA 74:2909–2913.PubMedGoogle Scholar
  76. 76.
    Gold, L. I., and Pearlstein, E., 1980, Fibronectin-collagen binding and requirement during cel¬lular adhesion, Biochem. J.186:551–559.Google Scholar
  77. 77.
    Somlyo, A. V., 1980, Ultrastructure of vascular smooth muscle, in: Handbook of Physiology: The Cardiovascular System: Vascular Muscle D. F. Bohr, A. P. Somlyo, and H. V. Sparks, eds.), American Physiological Society, Bethesda, pp. 33–67.Google Scholar
  78. 78.
    Forbes, M. S., 1982, Ultrastructure of vascular smooth muscle cells in mammalian heart, in: The Coronary ArteryS. Kalsner, ed.), Oxford University Press, London, pp. 3–58.Google Scholar
  79. 79.
    Kowarski, D., Shuman, H., Somlyo, A. P., and Somlyo, A. V., 1985, Calcium release by norepinephrine from central sarcoplasmic reticulum in rabbit main pulmonary artery smooth muscle, J. Physiol CLondon 366:153–175.Google Scholar
  80. 80.
    Somlyo, A. P., and Somlyo, A. V., 1975, Ultrastructure of smooth muscle, in: Methods in Pharmacology, Volume 3 (E. E. Daniels and D. M. Paton, eds.) Plenum Press, New York, pp. 3–45.Google Scholar
  81. 81.
    Bergman, R. A., 1968, Uterine smooth muscle fibers in castrate and oestrogen treated rats, J. Cell Biol 36:636–648.Google Scholar
  82. 82.
    Ross, R., and Klebanoff, S. J., 1971, The smooth muscle cell. I.In vivosynthesis of connective tissue proteins, J. Cell Biol 50:159–171.PubMedGoogle Scholar
  83. 83.
    Franzini-Armstrong, C., 1970, Studies of the triad. I. Structure of the junction in frog twitch fibers, J. Cell Biol 47:488–499.PubMedGoogle Scholar
  84. 84.
    Somlyo, A. P., 1985, Excitation-contraction coupling and the ultrastructure of smooth muscle, Circ. Res 57:497–507.PubMedGoogle Scholar
  85. 85.
    Somlyo, A. P., Devine, C. E., Somlyo, A. V., and North, S. R., 1971, Sarcoplasmic reticulum and the temperature-dependent contraction of smooth muscle in calcium-free solutions, J. Cell Biol.51:722–741PubMedGoogle Scholar
  86. 86.
    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 61:723–742.PubMedGoogle Scholar
  87. 87.
    Makita, T., and Kiwaki, S., 1978, Connection of microtubules, caveolae, mitochondria, and sarcoplasmic reticulum in the taenia coli of guinea pigs, Arch. Histol. Jpn 41:167–171.PubMedGoogle Scholar
  88. 88.
    Beams, H. W., and Kessel, R. G., 1968, The Golgi apparatus: Structure and function, Int. Rev. Cytol 23:209–276.PubMedGoogle Scholar
  89. 89.
    Dingle, J., Dean, R., and Sly, W. (eds.), 1984, Lysosomes in Biology and Pathology, Volume 7, Elsevier, Amsterdam.Google Scholar
  90. 90.
    Somlyo, A. V., and Somlyo, A. P., 1971, Strontium accumulation by sarcoplasmic reticulum and mitochondria in vascular smooth muscle, Science 174:955–958.PubMedGoogle Scholar
  91. 91.
    Rubanyi, G., Balogh, I., Kovach, A. G., Somogyi, E., and Sotonyi, P., 1980, Ultrastructure and localization of calcium in uterine smooth muscle, Acta Morphol. Acad. Sci. Hung 28:269–278.PubMedGoogle Scholar
  92. 92.
    Popescu, L. M., and Diculescu, I., 1975, Calcium in smooth muscle sarcoplasmic reticulum in situ: Conventional and X-ray analytical electron microscopy, J. Cell Biol 67:911–918.PubMedGoogle Scholar
  93. 93.
    Heumann, H.-G., 1976, The subcellular localization of calcium in vertebrate smooth muscle: Calcium containing and calcium accumulating structures in muscle cells of mouse intestine, Cell Tissue Res.169:221–231.PubMedGoogle Scholar
  94. 94.
    Somlyo, A. P., Somlyo, A. V., Shuman, H., and Endo, M., 1982, Calcium and monovalent ions in smooth muscle, Fed. Proc 41:2883–2890.PubMedGoogle Scholar
  95. 95.
    Somlyo, A. P., Somlyo, A. V., and Shuman, H., 1979, Electron probe analysis of vascular smooth muscle: Composition of mitochondria, nuclei and cytoplasm, J. Cell Biol 81:316–335.PubMedGoogle Scholar
  96. 96.
    Bond, M., Kitazawz, T., Somlyo, A. P., and Somlyo, A. V., 1984, Release and recycling of calcium by the sarcoplasmic reticulum in guinea pig portal vein smooth muscle, J. Physiol. (London 355:677–695.Google Scholar
  97. 97.
    Somlyo, A. V., Gonzalez-Serratos, H., Shuman, H., McClellan, G., and Somlyo, A. P., 1981, Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: An electron probe study, J. Cell Biol 90:577–594.PubMedGoogle Scholar
  98. 98.
    Wuytack, F., Raemaekers, L., Verbist, J., Jones, L. R., and Casteels, R., 1987, Smooth-muscle endoplasmic reticulum contains a cardiac-like form of calsequestrin, Biochim. Biophys. Acta 899:151–158.PubMedGoogle Scholar
  99. 99.
    Somlyo, A. V., 1979, Bridging structures spanning the junctional gap at the triad of skeletal muscle, J. Cell Biol 80:743–750.PubMedGoogle Scholar
  100. 100.
    Sommer, J. R., and Johnson, E. A., 1979, Ultrastructure of cardiac muscle, in: Handbook of Physiology: The Cardiovascular System, Volume I ( R. M. Berne, ed.), American Physiological Society, Bethesda, pp. 113–186.Google Scholar
  101. 101.
    Droogmans, G., Raemaekers, L., and Casteels, R., 1977, Electro- and pharmacomechanical coupling in the smooth muscle cell of the rabbit ear artery, J. Gen. Physiol 70:129–148.PubMedGoogle Scholar
  102. 102.
    Saki, K., Yamaguchi, T., and Uchita, M., 1981, Oxytocin-induced calcium-free contraction of rat uterine smooth muscle: Effects of divalent cations and drugs, Arch. Int. Pharmacodyn 250:40–50.Google Scholar
  103. 103.
    Kyozuka, M., 1983, Contraction of rat uterine smooth muscle in Ca-free high K solution, Biomed. Res 4:523–532.Google Scholar
  104. 104.
    Lalanne, C., Mironneau, C., Mironneau, J., and Savineau, J. P., 1984, Contraction of rat uterine smooth muscle induced by acetylcholine and angiotensin II in Ca-free medium, Br. J. Pharmacol 81:317–326.PubMedGoogle Scholar
  105. 105.
    Ashoori, F., Taki, A., and Tomita, T., 1985, The response of non-pregnant rat myometrium to oxytocin in Ca-free solution, Br. J. Pharmacol84:175–183.Google Scholar
  106. 106.
    Mironneau, J., Mironneau, C., and Savineau, J. P., 1984, Maintained contraction of rat uterine smooth muscle incubated in Ca-free solution, Br. J. Pharmacol 82:735–743.PubMedGoogle Scholar
  107. 107.
    Kyozuka, M., Crankshaw, J., Berezin, I,, Collins, S. M., and Daniel, E. E., 1987, Calcium and Ray Broderick and Karen A. B rode rick contraction of isolated smooth muscle cells from rat myometrium, Can. J. Physiol. Pharmacol 65:1966–1975.Google Scholar
  108. 108.
    Johansson, B., and Somlyo, A. P., 1980, Electrophysiology and excitation-contraction coupling, in: Handbook of Physiology: Vascular Smooth Muscle, Volume II ( D. F. Bohr, A. P. Somlyo, and H. V. Sparks, eds.), American Physiological Society, Bethesda, pp. 301–324.Google Scholar
  109. 109.
    Weber, A., and Herz, R., 1968, The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum, J. Physiol. (London 52:750–759.Google Scholar
  110. 110.
    Deth, R., and Casteels, R., 1977, A study of releasable Ca fractions in smooth muscle cells of rabbit aorta, J. Gen. Physiol 69:401–416.PubMedGoogle Scholar
  111. 111.
    Deth, R. C., and Lynch, C. J., 1981, Mobilization of a common source of smooth muscle calcium in norepinephrine and methylxanthines, Am. J. Physiol 240:C239–C247.PubMedGoogle Scholar
  112. 112.
    Itoh, T., Kuriyama, H., and Suzuki, H., 1981, Excitation-contraction coupling in smooth muscle cells of the guinea pig mesenteric artery, J. Physiol. (London 321:513–535.Google Scholar
  113. 113.
    Leijten, P. A., and van Breemen, C., 1984, The effects of caffeine on the noradrenaline-sensitive calcium store in rabbit aorta, J. Physiol. (London 357:327–339.Google Scholar
  114. 114.
    Deth, R., and van Breemen, C., 1977, Agonist induced release of intracellular Ca in the rabbit aorta, J. Membr. Biol 30:363–380.PubMedGoogle Scholar
  115. 115.
    Freeman, D. J., and Daniel, E. E., 1973, Calcium movement in vascular smooth muscle and its detection using lanthanum as a tool, Can. J. Physiol. Pharmacol 51:900–913.PubMedGoogle Scholar
  116. 116.
    Weiss, G. B., 1977, Approaches to delineation of differing calcium binding sites in smooth muscle, in: Excitation-Contraction Coupling in Smooth Muscle R. Casteels, ed.), Elsevier/North-Hol- land, Amsterdam, pp. 32–48.Google Scholar
  117. 117.
    Deth, R., and van Breemen, C., 1974, Relative contributions of calcium influx and cellular calcium release during drug induced activation of the rabbit aorta, Pfluegers Arch.348:13–22.Google Scholar
  118. 118.
    Eisenberg, B. R., 1983, Quantitative ultrastructure of mammalian skeletal muscle, in: Handbook of Physiology: Skeletal Muscle L. D. Peachey, R. H. Adrian, and S. R. Geiger, eds.), American Physiological Society, Bethesda, pp. 73–112.Google Scholar
  119. 119.
    Yoshioka, T., and Somlyo, A. P., 1984, The calcium and magnesium contents and volume of the terminal cisternae in caffeine-treated skeletal muscle, J. Cell Biol 99:558–568.PubMedGoogle Scholar
  120. 120.
    Bond, M., Wasserman, A. J., Kowarski, D., Somlyo, A. V., and Somlyo, A. P., 1985, The range of mitochondrial calcium in smooth muscle, Biophys. J.47:414a.Google Scholar
  121. 121.
    Broderick, R., and Somlyo, A. P., 1987, Calcium and magnesium transport by in situmitochondria: Electron probe analysis of vascular smooth muscle, Circ. Res 61:523–530.PubMedGoogle Scholar
  122. 122.
    Bond, M., Shuman, H., Somlyo, A. P., and Somlyo, A. V., 1984, Total cytoplasmic calcium in relaxed and maximally contracted rabbit portal vein smooth muscle, J. Physiol. (London 357:185–201.Google Scholar
  123. 123.
    Somlyo, A. P., Somlyo, A. V., Shuman, H., and Endo, M., 1982, Calcium and monovalent ions in smooth muscle, Fed. Proc 41:2883–2890.PubMedGoogle Scholar
  124. 124.
    Vallieres, J., Scarpa, A., and Somlyo, A. P., 1975, Subcellular fractions of smooth muscle: Isolation, substrate utilization and Ca transport by main pulmonary artery and mesenteric vein mitochondria, Arch. Biochem. Biophys 170:659–669.PubMedGoogle Scholar
  125. 125.
    Wikstrom, M., Ahonen, P., and Luukkaine, T., 1975, The role of mitochondria in uterine contraction, FEBS Lett.56:120–123.PubMedGoogle Scholar
  126. 126.
    Morgan, K. G., Morgan, J. P., and DeFeo, T. T., 1984, Determination of absolute ionized calcium concentrations in vascular smooth muscle using aequorin, Fed. Proc.43:767a.Google Scholar
  127. 127.
    Rembold, C. M., and Murphy, R. A., 1986, Myoplasmic calcium, myosin phosphorylation, and regulation of the crossbridge cycle in swine arterial smooth muscle, Circ. Res 58:803–815.PubMedGoogle Scholar
  128. 128.
    Crompton, M., Moser, R., Ludi, H., and Carafoli, E., 1978, The interrelations between the transport of sodium and calcium in mitochondria of various mammalian tissues, Eur. J. Biochem 82:25–31.PubMedGoogle Scholar
  129. 129.
    Denton, R. M., McCormack, J. G., and Edgell, N. J., 1980, Role of calcium ions in the regulation of intramitochondrial metabolism, Biochem. J 190:107–117.PubMedGoogle Scholar
  130. 130.
    Rossi, C. S., and Lehninger, A. L., 1963, Stoichiometric relationship between accumulation of ions by mitochondria and the energy-coupling sites in the respiratory chain, Biochem. Z 338:698–713.PubMedGoogle Scholar
  131. 131.
    Rudge, M. F., and Duncan, C. J., 1984, Comparative studies on the role of calcium in triggering subcellular damage in cardiac muscle, Comp. Biochem. Physiol 77:459–468.Google Scholar
  132. 132.
    Zimmerman, A. N., Daems, W., Hulsmann, W. C., Snyder, J., Wise, E., and Durrer, D., 1967, Morphological changes in heart muscle caused by successive perfusion with calcium-free and calcium containing solution (calcium paradox), Cardiovasc. Res 1:201–209.Google Scholar
  133. 133.
    Paul, R. J., 1980, Chemical energetics of vascular smooth muscle, in: Handbook of Physiology: The Cardiovascular System D. F. Bohr, A. P. Somlyo, and H. V. Sparks, eds.), American Physiological Society, Bethesda, pp. 201–236.Google Scholar
  134. 134.
    Fleckenstein, A., 1983, Calcium Antagonism in Heart and Smooth Muscle: Experimental Facts and Therapeutic Prospects, Wiley, New York.Google Scholar
  135. 135.
    Morgan, J. P., and Morgan, K. G., 1984, Stimulus-specific patterns of intracellular calcium levels in smooth muscle of the ferret portal vein, J. Physiol. (London 351:155–167.Google Scholar
  136. 136.
    Himpens, B., and Somlyo, A. P., 1988, Free-calcium transients during depolarization and phar- macomechanical coupling in guinea-pig smooth muscle, J. Physiol. (London 395:507–530.Google Scholar
  137. 137.
    Grover, A. K., and Oakes, P. J., 1985, Calcium channel antagonist binding and pharmacology in rat uterine smooth muscle, Life Sci.37:2187–2192.PubMedGoogle Scholar
  138. 138.
    Grover, A. K., Kwan, C. Y., Crankshaw, D. J., Garfield, R. E., and Daniel, E. E., 1980, Characteristics of Ca transport and binding by rat myometrium plasma membrane subfractions, Am. J. Physiol 239:C66–C74.PubMedGoogle Scholar
  139. 139.
    Grover, A. K., Kwan, C. Y., and Daniel, E. E., 1982, High affinity pH-dependent passive Ca binding by myometrial plasma membrane vesicles, Am. J. Physiol 241:C61–C67.Google Scholar
  140. 140.
    Grover, A. K., Kwan, C. Y., and Daniel, E. E., 1982, Ca-concentration dependence of Ca-uptake by rat myometrium plasma membrane enriched fraction, Am. J. Physiol 242:C278–C287.PubMedGoogle Scholar
  141. 141.
    De Schutter, G., Wuytack, F., Verbist, J., and Casteels, R., 1984, Tissue levels and purification by affinity chromatography of the calmodulin-stimulated Ca-transport ATPase in pig antrum smooth muscle, Biochim. Biophys. Acta 773:1–10.PubMedGoogle Scholar
  142. 142.
    Grover, A. K., Kwan, C. Y., and Daniel, E. E., 1981, Na-Ca exchange in rat myometrium membrane vesicles highly enriched in plasma membranes, Am. J. Physiol 240:C175.PubMedGoogle Scholar
  143. 143.
    Sheu, S.-S., and Blaustein, M., 1986, Sodium/calcium exchange and regulation of cell calcium and contractility in cardiac muscle, with a note about vascular smooth muscle, in: The Heart and the Cardiovascular SystemH. M. Fozzard, R. B., Jennings, E. Haber, A. M. Katz, and H. E. Morgan, eds.), Raven Press, New York, pp. 509–536.Google Scholar
  144. 144.
    Hille, B., 1984, Ionic Channels of Excitable Membranes, Sinauer Associates, Sunderland, Mass.Google Scholar
  145. 145.
    Nestler, E. J., Walaas, S. I., Greengard, P., 1984, Neuronal phosphoproteins: Physiological and clinical implications, Science 225:1357–1364.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1990

Authors and Affiliations

  • Ray Broderick
    • 1
  • Karen A. Broderick
    • 2
  1. 1.Department of Pharmacology and Experimental TherapeuticsUniversity of Maryland, School of MedicineBaltimoreUSA
  2. 2.Division of Neonatology, Department of PediatricsSt. Agnes HospitalBaltimoreUSA

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