Ca Distribution and its Regulation in Smooth Muscle Cells

  • J. Verbist
  • G. Droogmans
  • F. Wuytack
  • R. Casteels
Chapter
Part of the NATO ASI Series book series (NSSA, volume 109)

Abstract

Although there exists an important variation between different smooth muscle cells, many common mechanisms can be presumed for the regulation of their excitation-contraction coupling. There is no doubt that the final step in the activation of smooth muscle, i.e. the force development depends on an interaction of the actin and myosin filaments. The main regulatory factor of this activity is the concentration of ionized calcium in the cytoplasm. From this point of view an analysis and an understanding of the regulation of the cytoplasmic Ca concentration is essential for the elucidation of the excitation-contraction coupling in these cells. However there is ample evidence in several cell types that Ca2+ is not the unique regulating factor and that other intracellular mediators as cAMP, cGMP and diacylglycerol can modulate the effect of varying cytoplasmic Ca concentrations. However the importance and the exact role of these intracellular messengers has not been sufficiently determined in smooth muscle cells.

Keywords

Contractile Response Smooth Muscle Tissue Smooth Muscle Membrane Calmodulin Affinity Phasic Contractile Response 
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.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aaronson, P., and van Breemen, C., 1981, Effects of sodium gradient manipulation upon cellular calcium, 45Ca fluxes and cellular sodium in the guinea-pig taenia coli. J. Physiol. 319: 443–461.Google Scholar
  2. Aaronson, P., van Breemen, C., Loutzenhiser, R., and Kolber, M. A., 1979, A new method for measuring the kinetics of transmembrane calcium-45 efflux in the smooth muscle of the guinea pig taenia coli. Life Science 25: 1781–1790.CrossRefGoogle Scholar
  3. Anderson, N.C., Ramon, F., and Snyder, A., 1971, Studies on calcium and sodium in uterine smooth muscle excitation under current-clamp and voltage-clamp conditions. J. Gen. Physiol. 58: 322–339.CrossRefGoogle Scholar
  4. Batra, S., 1973, The role of mitochondrial calcium uptake in contraction and relaxation of the human myometrium. Biochim. Biophys. Acta. 305: 428–432.CrossRefGoogle Scholar
  5. Bohr, D.F., 1973, Vascular smooth muscle updated. Circulation Res. 32: 665–672.Google Scholar
  6. Bolton, T.B., 1979, Mechanism of action of transmitters and other substances on smooth muscle. Physiol Rev. 59: 606–718.Google Scholar
  7. Burnstock, G., 1976, Do some nerves release more than one transmitter. Neuroscience 1: 239–248.CrossRefGoogle Scholar
  8. Caroni, P., and Carafoli, E., 1981, The Ca2+ -pumping ATPase of heart sarcolemma. J. Biol. Chem. 256: 3263–3270.Google Scholar
  9. Carsten, M.E., 1969, Role of calcium binding by sarcoplasmic reticulum in the contraction and relaxation of uterine smooth muscle. J. Gen. Physiol. 53: 414–426.CrossRefGoogle Scholar
  10. Casteels, R., and Droogmans, G., 1975, Compartmental analysis of ion movements it in: “Methods in Pharmacology,” E.E. Daniel and D.M. Paton, ed, Vol 3, pp 663–671, Plenum Press.Google Scholar
  11. Casteels, R., and Droogmans, G., 1981, Exchange characteristics of the noradrenaline-sensitive calcium store in vascular smooth muscle cells of rabbit ear artery, J. Physiol. 317: 263–279.Google Scholar
  12. Casteels, R., Droogmans, G., and Hendrickx, H., 1971, Membrane potential of smooth muscle cells in K-free solution, J. Physiol. 217: 281–295.Google Scholar
  13. Casteels, R., Kitamura, K., Kuriyama, H., and Suzuki, H., 1977, Excitation-contraction coupling in the smooth muscle cells of the rabbit main pulmonary artery, J. Physiol. 271: 63–79.Google Scholar
  14. Casteels, R., Kitamura, K., Kuriyama, H., and Suzuki, H., 1977, The membrane properties of the smooth muscle cells of the rabbit main pulmonary artery. J. Physiol. 271: 41–61.Google Scholar
  15. Casteels, R., and Raeymaekers, L., 1979, The action of acetylcholine and catecholamines on an intracellular calcium store in the smooth muscle cells of the guinea-pig taenia coli, J. Physiol. 294: 51–68.Google Scholar
  16. Casteels, R., Raeymaekers, L., Droogmans, G., and Wuytack, F., 1985, Na+-K+ ATPase, Na-Ca exchange, and excitation contraction coupling in smooth muscle, J. Cardiovasc. Pharmacol, in press.Google Scholar
  17. Casteels, R., Raeymaekers, L., Suzuki, H., and Van Eldere, J., 1981, Tension response and 45Ca release in vascular smooth muscle incubated in Ca-free solution, Pflügers Arch., 392: 139–145.CrossRefGoogle Scholar
  18. Cauvin, C., Loutzenhiser, R., and van Breemen, C., 1983, Mechanisms of calcium antagonist-induced vasodilatation, Ann. Rev. Pharmacol. Toxicol. 23: 373–396.CrossRefGoogle Scholar
  19. Cheung, D.W., 1982, Two components in the cellular response of rat tail arteries to nerve stimulation, J. Physiol. 328: 461–468.Google Scholar
  20. Deth, R., and Casteels, R., 1977, A study of releasable Ca fractions in smooth muscle cells of the rabbit aorta, J. Gen. Physiol. 69: 401–416.CrossRefGoogle Scholar
  21. Deth, R., and van Breemen, C., 1977, Agonist induced release of intracellular Ca in the rabbit aorta, J. Membrane Biol. 30: 363–380.CrossRefGoogle Scholar
  22. Deth R., and Lynch, C. J., 1981, Mobilization of a common source of smooth muscle Ca by norepinephrine and methylxanthines, Am. J. Physiol. 240: C239–C247.Google Scholar
  23. Devine, C.E., Somlyo, A.V., and Somlyo, A.P., 1971, Sarcoplasmic reticulum and excitation-contraction coupling in mammalian smooth muscle, J. Cell Biol. 52: 690–715.CrossRefGoogle Scholar
  24. Dipolo, R., and Beauge, L., 1983, The calcium pump and sodium-calcium exchange in squid axons, Ann. Rev. Physiol. 45: 313–324.CrossRefGoogle Scholar
  25. Droogmans, G., and Casteels, R., 1979, Sodium and calcium interactions in vascular smooth muscle cells of the rabbit ear artery, J. Gen. Physiol. 74: 57–70.CrossRefGoogle Scholar
  26. Droogmans, G., and Casteels, R., 1981, Temperature-dependence of 45Ca fluxes and contraction in vascular smooth muscle cells in rabbit ear artery, Pflügers Arch. 391: 183–189.CrossRefGoogle Scholar
  27. Droogmans, G., Raeymaekers, L., and Casteels, R., 1977, Electro- and pharmacomechanical coupling in the smooth muscle cells of the rabbit ear artery, J. Gen. Physiol. 70: 129–148.CrossRefGoogle Scholar
  28. Gietzen, K., Teschka, M., and Wolf, H.U., 1980, Calmodulin affinity chromatography yields a functional purified erythrocyte (Ca2++Mg2+) dependent adenosine triphosphatase, Biochem. J. 189: 81–88.Google Scholar
  29. Gietzen, K., Sadorf, I., and Bader, H., 1982, A model for the of the calmodulin-dependent enzymes erythrocyte Ca2+ transport ATPase and brain phosphodiesterase by activators and inhibitors, Biochem. J. 207: 541–548.Google Scholar
  30. Glossmann, H., Ferry, D.R., Lubbecke, F., Mewes, R., and Hoffman, F., 1982, Calcium channels: direct identification with radioligand binding studies, Trends Pharmacol. Sci. 3: 431–437.CrossRefGoogle Scholar
  31. Godfraind, T., 1976, Calcium exchange in vascular smooth muscle, action of noradrenaline and lanthanum, J. Physiol. (London) 260: 21–36.CrossRefGoogle Scholar
  32. Golenhofen, K., Hermstein, N., and Lammel, E., 1973, Membrane potential and contraction of vascular smooth muscle (portal vein) during application of noradrenaline and high potassium, and selective inhibitory effects of iproveratril (verapamil), Microvasc. Res. 5: 73–80.CrossRefGoogle Scholar
  33. Goodford, P.J., 1965, The loss of radioactive 45calcium from the smooth muscle of the guinea-pig taenia coli, J. Physiol. 176: 180–190.Google Scholar
  34. 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: 0175–0182.Google Scholar
  35. Harder, D.R., 1980, Comparison of electrical properties of middle cerebral and mesenteric artery in the cat, Am. J. Physiol. 239: C23–C26.Google Scholar
  36. Harder, D.R., and Sperelakis, N., 1979, Action potentials induced in guinea-pig arterial smooth muscle by tetraethylammonium, Am. J. Physiol. 237: C75 - C80.Google Scholar
  37. Hirst, G.D.S., 1977, Neuromuscular transmission in arterioles of guinea-pig submucosa, J. Physiol. 273: 263–275.Google Scholar
  38. Hirst, G.D.S., and Neild, T.O., 1980, Evidence for two populations of excitatory receptors for noradrenaline on arteriolar smooth muscle, Nature 283: 767–768.CrossRefGoogle Scholar
  39. Holman, M.E., and Surprenant, A.M., 1979, Some properties of the excitatory junction potentials recorded from spontaneous arteries of rabbits, J. Physiol. 287: 337–352.Google Scholar
  40. Itoh, T., Kajiwara, M., Kitamura, K., and Kuriyama, H., 1982, Roles of stored calcium on the mechanical response evoked in smooth muscle cells of the porcine coronary artery, J. Physiol. 22: 107–125.Google Scholar
  41. Itoh, T., Kuriyama H., and Suzuki, H., 1983, Differences and similarities in the noradrenaline- and caffeine-induced mechanical responses in the rabbit mesenteric artery, J. Physiol. 337: 609–629.Google Scholar
  42. Kajiwara, M., and Casteels, M., 1983, Effects of Ca-antagonists on neuromuscular transmission in the rabbit ear artery, Pflügers Arch. 396: 1–7.CrossRefGoogle Scholar
  43. Kitamura, K., and Kuriyama, H., 1979, Effects of acetylcholine on the smooth muscle cells of isolated main coronary artery of the guinea-pig, J. Physiol. 293: 119–133.Google Scholar
  44. Kolber, M.A., and van Breemen, C., 1981, Competitive membrane adsorption of Na+, K+ and Ca2+ in smooth muscle cells, J. Membrane Biol. 58: 115–121.CrossRefGoogle Scholar
  45. Korenbrot, J., 1977, Ion transport in membranes: Incorporation of biological ion-translocating proteins in model membrane systems, Ann. Rev. Physiol. 39: 19–49.CrossRefGoogle Scholar
  46. Kuriyama, H., Itoh, Y., Suzuki, H., Kitamura, K., Itoh, T., Kajiwara, M., and Fukiwara, S., 1983, Actions of diltiazem on single smooth muscle cells and on neuromuscular transmission in the vascular bed, Circulation Res, supp I, 52: 92–96.Google Scholar
  47. Makita, Y., Kanmura, Y., Itoh, T., Suzuki, H., and Kuriyama, H., 1983, Effects of nifedipine derivates on smooth muscle cells and neuromuscular transmission in the rabbit mesenteric artery, Arch. Pharmacol. 324: 302–312.CrossRefGoogle Scholar
  48. Mangel, A., Fahim, M., and van Breemen, C., 1982, Control of vascular contractility by the cardiac pacemaker, Science 215: 1627–1629.CrossRefGoogle Scholar
  49. Mayer, C.J., van Breemen, C., and Casteels, R., 1972, The action of lanthanum and D600 on the calcium exchange in the smooth muscle cells of the guinea-pig coli, Pflügers Arch. 337: 333–350.CrossRefGoogle Scholar
  50. Meisheri, K.D., Hwang, O., and van Breemen, C., 1981, Evidence for two separate Ca pathways in smooth muscle plasmalemma, J. Membrane Biol. 59: 19–25.CrossRefGoogle Scholar
  51. Mironneau, J., Eugene, D., and Mironneau, C., 1982, Sodium action potentials induced by calcium chelation in rat uterine smooth muscle, Pflügers Arch. 395: 232–238.CrossRefGoogle Scholar
  52. Morel, N., and Godfraind, T., 1984, Sodium/calcium exchange in smooth muscle microsomal fractions, Biochem. J. 218: 421–427.Google Scholar
  53. Niggli, V., Penniston, J.T., and Carafoli, E., 1979, Purification of the (Ca2+ + Mg2+)-ATPase from human erythrocyte membranes using a calmodulin affinity column, J. Biol. Chem. 254: 9955–9958.Google Scholar
  54. Niggli, V., Adunyah, E.S., Penniston, J.T., and Carafoli, E., 1981, Purified (Ca2+ + Mg2+)-ATPase of the erythrocyte membrane. Reconstitution and effect of calmodulin and phospholipids, J. Biol. Chem. 256: 395–401.Google Scholar
  55. Ozaki, H., and Urakawa, N., 1981, Involvement of a Na-Ca exchange mechanism in contraction induced by low-Na solution in isolated guinea-pig aorta, Pflügers Arch. 390: 107–112.CrossRefGoogle Scholar
  56. Peiper, U., Griebel, L., and Wende, W., 1971a, Activation of vascular smooth muscle of rat aorta by noradrenaline and depolarization: two different mechanisms, Pflügers Arch. 330: 74–89.CrossRefGoogle Scholar
  57. Peiper, U., Griebel, L., and Wende, W., 1971b, Unterschiedliche temperaturabhangigkeit der gefassmuskelkontraktion nach aktivierung durch kalium-depolarisation bzw. Noradrenalin, Pflügers Arch. 324: 67–78.CrossRefGoogle Scholar
  58. Raeymaekers, L., 1982, The sarcoplasmic reticulum of smooth muscle fibers, Z. Naturforsch. 37c: 481–488.Google Scholar
  59. Raeymaekers, L., and Casteels, R., 1981, Measurement of Ca uptake in the endoplasmic reticulum of the smooth muscle cells of the rabbit ear artery, Arch. Int. Physiol. Blochem. 89: 33–34.Google Scholar
  60. Raeymaekers, L., and Casteels, R., 1984, The calcium uptake in smooth muscle microsomal vesicles is reduced by centrifugation, Cell Calcium 5: 205–210.CrossRefGoogle Scholar
  61. Raeymaekers, L., Wuytack, F., and Casteels, R., 1975, Na-Ca exchange in taenia coli of the guinea-pig, Pflügers Arch. 347: 329–340.CrossRefGoogle Scholar
  62. Raeymaekers, L., Wuytack, F., Eggermont, J., De Schutter, G., and Casteels, R., 1983, Isolation of a highly enriched plasma membrane fraction from gastric smooth muscle. Comparision of the Ca-uptake to that in endoplasmic reticulum, Biochem. J. 210: 315–322.Google Scholar
  63. Sarkadi, B., Enyedi, A., and Gardos. G., 1980, Molecular properties of the red cell calcium pump. I. Effects of calmodulin, proteolytic digestion and drugs on the kinetics of active calcium uptake in inside-out red cell membrane vesicles, Cell Calcium 1: 287–297.CrossRefGoogle Scholar
  64. Schatzmanm, H.J., 1961, Calciumaufnahme und Abgabe am Darmmuskel des Meerschweinchens, Pflügers Arch. 274: 295–310.CrossRefGoogle Scholar
  65. Schatzmann, H.J., 1982, The plasma membrane calcium pump of erythrocytes and other animal cells, in: “Membrane transport of calcium,” E. Carafoli, ed., pp. 41–108, Acad. Press, London.Google Scholar
  66. Schumann, H.J., Gorlitz, B.D., and Wagner, J., 1975, Influence of papaverine, D600, and nifedine on the effects of noradrenaline and calcium on the isolated aorta and mesenteric artery of the rabbit, Arch. Pharamcol. 289: 409–418.CrossRefGoogle Scholar
  67. Sitrin, M.D., and Bohr, D., 1971, Ca and Na interaction in vascular smooth muscle contraction, Am. J. Physiol. 220: 112V1128.Google Scholar
  68. Sneddon, P., and Westfall, D.P., 1984, Pharmacological evidence that adenosine triphosphate and noradrenaline are cotransmitters in the guinea-pig vas deferens, J. Physiol. 347: 561–580.Google Scholar
  69. 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. 67: 911–918.Google Scholar
  70. Stout, M.A., and Diecke, F.P.J., 1983, 45Ca distribution and transport in saponin skinned vascular smooth muscle, J. Pharmacol. Exp. Ther. 225: 102–111.Google Scholar
  71. Su, C., Bevan, J.A., and Ursillo, R.C., 1964, Electrical quiescence of pulmonary artery smooth muscle during sympathomimetic stimulation, Circulation Res. 15: 20–27.Google Scholar
  72. Surprenant, A., Neild, T.O., and Holman, M.E., 1983, Effects of nifedipine on nerve-evoked action potentials and consequent contractions in rat tail artery, Pflügers Arch. 396: 342 - 349.CrossRefGoogle Scholar
  73. Suzuki, H., 1981, Effects of endogenous and exogenous noradrenaline on the smooth muscle of guinea-pig mesenteric vein, J. Physiol. 321: 495–512.Google Scholar
  74. Suzuki, H., 1985, Electrical responses of smooth muscle cells of the rabbit ear artery to adenosine triphosphate, J. Physiol. 359: 401–415.Google Scholar
  75. Suzuki, H., Itoh, T., and Kuriyama, H., 1982, Effects of diltiazem on smooth muscle and neuromuscular junction in mesenteric artery, Am. J. Physiol. 242: H325–H336.Google Scholar
  76. van Breemen, C., 1977, Calcium requirement for activation of aortic smooth muscle, J. Physiol. 272: 317–330.Google Scholar
  77. van Breemen, C., Aaronson, P., Loutzenhiser, R., and Meisheri, K., 1980, Ca movements in smooth muscle, Chest 78: 157–165.Google Scholar
  78. van Breemen, C., Casteels, R., 1974, The use of Ca-EGTA in measurements of 45Ca efflux from smooth muscle, Pflügers Arch 348: 239–245.CrossRefGoogle Scholar
  79. van Breemen, C., Farinas, B.R., Casteels, R., Gerba, P., Wuytack, F., and Deth, R., 1973, Factors controlling cytoplasmic Ca-concentration, Phil. Trans. R. Soc. Lond. B 265: 57–71.CrossRefGoogle Scholar
  80. van Breemen, C., and McNaughton, E., 1970, The separation of cell membrane calcium transport from extracellular calcium exchange in vascular smooth muscle, Biochem. Blophys. Res. Commun. 39: 567–574.CrossRefGoogle Scholar
  81. Van Eldere, J., Raeymaekers, L., and Casteels, R., 1982, Effect of isoprenaline on intracellular Ca uptake and on Ca influx in arterial smooth muscle, Pflügers Arch. 395: 81–83.CrossRefGoogle Scholar
  82. Verbist, J., Wuytack, F., De Schutter, G., Raeymaekers, L., and Casteels, R., 1984, Reconstitution of the purified calmodulin (Ca2+ +Mg2+)-ATPase from smooth muscle, Cell Calcium 5: 253–263.CrossRefGoogle Scholar
  83. Walsh, J.V., and Singer, J.J., 1980, Calcium action potentials in single freshly isolated smooth muscle cells, Am. J. Physiol. 239: C162–C174.Google Scholar
  84. Wuytack, F., and Casteels, R., 1980, Demonstration of a (Ca2+ +Mg2+) ATPase activity probably related to Ca2+ transport in the microsomal fraction of porcine coronary artery smooth muscle. Biochim. Biophys. Acta 595: 257–263.CrossRefGoogle Scholar
  85. Wuytack, F., De Schutter, G., and Casteels, R., 1981, Purification of (Ca2+ + Mg2+)-ATPase from smooth muscle by calmodulin affinity chromatography, FEBS Letters 129: 297 - 300.CrossRefGoogle Scholar
  86. Wuytack, F., Landon, E., Fleischer, R., and Hardman, J.G., 1978, The calcium accumulation in a microsomal fraction from porcine artery smooth muscle. A study of the heterogeneity of the fraction, Biochim. Biophys. Acta 540: 253–269.CrossRefGoogle Scholar
  87. Wuytack, F., Raeymaekers, L., De Schutter, G., and Casteels, R., 1982, Demonstration of the phosphorylated intermediates of the Ca2+ transport ATPase in a microsomal fraction in a (Ca2+ + Mg2+)-ATPase purified from smooth muscle by means of calmodulin affinity chromatography, Biochim. Biophys. Acta 693: 45–52.CrossRefGoogle Scholar
  88. Wuytack, F., Raeymaekers, L., Verbist, J., Desmedt, H., and Casteels, R 1984, Evidence for the presence in smooth muscle of two types of Ca2+ -transport ATPase, Bioichem. J. 224: 445–451.Google Scholar
  89. Zelcer, E., and Sperelakis, N., 1981, Ionic dependence of electrical activity in small mesenteric arteries of guinea-pig, Pflügers Arch 392: 72–78.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • J. Verbist
    • 1
  • G. Droogmans
    • 1
  • F. Wuytack
    • 1
  • R. Casteels
    • 1
  1. 1.Laboratorium voor FysiologieKatholieke Universiteit LeuvenLeuvenBelgium

Personalised recommendations