Regulation of a Smooth Muscle Contraction: A Hypothesis Based on Skinned Fiber Studies

  • Robert S. Moreland
  • Jan Willem R. Pott
  • Jacqueline Cilea
  • Suzanne Moreland
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 304)

Abstract

Although it is generally believed that smooth muscle will contract in response to an increase in cytosolic free calcium ion concentration, there is still considerable controversy concerning the explicit mechanism(s) coupling calcium to contraction. Bremel (1974), using filament displacement studies, showed that the Ca2+ dependence of vertebrate smooth muscle contraction is associated primarily with the thick filament. A few years later, Aksoy et al. (1976) and Sobieszek (1977) demonstrated that the Ca2+ sensitivity of acto-myosin ATPase activity was associated with phosphorylation of the 20 kDa myosin light chain (MLC) which was subsequently shown to result from activation of MLC kinase, a Ca2+ and calmodulin dependent enzyme (for reviews see Kamm and Stull, 1985; Hartshorne, 1987). Correlations have been shown between MLC phosphorylation and both Ca2+ dependent actin-activated myosin ATPase activity (Dabrowska et al., 1978; DiSalvo et al., 1978) and force development in either skinned (Kerrick et al., 1980; Chatterjee and Murphy, 1983) or intact (Barron et al., 1980; Driska et al., 1981) muscle fibers. These findings have brought about the widespread belief that this system is the primary regulator of smooth muscle contraction.

Keywords

Magnesium Glycerol Norepinephrine Sine Triphosphate 

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References

  1. Aksoy, M. O., Williams, D., Sharkey, E. M., and Hartshorne, D. J., 1976, A relationship between Ca2+ sensitivity and phosphorylation of gizzard actomyosin, Biochem. Biophys. Res. Commun., 69: 35.PubMedCrossRefGoogle Scholar
  2. Aksoy, M. O., Murphy, R. A., Kamm, K. E., 1982, Role of Ca2+ and myosin light chain phosphorylation in regulation of smooth muscle, Am. J. Physiol, 242: C109.Google Scholar
  3. Aksoy, M. O., Mras, S., Kamm, K. E., and Murphy, R. A., 1983, Ca2+, cAMP, and changes in myosin phosphorylation during contraction of smooth muscle, Am. J. Physiol, 245: C255.PubMedGoogle Scholar
  4. Arner, A., 1983, Force-velocity relation in chemically skinned rat portal vein. Effects of Ca2+ and Mg2+, Pflügers Arch., 397: 6.PubMedCrossRefGoogle Scholar
  5. Bárány, M., 1967, ATPase activity of myosin correlated with speed of muscle shortening, J. Gen. Physiol, 50: 197.PubMedCrossRefGoogle Scholar
  6. Barron, J. T., Bárány, M., Bárány, K., and Storti, R. V., 1980, Reversible phosphorylation and dephosphorylation of the 20000 dalton light chain of myosin during the contraction-relaxation-contraction cycle of arterial smooth muscle, J. Biol. Chem., 255: 6238.PubMedGoogle Scholar
  7. Bozler, E., 1930, The heat production of smooth muscle, J. Physiol., 69: 442.PubMedGoogle Scholar
  8. Bremel, R. D., 1974, Myosin linked calcium regulation in vertebrate smooth muscle, Nature, 252: 405.PubMedCrossRefGoogle Scholar
  9. Briggs, A. H., 1963, Characteristics of contraction of glycerinated uterine smooth muscle, Am. J. Physiol, 204: 739.PubMedGoogle Scholar
  10. Butler, T. M., Siegman, M. J., Mooers, S. U., and Narayan, S. R., 1990, Myosin-product complex in the resting state and during relaxation of smooth muscle, Am. J. Physiol, 258: C1092.Google Scholar
  11. Cassidy, P., Hoar, P. E., and Kerrick, W. G. L., 1979, Irreversible thiophosphor-ylation and activation of tension in functionally skinned rabbit ileum strips by [35S]ATPγS, J. Biol. Chem., 254: 11148.PubMedGoogle Scholar
  12. Chatterjee, M. and Murphy, R. A., 1983, Calcium dependent stress maintenance without myosin phosphorylation in skinned smooth muscle, Science, 221: 464.PubMedCrossRefGoogle Scholar
  13. Chatterjee, M., Hai, C-M., and Murphy, R. A., 1987, Dependence of stress and velocity on Ca2+ and myosin phosphorylation in the skinned swine carotid media, in: “Regulation and Contraction of Smooth Muscle”, M. J. Siegman, A. P. Somlyo, and N. L. Stephens, eds., Alan R. Liss., New York, p. 399.Google Scholar
  14. Dabrowska, R., Sherry, J. M. F., Aromatorio, D. K., and Hartshorne, D. J., 1978, Modulator protein as a component of the myosin light chain kinase from chicken gizzard, Biochemistry, 17: 253.PubMedCrossRefGoogle Scholar
  15. Dillon, P. F., Aksoy, M. O., Driska, S. P., and Murphy, R. A., 1981, Myosin phosphorylation and the cross-bridge cycle in arterial smooth muscle, Science, 211: 495.PubMedCrossRefGoogle Scholar
  16. Dillon, P. F. and Murphy, R. A., 1982, Tonic force maintenance with reduced shortening velocity in arterial smooth muscle, Am. J. Physiol, 242: C102.Google Scholar
  17. DiSalvo, J., Gruenstein, E., and Silver, P., 1978, Ca2+-dependent phosphorylation of bovine aortic actomyosin, Proc. Soc. Exp. Biol Med., 158: 410.PubMedGoogle Scholar
  18. Driska, S. P., Aksoy, M. O., and Murphy, R. A., 1981, Myosin light chain phosphorylation associated with contraction in arterial smooth muscle, Am. J. Physiol, 240: C222.PubMedGoogle Scholar
  19. Filo, R. S., Bohr, D. F., and Rüegg, J. C., 1965, Glycerinated skeletal and smooth muscle: Calcium and magnesium dependence, Science, 147: 1581.PubMedCrossRefGoogle Scholar
  20. Fujiwara, T., Itoh, T., Kubota, Y., and Kuriyama, H., 1989, Effect of guanosine nucleotides on skinned smooth muscle tissue of the rabbit mesenteric artery, J. Physiol, 408: 535.PubMedGoogle Scholar
  21. Glück, E. and Paul, R. J., 1977, The aerobic metabolism of porcine carotid artery and its relation to force. Energy cost of isometric contraction, Pflügers Arch., 370: 9.PubMedCrossRefGoogle Scholar
  22. Gordon, A. R., 1978, Contraction of detergent-treated smooth muscle, Proc. Nat’l Acad. Sci. U.S.A., 75: 3527.CrossRefGoogle Scholar
  23. Haeberle, J. R., Hott, J. W., Hathaway, D. R., 1985, Regulation of isometric force and isotonic shortening velocity by phosphorylation of the 20,000 dalton myosin light chain of rat uterine smooth muscle, Pflügers Arch., 403: 215.PubMedCrossRefGoogle Scholar
  24. Hai, C-M. and Murphy, R. A., 1988a, Cross-bridge phosphorylation and regulation of latch state in smooth muscle, Am. J. Physiol, 254: C99.PubMedGoogle Scholar
  25. Hai, C-M. and Murphy, R. A., 1988b, Regulation of shortening velocity by cross-bridge phosphorylation in smooth muscle, Am. J. Physiol, 255: C86.PubMedGoogle Scholar
  26. 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, p. 423.Google Scholar
  27. Hasselbach, W. and Ledermair, O., 1958, Contraction cycle of isolated contractile structures of uterine musculature and its peculiarities, Pflügers Arch., 267: 532.PubMedCrossRefGoogle Scholar
  28. Hellstrand, P. and Johansson, B., 1975, The force velocity relation in phasic contraction of venous smooth muscle, Acta Physiol. Scand., 93: 157.PubMedCrossRefGoogle Scholar
  29. Hellstrand, P. and Arner, A., 1985, Myosin light chain phosphorylation and the cross-bridge cycle at low substrate concentration in chemically skinned guinea pig taenia coli, Pflügers Arch., 405: 323.PubMedCrossRefGoogle Scholar
  30. Himpens, B., Matthijs, G., Somlyo, A. V., Butler, T. M., and Somlyo, A. P., 1988, Cytoplasmic free calcium, myosin light chain phosphorylation, and force in phasic and tonic smooth muscle, J. Gen. Physiol, 92: 713.PubMedCrossRefGoogle Scholar
  31. Hoar, P. E., Kerrick, W. G. L., and Cassidy, P. S., 1979, Chicken gizzard: Relation between calcium-activated phosphorylation and contraction, Science, 204: 503.PubMedCrossRefGoogle Scholar
  32. Hoar, P.E., Pato, M. D., and Kerrick, W. G. L., 1985, Myosin light chain phosphatase. Effect on the activation and relaxation of gizzard smooth muscle fibers, J. Biol Chem., 260: 8760.PubMedGoogle Scholar
  33. Ikebe, M., Barsotti, R. J., Hinkins, S., and Hartshorne, D. J., 1984, Effects of magnesium chloride on smooth muscle actomyosin adenosine-5′-triphosphate activity, myosin conformation, and tension development in glycerinated smooth muscle fibers, Biochemistry, 23: 5062.PubMedCrossRefGoogle Scholar
  34. Kamm, K. E. and Stull, J. T., 1985, Myosin phosphorylation, force, and maximal shortening velocity in neurally stimulated tracheal smooth muscle, Am. J. Physiol, 249: C238.PubMedGoogle Scholar
  35. Kamm, K. E. and Stull, J. T., 1985, The function of myosin and myosin light chain kinase phosphorylation in smooth muscle, Ann. Rev. Pharmacol. Toxicol, 25: 593.CrossRefGoogle Scholar
  36. Kerrick, W. G. L. and Hoar, P. E., 1987, Non-Ca2+-activated contraction in smooth muscle, in: “Regulation and Contraction of Smooth Muscle”, M. J. Siegman, A. P. Somlyo, and N. L. Stephens, eds., Alan R. Liss, New York, p. 437.Google Scholar
  37. Kerrick, W. G. L., Hoar, P. E., and Cassidy, P. S., 1980, Calcium activated tension: The role of myosin light chain phosphorylation, Fed. Proc, 39: 1558.PubMedGoogle Scholar
  38. Kitazawa, T., Kobayashi, S., Horiuti, K., Somlyo, A. V., and Somlyo, A. P., 1989, Receptor-coupled, permeabilized smooth muscle. Role of the phos-phatidylinositol cascade, G-proteins, and modulation of the contractile response to Ca2+, J. Biol Chem., 264: 5339.PubMedGoogle Scholar
  39. Kubota, Y., Kamm, K. E., and Stull, J. T., 1990, Mechanism of GTPγS-dependent regulation of smooth muscle contraction, Biophys. J., 57: 163a.CrossRefGoogle Scholar
  40. Kühn, H., Tewes, A., Gagelmann, M., Güth, K., Arner, A., and Rüegg, J. C., 1990, Temporal relationship between force, ATPase activity, and myosin phosphorylation during a contraction/relaxation cycle in a skinned smooth muscle, Pflügers Arch., 416: 512.PubMedCrossRefGoogle Scholar
  41. Moreland, R. S. and Ford, G. D., 1982, The influence of Mg2+ on the phosphorylation and dephosphorylation of myosin by an actomyosin preparation from vascular smooth muscle, Biochem. Biophys. Res. Commun., 106: 652.PubMedCrossRefGoogle Scholar
  42. Moreland, R. S. and Moreland, S., 1991, Characterization of magnesium-induced contractions in detergent-skinned swine carotid media, Am. J. Physiol., in press.Google Scholar
  43. Moreland, R. S., Moreland, S., and Murphy, R. A., 1988, Effects of length, Ca2+, and myosin phosphorylation on stress generation in smooth muscle, Am. J. Physiol, 255: C473.PubMedGoogle Scholar
  44. Moreland, R. S. and Murphy, R. A., 1986, Determinants of Ca2+-dependent stress maintenance in skinned swine carotid media, Am. J. Physiol, 251: C892.PubMedGoogle Scholar
  45. Moreland, S., Antes, L. M., McMullen, D. M., Sleph, P. G., and Grover, G. J., 1990, Myosin light-chain phosphorylation and vascular resistance in canine anterior tibial arteries in situ, Pflügers Arch., 417: 180.PubMedCrossRefGoogle Scholar
  46. Moreland, S., Little, D. K., and Moreland, R. S., 1987, Calmodulin antagonists inhibit latch bridges in detergent skinned swine carotid media, Am. J. Physiol, 252:C523.PubMedGoogle Scholar
  47. Moreland, S. and Moreland, R. S., 1987, Effects of dihydropyridines on stress, myosin phosphorylation, and Vo in smooth muscle, Am. J. Physiol, 252: H1049.PubMedGoogle Scholar
  48. Moreland, S., Moreland, R. S., and Singer, H. S., 1987, Apparent dissociation of myosin light chain phosphorylation and maximal velocity of shortening in KCl depolarized swine carotid artery: Effects of temperature and [KCl], Pflügers Arch., 408: 139.PubMedCrossRefGoogle Scholar
  49. Morgan, J. P. and Morgan, K. G., 1984, Stimulus-specific patterns of intracellular calcium levels in smooth muscle of ferret portal vein, J. Physiol, 351: 155.PubMedGoogle Scholar
  50. Ngai, P. K. and Walsh, M. P., 1984, Inhibition of smooth muscle actin-activated myosin Mg2+-ATPase activity by caldesmon, J. Biol Chem., 259: 13656.PubMedGoogle Scholar
  51. Nishimura, J. and van Breemen, C., 1989, Possible involvement of actomyosin ADP complex in regulation of Ca2+ sensitivity in α-toxin permeabilized smooth muscle, Biochem. Biophys. Res. Commun., 165: 408.PubMedCrossRefGoogle Scholar
  52. Paul, R. J. and Peterson, J. W., 1975, Relation between length, isometric force and oxygen consumption rate in vascular smooth muscle, Am. J. Physiol, 228: 915.PubMedGoogle Scholar
  53. Paul, R. J., 1983, Coordination of metabolism and contractility in vascular smooth muscle, Fed. Proc, 42: 62.PubMedGoogle Scholar
  54. Rembold, C. M. and Murphy, R. A., 1988, Myoplasmic [Ca2+] determines myosin phosphorylation and isometric force in agonist-stimulated swine arterial smooth muscle, J. Cardiovasc. Pharmacol., 12(Suppl 5): S38.PubMedGoogle Scholar
  55. Saida, K. and Nonomura, Y., 1978, Characteristics of Ca2+-and Mg2+-induced tension development in chemically skinned smooth muscle fibers, J. Gen. Physiol, 72: 1.PubMedCrossRefGoogle Scholar
  56. Siegman, M. J., Butler, T. M., Mooers, S. U., and Davies, R. E., 1980, Chemical energetics of force development, force maintenance, and relaxation in mammalian smooth muscle, J. Gen. Physiol, 76: 609.PubMedCrossRefGoogle Scholar
  57. Siegman, M. J., Butler, T. M., Mooers, S. U., and Michalek, A., 1984, Ca2+ can affect Vmax without changes in myosin light chain phosphorylation in smooth muscle, Pflügers Arch., 401: 385.PubMedCrossRefGoogle Scholar
  58. Siegman, M. J., Butler, T. M., and Mooers, S. U., 1989, Phosphatase inhibition with okadaic acid does not alter the relationship between force and myosin light chain phosphorylation in permeabilized smooth muscle, Biochem. Biophys. Res. Commun., 161: 838.PubMedCrossRefGoogle Scholar
  59. Singer, H. S. and Murphy, R. A., 1987, Maximal rates of activation in electrically stimulated swine carotid media, Circ. Res., 60: 438.PubMedGoogle Scholar
  60. Sobieszek, A., 1977, Ca2+-linked phosphorylation of a light chain in vertebrate smooth muscle myosin, Eur. J. Biochem., 73: 477.PubMedCrossRefGoogle Scholar
  61. Somlyo, A. V., Goldman, Y. E., Fujimori, T., Bond, M., Trentham, D. R., and Somlyo, A. P., 1988, Cross-bridge kinetics, cooperativity, and negatively strained cross-bridges in vertebrate smooth muscle, J. Gen. Physiol, 91: 165.PubMedCrossRefGoogle Scholar
  62. Somlyo, A. P., Kitazawa, T., Himpens, B., Matthijs, G., Horiuti, K., Kobayashi, S., Goldman, Y. E., and Somlyo, A. V., 1989, Modulation of Ca2+-sensitivity and of the time course of contraction in smooth muscle: A major role of protein phosphatases?, in: “Adv. Prot. Phosphatases; Vol. 5”, W. Merleude and J. DiSalvo, eds., Leuven University Press, Leuven, p. 181.Google Scholar
  63. Takahashi, K., Hiwada, K., and Kokubu, T., 1988, Vascular smooth muscle calponin. A novel troponin T-like protein, Hypertension, 11: 620.PubMedGoogle Scholar
  64. Wagner, J. and Rüegg, J. C., 1986, Skinned smooth muscle: Calcium-calmodulin activation independent of myosin phosphorylation, Pflügers Arch., 407: 569.PubMedCrossRefGoogle Scholar
  65. Walsh, M. P., Bridenbaugh, R., Hartshorne, D. J., and Kerrick, W. G. L., 1982, Phosphorylation-dependent activated tension in skinned gizzard muscle fibers in the absence of Ca2+, J. Biol. Chem., 257: 5987.PubMedGoogle Scholar
  66. Winder, S. J. and Walsh, M. P., 1990, Smooth muscle calponin. Inhibition of actomyosin Mg ATPase and regulation by phosphorylation, J. Biol. Chem., 265: 10148.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • Robert S. Moreland
    • 1
  • Jan Willem R. Pott
    • 1
  • Jacqueline Cilea
    • 1
  • Suzanne Moreland
    • 1
    • 2
  1. 1.Bockus Research InstituteGraduate HospitalPhiladelphiaUSA
  2. 2.Department of PharmacologyBristol-Myers Squibb Pharmaceutical Research InstitutePrincetonUSA

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