Skip to main content

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

  • Chapter
Regulation of Smooth Muscle Contraction

Part of the book series: Advances in Experimental Medicine and Biology ((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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Arner, A., 1983, Force-velocity relation in chemically skinned rat portal vein. Effects of Ca2+ and Mg2+, Pflügers Arch., 397: 6.

    Article  PubMed  CAS  Google Scholar 

  • Bárány, M., 1967, ATPase activity of myosin correlated with speed of muscle shortening, J. Gen. Physiol, 50: 197.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Bozler, E., 1930, The heat production of smooth muscle, J. Physiol., 69: 442.

    PubMed  CAS  Google Scholar 

  • Bremel, R. D., 1974, Myosin linked calcium regulation in vertebrate smooth muscle, Nature, 252: 405.

    Article  PubMed  CAS  Google Scholar 

  • Briggs, A. H., 1963, Characteristics of contraction of glycerinated uterine smooth muscle, Am. J. Physiol, 204: 739.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Chatterjee, M. and Murphy, R. A., 1983, Calcium dependent stress maintenance without myosin phosphorylation in skinned smooth muscle, Science, 221: 464.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • DiSalvo, J., Gruenstein, E., and Silver, P., 1978, Ca2+-dependent phosphorylation of bovine aortic actomyosin, Proc. Soc. Exp. Biol Med., 158: 410.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Filo, R. S., Bohr, D. F., and Rüegg, J. C., 1965, Glycerinated skeletal and smooth muscle: Calcium and magnesium dependence, Science, 147: 1581.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Gordon, A. R., 1978, Contraction of detergent-treated smooth muscle, Proc. Nat’l Acad. Sci. U.S.A., 75: 3527.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Hai, C-M. and Murphy, R. A., 1988a, Cross-bridge phosphorylation and regulation of latch state in smooth muscle, Am. J. Physiol, 254: C99.

    PubMed  CAS  Google Scholar 

  • Hai, C-M. and Murphy, R. A., 1988b, Regulation of shortening velocity by cross-bridge phosphorylation in smooth muscle, Am. J. Physiol, 255: C86.

    PubMed  CAS  Google Scholar 

  • 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 

  • Hasselbach, W. and Ledermair, O., 1958, Contraction cycle of isolated contractile structures of uterine musculature and its peculiarities, Pflügers Arch., 267: 532.

    Article  PubMed  CAS  Google Scholar 

  • Hellstrand, P. and Johansson, B., 1975, The force velocity relation in phasic contraction of venous smooth muscle, Acta Physiol. Scand., 93: 157.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Hoar, P. E., Kerrick, W. G. L., and Cassidy, P. S., 1979, Chicken gizzard: Relation between calcium-activated phosphorylation and contraction, Science, 204: 503.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Kubota, Y., Kamm, K. E., and Stull, J. T., 1990, Mechanism of GTPγS-dependent regulation of smooth muscle contraction, Biophys. J., 57: 163a.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Moreland, R. S. and Murphy, R. A., 1986, Determinants of Ca2+-dependent stress maintenance in skinned swine carotid media, Am. J. Physiol, 251: C892.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Moreland, S. and Moreland, R. S., 1987, Effects of dihydropyridines on stress, myosin phosphorylation, and Vo in smooth muscle, Am. J. Physiol, 252: H1049.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Paul, R. J., 1983, Coordination of metabolism and contractility in vascular smooth muscle, Fed. Proc, 42: 62.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Singer, H. S. and Murphy, R. A., 1987, Maximal rates of activation in electrically stimulated swine carotid media, Circ. Res., 60: 438.

    PubMed  CAS  Google Scholar 

  • Sobieszek, A., 1977, Ca2+-linked phosphorylation of a light chain in vertebrate smooth muscle myosin, Eur. J. Biochem., 73: 477.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Takahashi, K., Hiwada, K., and Kokubu, T., 1988, Vascular smooth muscle calponin. A novel troponin T-like protein, Hypertension, 11: 620.

    PubMed  CAS  Google Scholar 

  • Wagner, J. and Rüegg, J. C., 1986, Skinned smooth muscle: Calcium-calmodulin activation independent of myosin phosphorylation, Pflügers Arch., 407: 569.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Plenum Press, New York

About this chapter

Cite this chapter

Moreland, R.S., Pott, J.W.R., Cilea, J., Moreland, S. (1991). Regulation of a Smooth Muscle Contraction: A Hypothesis Based on Skinned Fiber Studies. In: Moreland, R.S. (eds) Regulation of Smooth Muscle Contraction. Advances in Experimental Medicine and Biology, vol 304. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-6003-2_7

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-6003-2_7

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-6005-6

  • Online ISBN: 978-1-4684-6003-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics