Advertisement

Second Messenger Effects on the Myosin Phosphorylation System in Smooth Muscle

  • J. T. Stull
  • B. F. Bowman
  • J. C. Colburn
  • L.-C. Hsu
  • C. H. Michnoff
  • D. A. Taylor
  • K. E. Kamm
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 255)

Abstract

All smooth muscle cells contain the contractile proteins actin, myosin, and tropomyosin (Hartshorne, 1987). The enzyme myosin is the primary protein of the thick filament in smooth muscle and is composed of two high molecular weight subunits, or heavy chains, and two each of two types of low molecular weight subunits, or light chains. The molecular mass of each heavy chain subunit is about 200 kDa whereas the light chain subunits are 20 and 17 kDa respectively. The native hexameric form of myosin is configured as an intertwined coiled-tail region of two heavy chains embedded in the thick filament and two globular head regions that protrude at regular intervals to form cross bridges. These head regions contain the actin-binding domain, the catalytic site for ATP hydrolysis, and the associated light chain subunits. According to the sliding filament theory of muscle contraction, thick (myosin) and thin (actin and tropomyosin) filaments move past one another. This process is related to the binding of cross bridges to actin and to the hydrolysis of ATP. The sliding filament theory has been developed primarily from detailed investigations of skeletal muscle, but the general organization of thin and thick filaments in smooth muscle is consistent with a similar mechanism of contraction.

Keywords

Light Chain Myosin Light Chain Myosin Light Chain Kinase Thick Filament Tracheal Smooth Muscle 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bengur, A.R., Robinson, E.A., Apella, E., and Sellers, J.R., 1987, Sequence of the sites phosphorylated by protein kinase C in the smooth muscle myosin light chain, J. Biol. Chem., 262:7613–7616.PubMedGoogle Scholar
  2. Bitar, K.N., Bradford, P., Putney, Jr. J.W., and Makhloug, G.M., 1986, Cytosolic calcium during contraction of isolated mammalian gastric muscle cells, Science, 232:1143–1145.PubMedCrossRefGoogle Scholar
  3. Brading, A.F. and Sneddon, P., 1980, Evidence for multiple sources of calcium for activation of the contractile mechanism of guinea-pig taenia coli on stimulation with carbachol, Br. J. Pharmacol., 70:229–240.PubMedGoogle Scholar
  4. Brown, R.D., Prendiville, P., and Cain, C., 1986, Alpha 1-adrenergic and Hl-histamine receptor control of intracellular Ca2+ in a muscle cell line: the influence of prior agonist exposure on receptor responsiveness, Molec. Pharmacol., 29:531–539.Google Scholar
  5. Colburn, J.C., Michnoff, C.H., Hsu, L., Slaughter, C.A., Kamm, K.E., and Stull, J.T., 1988, Sites phosphorylated in myosin light chain in contracting smooth muscle, J. Biol. Chem., in press.Google Scholar
  6. Eccleston, J.F., Messerschmidt, R.G., and Yates, D.W., 1980, A simple rapid mixing device, Anal. Biochem., 10673–10677.Google Scholar
  7. Grynkiewicz, G., Poenie, M., and Tsien, R.Y., 1985, A new generation of Ca2+ indicators with greatly improved fluorescence properties, J. Biol. Chem., 260:3440–3450.PubMedGoogle Scholar
  8. Hartshorne, D.J., 1987, Biochemistry of the contractile process in smooth muscle, in “Physiology of the Gastrointestinal Tract, Second Edition, L.R. Johnson, ed., Raven Press, New York.Google Scholar
  9. Ikebe, M., and Hartshorne, D.J., 1985, Phosphorylation of smooth muscle myosin at two distinct sites by myosin light chain kinase, J. Biol. Chem., 260:10027–10031.PubMedGoogle Scholar
  10. Ikebe, M., Hartshorne, D.J., and Elzinga, M., 1986, Identification, phosphorylation, and dephosphorylation of a second site for myosin light chain kinase on the 20,000 dalton light chain of smooth muscle myosin, J. Biol. Chem., 261:36–39.PubMedGoogle Scholar
  11. Ikebe, M., Hartshorne, D.J., and Elzinga, M., 1987, Phosphorylation of the 20,000-dalton light chain of smooth muscle myosin by the calcium-activated, phospholipid-dependent protein kinase, J. Biol. Chem., 262:9569–9573.PubMedGoogle Scholar
  12. Ikebe, M., Koretz, J., and Hartshorne, D.J., 1988, Effects of phosphorylation of light chain residues threonine 18 and serine 19 on the properties and conformation of smooth muscle myosin, J. Biol. Chem., 263:6432–6437.PubMedGoogle Scholar
  13. Kamm, K.E., and Stull, J.T., 1985b, Myosin phosphorylation, force and maximal shortening velocity in neurally stimulated tracheal smooth muscle, Amer. J. Physiol., 249: C238–C247.PubMedGoogle Scholar
  14. Kamm, K.E., and Stull, J.T., 1989, Regulation of smooth muscle contractile elements by second messengers, Annu. Rev. Physiol., in press.Google Scholar
  15. Kanaide, H., Hasegawa, M., Kobayashi, S., and Nakamura, M., 1987, Serotonin-induced cytosolic free calcium transients in cultured vascular smooth muscle cells, Biochem. Biophys. Res. Comm., 143:532–538.PubMedCrossRefGoogle Scholar
  16. Kawamoto, S. and Adelstein, R.S., 1988, The heavy chain of smooth muscle myosin is phosphorylated in aorta cells, J. Biol. Chem., 263:1099–1102.PubMedGoogle Scholar
  17. Ludowyke, R.I., Peleg, I., Beaven, M.A., and Adelstein, R.S., 1987, Analysis of phosphorylation of myosin heavy and light chains during antigen stimulation of basophil leukemic cells, J. Cell. Biol., 105:118a.Google Scholar
  18. Naka, M., Saitoh, M., and Hidaka, H., 1988, Two phosphorylated forms of myosin in thrombin-stimulated platelets, Arch, of Biochem. and Biophysics, 261:235–240.CrossRefGoogle Scholar
  19. Nishikawa, M., Sellers, J.R., Adelstein, R.S., and Hidaka, H., 1984, Protein kinase C modulates in vitro phosphorylation of the smooth muscle heavy meromyosin by myosin light chain kinase, J. Biol. Chem., 259:8808–8814.PubMedGoogle Scholar
  20. Persechini, A., Kamm, K.E., and Stull, J.T., 1986, Different phosphorylated forms of myosin in contracting tracheal smooth muscle, J. Biol. Chem., 261:6293–6299.PubMedGoogle Scholar
  21. Scanlon, M., Williams, D.A., and Fay, F.S., 1987, A Ca2+-insensitive form of fura-2 associated with polymorphonuclear leukocytes, J. Biol Chem., 262:6308–6312PubMedGoogle Scholar
  22. Taylor, D.A., and Stull, J.R., 1988, Calcium dependence of myosin light chain phosphorylation in smooth muscle cells, J. Biol. Chem., 263:14456–14462.PubMedGoogle Scholar
  23. Tsien, R.Y., Pozzan, T., and Rink, T.J., 1982, Calcium homeostasis in intact lymphocytes: Cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator, J. Cell Biol., 94:325–334.PubMedCrossRefGoogle Scholar
  24. Umekawa, H., Naka, M., Inagaki, M., Onishi, H., Wakabayashi, T., and Hidaka, H., 1985, Conformational studies of myosin phosphorylated by protein kinase C, J. Biol. Chem., 260:9833–9837.PubMedGoogle Scholar
  25. Williams, D.A., Fogarty, K.E., Tsien, R.Y., and Fay, F.S., 1985, Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using fura-2, Nature, 318:558–561.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • J. T. Stull
    • 1
  • B. F. Bowman
    • 1
  • J. C. Colburn
    • 1
  • L.-C. Hsu
    • 1
  • C. H. Michnoff
    • 1
  • D. A. Taylor
    • 1
  • K. E. Kamm
    • 1
  1. 1.Department of Physiology and Moss Heart CenterUniversity of Texas Southwestern Medical Center at DallasDallasUSA

Personalised recommendations