Journal of Muscle Research & Cell Motility

, Volume 11, Issue 4, pp 293–301

The action of brevin, an F-actin severing protein, on the mechanical properties and ATPase activity of skinned smooth muscle

  • Ph. Gailly
  • Th. Lejeune
  • J. P. Capony
  • J. M. Gillis
Papers
  • 38 Downloads

Summary

Brevin is a protein which regulates the actin gel-sol transformation: it severs F-actin filaments into shorter ones. This action is Ca-dependent and is prevented by tropomyosin. We tested the effect of brevin on isometric contractions of skinned smooth muscle (taenia coli) and noted a dramatic loss of tension that possibly reflects some F-actin fragmentation. This effect is tentatively attributed to a partial loss of tropomyosin in the skinning procedure. We also studied the effect of brevin on unloaded shortenings of skinned preparations: thin bundles and enzymatically dissociated cells. We observed a marked increase of the velocity of shortening in the presence of brevin. This effect cannot be attributed to an increased ATPase activity as the latter is slightly reduced in the presence of brevin. We interpret this result as reflecting a decrease in internal resistance to movement, possibly by solation of an actin-filamin domain.

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References

  1. Bond, M., &Somlyo, A. V. (1982) Dense bodies and actin polarity in vertebrate smooth muscle.J. Cell Biol. 95, 403–13.PubMedGoogle Scholar
  2. Chaponnier, C., Yin, H. L. &Stossel, T. P. (1987) Reversibility of gelsolin/actin interaction in macrophages.J. Exp. Med. 165, 97–106.PubMedGoogle Scholar
  3. Cooper, J.A., Bryan, J., Schwab III, B., Frieden, C., Loftus, D. J. &Elson, E. L. (1987). Microinjection of Gelsolin into living cells.J. Cell Biol. 104, 491–501.PubMedGoogle Scholar
  4. Cooper, J. A., Loftus, D. J., Frieden, C., Bryan, J. &Elson, E. L. (1988). Localization and mobility of gelsolin in cells.J. Cell Biol. 106, 1229–40.PubMedGoogle Scholar
  5. Endo, M., Kitazawa, T., Yagi, S., Iino, M. &Kakuta, Y. (1977) Some properties of chemically skinned smooth muscle fibers. InExcitation-Contraction Coupling in Smooth Muscle (edited by Casteels, R., Godfraind, T. & Rüegg, J. C.) pp. 199–209. Elsevier, Amsterdam.Google Scholar
  6. Fattoum, A., Hartwig, J. H. &Stossel, T. P. (1983) Isolation and some structural and functional properties of macrophage tropomyosin.Biochem. 22, 1187–93.Google Scholar
  7. Filo, R. S., Bohr, D. F. & rRüegg, J. C. (1965) Glycerinated skeletal and smooth muscle: calcium and magnesium dependence.Science 147, 1581–3.PubMedGoogle Scholar
  8. Gaertner, A., Ruhnau, K., Schröer, E., Selve, N., Wanger, M. &Wegner, A. (1989) Probing nucleation, cutting and capping of actin filaments.J. Muse. Res. Cell Mot. 10, 1–9.Google Scholar
  9. Gailly, P. (1989) The effect of brevin on unloaded shortening of isolated smooth muscle cell.Arch. Int. Physiol. Biochim. 98, 22.Google Scholar
  10. Gailly, P., Lejeune, T., Capony, J. P. &Gillis, J. M. (1989) Action of brevin on the contraction of skinned fibres from smooth and striated muscles.Arch. int. Physiol. Biochim. 97, P. 58.Google Scholar
  11. Gordon, A. R. (1978) Contraction of detergent-treated smooth muscle.Proc. Natl. Acad. Sci. USA. 75, 3527–30.PubMedGoogle Scholar
  12. Güth, K. &Junge, J. (1982) Low Ca2+ impedes cross-bridge detachment in chemically skinned Taenia coli.Nature. 300, 775–6.PubMedGoogle Scholar
  13. Higuchi, H. &Funatsu, T. (1989) Structure and function of connectin (titin) filaments revealed by selective removal with gelsolin of thin filaments in skeletal muscle.Proc. Internat. Union of Physiol. Sciences,XVII, P. 1449.Google Scholar
  14. Hinssen, H., Small, J. V. &Sobieszek, A. (1984) A Ca2+-dependent actin modulator from vertebrate smooth muscle.FEBS Letters 166, 90–5.PubMedGoogle Scholar
  15. Kilhoffer, M-C., Mely, Y. &Gerard, D. (1985) The effect of plasma gelsolin on actin filaments. Ca2+-dependency of the capping and the severing activities.Biochem. Biophys. Res. Commun. 131, 1132–8.PubMedGoogle Scholar
  16. Koffer, A. &Sleep, J. (1987) Activation of myosin ATPase by actin isolated from cultured BHK cells and the effect of gelsolin.J. Musc. Res. Cell Mot. 8, 541–7.Google Scholar
  17. Kossmann, T., Fürst, D. &Small, J. V. (1987) Structural and biochemical analysis of skinned smooth muscle preparations.J. Muse. Res. Cell Mot. 8, 135–44.Google Scholar
  18. Kwiatkowski, D. J., Stossel, T. P., Orkin, S. H., Mole, J. E., Colten, H. R. &Yin, H. L. (1986) Plasma and cytoplasmic gelsolins are encoded by a single gene and contain a duplicated actin-binding domain.Nature.323, 455–8.PubMedGoogle Scholar
  19. Kwiatkowski, D. J., Mehl, R. &Yin, H. L. (1988) Genomic organization and biosynthesis of secreted and cytoplasmic forms of gelsolin.J. Cell Biol. 106, 375–84.PubMedGoogle Scholar
  20. Lind, S. E., Smith, D. B., Janmey, P. A. &Stossel, T. P. (1986) Role of plasma gelsolin and vitamin D-binding protein in clearing actin from the circulation.J. Clin. Invest. 78, 736–42.PubMedGoogle Scholar
  21. Mooseker, M. S., Graves, T. A., Wharton, K. A., Falco, N. &Howe, C. L. (1980) Regulation of microvillus structure: calcium-dependent solation and cross-linking of actin filaments in the microvilli of intestinal epithelial cells.J. Cell Biol. 87, 809–22.PubMedGoogle Scholar
  22. Murakami, U. &Uchida, K. (1985) Contents of myofibrillar proteins in cardiac, skeletal and smooth muscles.J. Biochem. 98, 187–97.PubMedGoogle Scholar
  23. Nodes, B. R., Shackelford, J. E. &Lebherz, H. G. (1987) Synthesis and secretion of serum gelsolin by smooth muscle tissue.J. Biol. Chem. 262, 5422–7.PubMedGoogle Scholar
  24. Pollard, T. D. &Cooper, J. A. (1986) Actin and actin-binding proteins. A critical evaluation of mechanisms and functions.Ann. Rev. Biochem. 55, 987–1035.PubMedGoogle Scholar
  25. Porte, F. &Harricane, M-C. (1986) Interactions of plasma gelsolin with actin. Isolation and characterization of binary and ternary plasma-gelsolin-actin complexes.Eur. J. Biochem. 154, 87–93.PubMedGoogle Scholar
  26. Potter, J. D. (1974) The content of troponin, tropomyosin, actin, and myosin in rabbit skeletal muscle myofibrils.Arch. Biochem. Biophys. 162, 436–41.PubMedGoogle Scholar
  27. Rome, E. (1972) Structural studies by X-ray diffraction of striated muscles permeated with certain ions and proteins.Cold Spring Harbor symposia on quantitative biology,37, 331–9.Google Scholar
  28. Small, J. V. (1974) Contractile units in vertebrate smooth muscle cells.Nature. 249, 324–7.PubMedGoogle Scholar
  29. Small, J. V. (1977) Studies on isolated smooth muscle cells: the contractile apparatus.J. Cell Sci. 24, 327–49.PubMedGoogle Scholar
  30. Small, J. V., Fürst, D. O. &De Mey, J. (1986) Localization of filamin in smooth muscle.J. Cell Biol. 102, 210–20.PubMedGoogle Scholar
  31. Smith, D. B., Janmey, P. A. &Lind, S. E. (1988) Circulating actin-gelsolin complexes following oleic acid-induced lung injury.Am. J. Path. 130, 261–7.PubMedGoogle Scholar
  32. Soua, Z., Porte, F., Harricane, M-C., Feinberg, J. &Capony, J-P. (1985) Bovine serum brevin. Purification by hydrophobic chromatography and properties.Eur. J. Biochem. 153, 275–87.PubMedGoogle Scholar
  33. Sparrow, M. P., Mrwa, U., Hofmann, F. &Rüegg, J. C. (1981) Calmodulin is essential for smooth muscle contraction.FEBS Letters. 125, 141–5.PubMedGoogle Scholar
  34. Stendahl, O. I. &Stossel, T. P. (1980) Actin-binding protein amplifies actomyosin contraction, and gelsolin confers calcium control on the direction of contraction.Biochem. Biophys. Res. Commun. 92, 675–81.PubMedGoogle Scholar
  35. Strzelecka-Golaszewska, H., Hinssen, H. &Sobieszek, A. (1984) Influence of an actin-modulating protein from smooth muscle on actin-myosin interaction.FEBS Letters. 177, 209–16.PubMedGoogle Scholar
  36. Sugino, H. &Matsumura, F. (1983) Fragmin induces tension reduction of actomyosin threads in the presence of micromolar levels of Ca2+.J. Cell Biol. 96, 199–203.PubMedGoogle Scholar
  37. Weeds, A. G., Gooch, J., Pope, B. &Harris, H. E. (1986) Preparation and characterization of pig plasma and platelet gelsolins.Eur. J. Biochem. 161, 69–76.PubMedGoogle Scholar
  38. Yin, H. L. &Stossel, T. P. (1979) Control of cytoplasmic actin gel-sol transformation by gelsolin, a calcium-dependent regulatory protein.Nature. 281, 583–6.PubMedGoogle Scholar
  39. Yin, H. L., Zaner, K. S. &Stossel, T. P. (1980) Ca2+ control of actin gelation. Interaction of gelsolin with actin filaments and regulation of actin gelation.J. Biol. Chem. 255, 9494–9500.PubMedGoogle Scholar
  40. Yin, H. L., Albrecht, J. H. &Fattoum, A. (1981) Identification of gelsolin, a Ca2+-dependent regulatory protein of actin gel-sol transformation, and its intracellular distribution in a variety of cells and tissues.J. Cell Biol. 91, 901–6.PubMedGoogle Scholar
  41. Yin, H. L., Kwiatkowski, D. J., Mole, J. E. &Cole, F. S. (1984) Structure and biosynthesis of cytoplasmic and secreted variants of gelsolin.J. Biol. Chem. 259, 5271–6.PubMedGoogle Scholar
  42. Zeece, M. G., Robson, R. M. &Bechtel, P. J. (1979) Interaction of α-actinin, filamin and tropomyosin with F-actin.Biochem. Biophys. Acta. 581, 365–70.PubMedGoogle Scholar

Copyright information

© Chapman and Hall Ltd 1990

Authors and Affiliations

  • Ph. Gailly
    • 1
  • Th. Lejeune
    • 1
  • J. P. Capony
    • 2
  • J. M. Gillis
    • 1
  1. 1.Département de PhysiologieUniversité Catholique de Louvain, UCL 5540BruxellesBelgium
  2. 2.Centre de Recherche de Biochimie MacromoléculaireCNRS, et INSERM U 249MontpellierFrance

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