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X-ray diffraction study on mammalian visceral smooth muscles in resting and activated states

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Summary

Structural changes of guinea pig taenia coli and rat anococcygeus muscle during contraction were studied by X-ray diffraction. The diffraction pattern of the taenia coli showed the 14.4-nm myosin reflection, the 5.9-nm actin layer-line and a diffuse equatorial peak at 1/11.4 nm-1. On application of carbachol, the muscle contracted and the intensity of the 14.4-nm reflection showed a concentration-dependent decrease: the maximum decrease was 24% at 2×10-5 M. Such an intensity decrease was not observed in K-contrature (154 mM). The intensity of the 5.9-nm actin layer-line did not change appreciably on activation. The equatorial peak became broader during contraction. The 14.4-nm myosin reflection of the anococcygeus muscle was weak. Its intensity increased by 106% during contraction induced by 2×10-5 M phenylephrine and by 75% during K-contracture. These results suggest that the number of myosin filaments may increase during contraction of rat anococcygeus muscle but not guinea pig taenia coli.

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References

  • AMEMIYA, Y., WAKABAYASHI, K., HAMANAKA, T., WAKABAYASHI, T., HASHIZUME, H. & MATSUSHITA, T. (1983) Design of a small-angle X-ray diffractometer using synchrotron radiation at the photon factory. Nucl. Instr. Meth. 208, 471–7.

    Google Scholar 

  • AMEMIYA, Y., WAKABAYASHI, K., TANAKA, H., UENO, Y. & MIYAHARA, J. (1987) Laser-stimulated luminescence used to measure X-ray diffraction of a contracting striated muscle. Science 237, 164–8.

    Google Scholar 

  • ARNER, A., MALMQVIST, U., & WRAY, J. S. (1988) X-ray diffraction and electron microscopy of living and skinned rectococcygeus muscles of the rabbit. In Sarcomeric and Non-sarcomeric Muscles: Basic and Applied Research Prospects for the 90's (edited by U.Carraro), pp. 699–704. Padova: Unipress Padova.

    Google Scholar 

  • ARNER, A., RAPP, G. & WRAY, J. S. (1991) Time-resolved X-ray diffraction measurements on a living contracting mammalian smooth muscle. Biophys. J. 59, 10a.

    Google Scholar 

  • BAGBY, R. (1986) Toward a comprehensive three-dimensional model of the contractile system of vertebrate smooth muscle cells. Int. Rev. Cyt. 105, 67–128.

    Google Scholar 

  • CRAIG, R., SMITH, R. & KENDRICK-JONES, J. (1983) Light-chain phosphorylation controls the conformation of vertebrate non-muscle and smooth muscle myosin molecules. Nature 302, 436–9.

    Google Scholar 

  • DEFEO, T. T. & MORGAN, K. G. (1985) Calcium-force relationships as detected with aequorin in two different vascular smooth muscles of the ferret. J. Physiol. 369, 269–82.

    Google Scholar 

  • EBASHI, S. (1989) Calcium regulation of smooth muscle contraction. Prog. Clin. Biol. Res. 315, 239–51.

    Google Scholar 

  • ELLIOTT, G. F. & LOWY, J. (1968) Organization of actin in a mammalian smooth muscle. Nature 219, 156–7.

    Google Scholar 

  • GABELLA, G. (1981) Structure of smooth muscles. In Smooth Muscle: An Assessment of Current Knowledge (edited by BULBRING, E., BRADING, A. E., JONES, A. W. & TOMITA, T.) pp. 1–46. London:Edward Arnold.

    Google Scholar 

  • GAILLY, PH., LEJEUNE, Th., CAPONY, J. P. & GILLIS, J. M. (1990) The action of brevin, an F-actin severing protein, on the mechanical properties and ATPase activity of skinned smooth muscle. J. Muscle Res. Cell Motil. 11, 293–301.

    Google Scholar 

  • GAILLY, Ph., GILLIS, J. M. & CAPONY, J. P. (1991) Complex stiffness of smooth muscle cytoplasm in the presence of Ca-activated brevin. J. Muscle Res. Cell Motil. 12, 333–9.

    Google Scholar 

  • GILLESPIE, J. S. (1972) The rat anococcygeus muscle and its response to nerve stimulation and to some drugs. Br. J. Pharmacol. 45, 404–16.

    Google Scholar 

  • GILLIS, J. M., CAO, M. L. & GODFRAIND-DE BECKER, A. (1988) Density of myosin filaments in the rat anococcygeus muscle, at rest and in contraction. II. J. Muscle Res. Cell Motil. 9, 18–29.

    Google Scholar 

  • GODFRAIND-DE BECKER, A. & GILLIS, J. M. (1988) Analysis of the birefringence of the smooth muscle anococcygeus of the rat, at rest and in contraction. I. J. Muscle Res. Cell Motil. 9, 9–17.

    Google Scholar 

  • HASELGROVE, J. C. (1975) X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle. J. Mol. Biol. 92, 113–43.

    Google Scholar 

  • HIMPENS, B. & CASTEELS, R. (1990) Different effects of depolarization and muscarinic stimulation on the Ca2+/force relationship during the contraction-relaxation cycle in the guinea pig ileum. Pflügers Arch. 416, 28–35.

    Google Scholar 

  • KAMM, K. E. & STULL, J. T. (1985) The function of myosin light chain kinase phosphorylation in smooth muscle. Ann. Rev. Pharmacol. Toxicol. 25, 593–620.

    Google Scholar 

  • KRESS, M., HUXLEY, H. E., FARUQI, A. R. & HENDRIX, J. (1986) Structural changes during activation of frog muscle studied by time-resolved X-ray diffraction. J. Mol. Biol. 188, 325–42.

    Google Scholar 

  • LOWY, J., POULSEN, F. R. & VIBERT, P. J. (1970) Myosin filaments in vertebrate smooth muscle. Nature 225, 1053–4.

    Google Scholar 

  • LOWY, J., VIBERT, P. J., HASELGROVE, J. C. & POULSEN, F. R. (1973) The structure of the myosin elements in vertebrate smooth muscles. Phil. Trans. R. Soc. Lond. B 265, 191–6.

    Google Scholar 

  • MARSTON, S. B. & LEHMAN, W. (1985) Caldesmon is a Ca2+-regulatory component of native smooth muscle thin filaments. Biochem. J. 231, 517–22.

    Google Scholar 

  • MATSUBARA, I., YAGI, N., MIURA, H., OZEKI, M. & IZUMI, T. (1984) Intensification of the 5.9-nm actin layer line in contracting muscle. Nature 312, 471–3.

    Google Scholar 

  • ONISHI, H. & WAKABAYASHI, T. (1982) Electron microscopic studies of myosin molecules from chicken gizzard muscle. I. The formation of the intramolecular loop in the myosin tail. J. Biochem. 92, 871–9.

    Google Scholar 

  • POPP, D. & HOLMES, K. C. (1992) X-ray diffraction studies on oriented gels of vertebrate smooth muscle thin filaments. J. Mol. Biol. 224, 65–76.

    Google Scholar 

  • POULSEN, F. R., LOWY, J., COOKE, P. H., BARTELS, E. M., ELLIOTT, G. F. & HUGHES, R. A. (1987) Diffuse X-ray scatter from myosin heads in oriented synthetic filaments. Biophys. J. 51, 959–67.

    Google Scholar 

  • SHOENBERG, C. F. & HASELGROVE, J. C. (1974) Filaments and ribbons in vertebrate smooth muscle. Nature 249, 152–4.

    Google Scholar 

  • SMALL, J. V. & SQUIRE, J. M. (1972) Structural basis of contraction in vertebrate smooth muscle. J. Mol. Biol. 67, 117–49.

    Google Scholar 

  • SOBUE, K., MURAMOTO, Y., FUJITA, M. & KAKIUCHI, S. (1981) Purification of calmodulin-binding protein from chicken gizzard that interacts with F-actin. Proc. Natl. Acad. Sci. USA 78, 5652–5.

    Google Scholar 

  • SOMLYO, A. P., SOMLYO, A. V., DEVINE, C. E., & RICE, R. V. (1971) Aggregation of thick filaments into ribbons in mammalian smooth muscle. Nature New Biol. 231, 243–6.

    Google Scholar 

  • SOMLYO, A. V., BUTLER, T. M., BOND, M. & SOMLYO, A. P. (1981) Myosin filaments have non-phosphorylated light chains in relaxed smooth muscle. Nature 294, 567–9.

    Google Scholar 

  • SUZUKI, H., ONISHI, H., TAKAHASHI, K. & WATANABE, S. (1978) Structure and function of chicken gizzard myosin. J. Biochem. 84, 1529–42.

    Google Scholar 

  • TAKAHASHI, K., HIWADA, K. & KOKUBU, T. (1986) Isolation and characterization of a 34 000-dalton calmodulin- and Factin-binding protein from chicken gizzard smooth muscle. Biochem. Biophys. Res. Commun. 141, 20–6.

    Google Scholar 

  • TRYBUS, K. M. & LOWEY, S. (1984) Conformational states of smooth muscle myosin: effects of light chain phosphorylation and ionic strength. J. Biol. Chem. 259, 8564–71.

    Google Scholar 

  • VIBERT, P. J., HASELGROVE, J. C., LOWY, J. & POULSEN, F. R. (1972) Structural changes in actin-containing filaments of muscle. J. Mol. Biol. 71, 757–67.

    Google Scholar 

  • WAKABAYASHI, K., TANAKA, H., AMEMIYA, Y., FUJISHIMA, A., KOBAYASHI, T., HAMANAKA, T., SUGI, H. & MITSUI, T. (1985) Time-resolved X-ray diffraction studies on the intensity changes of the 5.9 and 5.1 nm actin layer-lines from frog skelatal muscle during an isometric tetanus using synchrotron radiation. Biophys. J. 47, 847–50.

    Google Scholar 

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Watanabe, M., Takemori, S. & Yagi, N. X-ray diffraction study on mammalian visceral smooth muscles in resting and activated states. J Muscle Res Cell Motil 14, 469–475 (1993). https://doi.org/10.1007/BF00297209

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