Abstract
Inositol 1,4,5-trisphosphate (InsP3) can stimulate skinned smooth and skeletal muscle to contract by initiating Ca2+ release from the sarcoplasmic reticulum1–5,27. Whether this process is an integral component of the in vivo muscle activation mechanism was tested by releasing InsP3 rapidly within skinned muscle fibres of rabbit main pulmonary artery and frog semitendinosus. InsP3 was liberated on laser pulse photolysis of a photolabile but biologically inactive precursor of InsP3 termed caged InsP3. Caged InsP3 is a mixture of compounds in which InsP3 is esterified with 1(2-nitrophenyl)diazoethane (probably at the P4- or P5 -position). Photochemical release of InsP3 induced a full contraction in both muscles at physiological free Mg2+ concentrations, but only in the smooth muscle were the InsP3 concentration (0.5 µM) and the activation rate compatible with the in vivo physiological response. Endogenous InsP3-specific phosphatase activity was present in smooth muscle and had about 35-fold greater activity than that in the skeletal-muscle preparation. Caged InsP3 was not susceptible to phosphatases in either preparation.
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References
1. Somlyo, A. V., Bond, M., Somlyo, A. P. & Scarpa, A. Proc. natn. Acad. Sci. U.S.A. 82, 5231–5235 (1985). 2. Suematsu, E., Hirata, M., Hashimoto, T. & Kuriyama, H. Biochem. biophys. Res. Commun. 120, 481–485 (1984). 3. Vergara, J., Tsien, R. Y. & Delay, M. Proc. natn. Acad. Sci. U.S.A. 82, 6352–6356 (1985). 4. Volpe, P., Salviati, G., Di Virgilio, F. & Pozzan, T. Nature 316, 347–349 (1985). 5. Donaldson, S. K., Goldberg, N. D., Walseth, T. F. & Huetteman, D. A. Biophys. J. 49,191a (1986). 6. Baylor, S. M. in The Handbook of Physiology: Skeletal Muscle (eds Peachey, L. D., Adrian, R. H. & Geiger, S. R.) 355–379 (Am. Physiol. Soc., Bethesda, Maryland, 1983). 7. Hartshorne, D. J. & Gorecka, A. in The Handbook of Physiology: The Cardiovascular System, Vascular Smooth Muscle Vol. II (eds Bohr, D. F., Somlyo, A. P. & Sparks, H. V.) 93–120 (Am. Physiol. Soc., Bethesda, Maryland, 1980). 8. Johansson, B. & Somlyo, A. P. in The Handbook of Physiology: The Cardiovascular System, Vascular Smooth Muscle Vol. II (eds Bohr, D. F., Somlyo, A. P. & Sparks, H. V.) 301–324 (Am. Physiol. Soc., Bethesda, Maryland, 1980) . 9. Somlyo, A. P. & Somlyo, A. V. /. Pharmac. exp. Ther. 159, 129–145 (1968). 10. Berridge, M. J. & Irvine, R. F. Nature 312, 315–321 (1984). 11. Fabiato, A. in The Regulation of Excitation and Contraction (ed. Nathan, R. D.) 283–293 (Academic, New York, 1986). 12. Lea, T. J., Griffiths, P. J., Tregear, R. T. & Ashley, C. C. FEES Lett. 207, 153–161 (1986). 13. Goldman, Y. E., Reid, G. P., Somlyo, A. P., Somlyo, A. V., Trentham, D. R. & Walker, J. W. J. Physiol, Lond. 377, 100P (1986). 14. McCray, J. A., Herbette, L., Kihara, T. & Trentham, D. R. Proc. natn. Acad. Sci. U.S.A. 77, 7237–7241 (1980). 15. Goldman, Y. E., Hibberd, M. G. & Trentham, D. R. / Physiol., Lond. 354, 577–604 (1984). 16. Devine, C. E., Somlyo, A. V. & Somlyo, A. P. J. cell Biol. 52, 690–718 (1972). 17. Kamm, K. E. & Stull, J. T. Science 232, 80–82 (1986). 18. Somlyo, A. P. et al. J. Mus. Res. Cell Motil. 7, 38 (1986). 19. Kress, M., Huxley, H. E., Faruqi, A. R. & Hendrix, J. /. molec. Biol. 188, 325–342 (1986). 20. Stephenson, E. W. / gen. Physiol. 77, 419–443 (1981). 21. Endo, M. Physiol. Rev. 57, 71–108 (1971). 22. Downes, C. P., Mussat, M. C. & Michell, R. H. Biochem. J. 203, 169–177 (1983). 23. Volpe, P., Di Virgilio, F., Pozzan, T. & Salviati, G. FEES Lett. 97, 1–4 (1986). 24. Somlyo, A. P. Nature 316, 298–299 (1985). 25. Irvine, R. F., Anggard, E. E., Letcher, A. J. & Downes, C. P. Biochem. J. 229,505–511 (1985). 26. Irvine, R. F., Brown, K. D. & Berridge, M. J. Biochem. J. 222, 269–272 (1984). 27. lino, M. Biochem. biophys. Res. Commun. 142, 47–52 (1987).
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Walker, J., Somlyo, A., Goldman, Y. et al. Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate. Nature 327, 249–252 (1987). https://doi.org/10.1038/327249a0
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DOI: https://doi.org/10.1038/327249a0
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