Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Inositol 1,4,5-trisphosphate induces calcium release from sarcoplasmic reticulum of skeletal muscle

Abstract

The sarcoplasmic reticulum of skeletal muscle is a specialized form of endoplasmic reticulum1 that controls myoplasmic calcium concentration and, therefore, the contraction–relaxation cycle2. Ultrastructural studies3 have shown that the sarcoplasmic reticulum is a continuous but heterogeneous membranous network composed of longitudinal tubules that surround myofibrils and terminal cisternae. These cisternae are junctionally associated, via bridging structures called ‘feet’4, with sarcolemmal invaginations (the transverse tubules) to form the triadic junction4. Following transverse tubule depolarization, a signal, transmitted along the triadic junction, triggers Ca2+ release from terminal cisternae5,6, but the mechanism of this coupling is still unknown7. Inositol 1,4,5-trisphosphate (Ins(1,4,5)P3) has recently been shown to mobilize Ca2+ from intracellular stores, referable to endoplasmic reticulum, in a variety of cell types (see ref. 8 for review), including smooth muscle cells of the porcine coronary artery9 and canine .cardiac muscle cells10. Here we show that Ins(1,4,5)P3 (1) releases Ca2+ from isolated, purified sarcoplasmic reticulum fractions of rabbit fast-twitch skeletal muscle, the effect being more pronounced on a fraction of terminal cisternae that contains morphologically intact feet structures11 ; and (2) elicits isometric force development in chemically skinned muscle fibres.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Porter, K. R. & Palade, G. E. Biophys. biochem. Cytol. 3, 269–300 (1957).

    Article  CAS  Google Scholar 

  2. De Meis, L. in Transport in Life Sciences Vol. 2 (ed Bittar, E. E.) 1–163 (Wiley, New York, 1981).

    Google Scholar 

  3. Peachey, L. D. J. Cell Biol. 25, 209–231 (1965).

    Article  Google Scholar 

  4. Franzini Armstrong, C. J. Cell Biol. 47, 488–499 (1970).

    Article  CAS  Google Scholar 

  5. Huxley, A. F. & Taylor, R. E. J. Physiol., Lond. 144, 426–441 (1958).

    Article  CAS  Google Scholar 

  6. Winegrad, S. J. gen. Physiol. 55, 77–88 (1970).

    Article  CAS  Google Scholar 

  7. Endo, M. Physiol. Rev. 57, 71–108 (1977).

    Article  CAS  Google Scholar 

  8. Berridge, M. J. & Irvine, R. F. Nature 312, 315–321 (1984).

    Article  ADS  CAS  Google Scholar 

  9. Suematsu, E., Hirata, M., Hashimoto, T. & Kuriyama, H. Biochem. biophys. Res. Commun. 120, 481–485 (1984).

    Article  CAS  Google Scholar 

  10. Hirata, M., Suematsu, E., Hashimoto, T., Hamachi, T. & Koga, T. Biochem. J. 223, 229–236 (1984).

    Article  CAS  Google Scholar 

  11. Saito, A., Seiler, S., Chu, A. & Fleischer, S. J. Cell Biol. 99, 875–885 (1984).

    Article  CAS  Google Scholar 

  12. Campbell, K. P. & Shamoo, A. E. J. Membrane. Biol. 54, 73–80 (1980).

    Article  CAS  Google Scholar 

  13. Miyamoto, H. & Racker, E. J. Membrane Biol. 66, 193–201 (1982).

    Article  CAS  Google Scholar 

  14. Mitchell, R. D., Volpe, P., Palade, P. & Fleischer, S. J. biol Chem. 258, 9867–9877 (1983).

    CAS  PubMed  Google Scholar 

  15. Kim, D. H., Ohnishi, S. T. & Ikemoto, N. J. biol. Chem. 258, 2365–2374 (1983).

    Google Scholar 

  16. Volpe, P., Palade, P., Costello, B., Mitchell, R. D. & Fleischer, S. J. biol Chem. 258, 12434–12442 (1983).

    CAS  PubMed  Google Scholar 

  17. Wood, D. S., Zollman, J. R., Reuben, J. P. & Brandt, P. W. Science 187, 1075–1076 (1975).

    Article  ADS  CAS  Google Scholar 

  18. Julian, F. J. J. Physiol., Lond. 218, 117–145 (1971).

    Article  CAS  Google Scholar 

  19. Somlyo, A. V., Gonzales-Serratos, H., Shuman, H., McLellan, G. & Somlyo, A. P. J. Cell Biol. 90, 577–594 (1981).

    Article  CAS  Google Scholar 

  20. Weber, A. & Herz, R. J. gen. Physiol. 52, 750–759 (1968).

    Article  CAS  Google Scholar 

  21. Luttgau, H. C. & Oetlicher, H. J. Physiol., Lond. 194, 51–74 (1968).

    Article  CAS  Google Scholar 

  22. Stephenson, E. W. J. gen. Physiol. 77, 419–443 (1981).

    Article  CAS  Google Scholar 

  23. Vergara, J. & Tsien, R. Y. Biophys. J. 47, 351a (1985).

    Google Scholar 

  24. Downes, C. P., Mussat, M. C. & Michell, R. H. Biochem. J. 203, 169–177 (1982).

    Article  CAS  Google Scholar 

  25. Novotny, I., Saleh, F. & Novotna, R. Gen. Physiol. Biophys. 2, 329–337 (1983).

    CAS  PubMed  Google Scholar 

  26. Ferenczi, M. A., Homsher, E. & Trentham, D. R. J. Physiol, Lond. 352, 575–599 (1984).

    Article  CAS  Google Scholar 

  27. Brown, J. E. et al. Nature 311, 160–163 (1984).

    Article  ADS  CAS  Google Scholar 

  28. Ghalayini, A. & Anderson, R. E. Biochem. biophys. Res. Commun. 124, 503–506 (1984).

    Article  CAS  Google Scholar 

  29. Gould, G. H. & Korenbrot, J. I. Proc. natn. Acad. U.S.A. 77, 5557–5561 (1980).

    Article  ADS  Google Scholar 

  30. Irvine, R. F., Brown, K. D. & Berridge, M. J. Biochem. J. 221, 269–272 (1984).

    Article  Google Scholar 

  31. Meissner, G. Molec. cell. Biochem. 55, 62–82 (1983).

    Article  Google Scholar 

  32. Zorzato, F., Salviati, G., Facchinetti, T. & Volpe, P. J. biol Chem.(in the press).

  33. Lowry, O. H., Rosebrough, N. J., Farr, A. R. & Randall, R. J. J. biol. Chem. 192, 265–275 (1951).

    Google Scholar 

  34. Downes, C. P. & Michell, R. H. Biochem. J. 133–140 (1981).

    Article  CAS  Google Scholar 

  35. Salviati, G., Sorenson, M. M. & Eastwood, A. R. J. gen. Physiol. 79, 603–632 (1982).

    Article  CAS  Google Scholar 

  36. Orentlicher, M., Brandt, P. W. & Reuben, J. P. Am. J. Physiol. 233, C127–C134 (1977).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Volpe, P., Salviati, G., Di Virgilio, F. et al. Inositol 1,4,5-trisphosphate induces calcium release from sarcoplasmic reticulum of skeletal muscle. Nature 316, 347–349 (1985). https://doi.org/10.1038/316347a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/316347a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing