Protein-Protein Interactions and the Functional States of Sarcoplasmic Reticulum Membranes

  • A. Martonosi
  • H. Nakamura
  • R. L. Jilka
  • J. H. Vanderkooi
Part of the Proceedings in Life Sciences book series (LIFE SCIENCES)


Rapid kinetic and electron microscope observations suggest that cooperative phenomena play an important role in the mechanism of Ca transport and Ca release by sarcoplasmic reticulum. The observations are consistent with the occurrence of tetramers of Ca transport ATPase in the membrane in equilibrium with monomers and dimers.

Fluorescence energy transfer between ATPase molecules labeled with N (iodoacetylamino)-1-naphthylamine-5-sulfonic acid (1,5-IAEDANS) and iodoacetamidofluorescein (IAF) support these conclusions.

A hypothesis is presented in which the physiological release of Ca from sarcoplasmic reticulum occurs through hydrophilic channels generated by the reversible formation of ATPase tetramers under the influence of action potential.


Sarcoplasmic Reticulum Purple Membrane Frog Skeletal Muscle Sarcoplasmic Reticulum Membrane Fluorescence Energy Transfer 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ashley, C.C., Caldwell, P.C.: Calcium movements in relationship to contraction. Biochem. Soc. Symp. 39, 29–50 (1974)PubMedGoogle Scholar
  2. Barlogie, B., Hasselbach, W., Makinose, M.: Activation of calcium efflux by ADP and inorganic phosphate. FEBS Lett. 12, 267–268 (1971)PubMedCrossRefGoogle Scholar
  3. Baylor, S.M., Oetliker, H.: Birefringence experiments on isolated skeletal muscle fibers suggest a possible signal from the sarcoplasmic reticulum. Nature (London) 253, 97–101 (1975)CrossRefGoogle Scholar
  4. Bianchi, C.P.: Calcium movements in muscle. Circulation 24, No, 2, Part 2, 518–522 (1961)Google Scholar
  5. Bezanilla, T., Horowicz, P.: Fluorescence intensity changes associated with contractile activation in frog muscle stained with Nile blue A. J. Physiol. 246, 709–735 (1975)PubMedGoogle Scholar
  6. Boland, A.R., Jilka, R.L., Martonosi, A.: Passive Ca permeability of phospholipid vesicles and sarcoplasmic reticulum membranes. J. Biol. Chem. 250, 7501–7510 (1975)PubMedGoogle Scholar
  7. Boland, R., Martonosi, A., Tillack, T.W.: Developmental changes in the composition and function of sarcoplasmic reticulum. J. Biol. Chem. 249, 612–623 (1974)PubMedGoogle Scholar
  8. Bunting, J.R., Cathou, R.E.: Energy transfer distance measurements in immunoglobulins. J. Mol. Biol. 77, 223–235 (1973)PubMedCrossRefGoogle Scholar
  9. Chandler, W.K., Rakowski, R.F., Schneider, M.I.: A non-linear voltage dependent charge movement in frog skeletal muscle. J. Physiol. 254, 245–283 (1976)PubMedGoogle Scholar
  10. Costantin, L.L.: The role of sodium current in the radial spread of contraction in frog muscle fibers. J. Gen. Physiol. 55, 703–715 (1970)PubMedCrossRefGoogle Scholar
  11. Ebashi, S., Endo, M.: Calcium ion and muscle contraction. Progr. Biophys. Mol. Biol. 18, 123–183 (1968)CrossRefGoogle Scholar
  12. Edidin, M.: Rotational and translational diffusion in membranes. Ann. Rev. Biophys. Bioeng. 3, 179–201 (1974)CrossRefGoogle Scholar
  13. Eisenberg, R.S., Gage, P.W.: Ionic conductances of the surface and transverse tubular membranes of frog sartorius fibers. J. Gen. Physiol. 53, 279–297 (1969)PubMedCrossRefGoogle Scholar
  14. Elson, E.L., Webb, W.W.: Concentration correlation spectroscopy: a new biophysical probe based on occupation number fluctuation. Ann. Rev. Biophys. Bioeng. 4, 311–334 (1975)CrossRefGoogle Scholar
  15. Finean, J.B., Martonosi, A.: The action of phospholipase C on muscle microsomes: a correlation of electron microscopy and biochemical data. Biochim. Biophys. Acta 98, 547–553 (1965)PubMedGoogle Scholar
  16. Henderson, R., Unwin, P.N.T.: Three-dimensional model of purple membrane obtained by electron microscopy. Nature (London) 257, 28–32 (1975)CrossRefGoogle Scholar
  17. Huang, K.H., Fairclough, R.H., Cantor, C.R.: Singlet energy transfer studies of the arrangement of proteins in the 30S Escherichia coli ribosome. J. Mol. Biol. 97, 443–470 (1975)PubMedCrossRefGoogle Scholar
  18. Huxley, A.F., Simmons, R.M.: Mechanical transients and the origin of muscular force. Cold Spring Harbor Symp. Quant. Biol. 37, 669–680 (1972)Google Scholar
  19. Ikemoto, N., Garcia, A.M., O’Shea, P.A., Gergely, J.: New structural aspects of proteins (ATPase, calsequestrin) of sarcoplasmic reticulum. J. Cell Biol. 67, No. 2, Part 2, 187a (1975)Google Scholar
  20. Jilka, R.L., Martonosi, A., Tillack, T.W.: Effect of the purified [Mg2+ + Ca2+]- activated ATPase of sarcoplasmic reticulum upon the passive Ca2+ permeability and ultrastructure of phospholipid vesicles. J. Biol. Chem. 250, 7511–7524 (1975)PubMedGoogle Scholar
  21. Kasai, M., Miyamoto, H.: Depolarization induced calcium release from sarcoplasmic reticulum membrane fragments by changing ionic environment. FEBS Lett. 34, 299–301 (1973)PubMedCrossRefGoogle Scholar
  22. LeMaire, M., Moller, J.V., Tanford, C.: Retention of enzyme activity by detergent-solubilized sarcoplasmic Ca2+-ATPase. Biochemistry 15, 2336–2342 (1976)CrossRefGoogle Scholar
  23. Louis, C., Shooter, E.M.: The proteins of rabbit skeletal muscle sarcoplasmic reticulum. Arch. Biochem. Biophys. 153, 641–655 (1972)PubMedCrossRefGoogle Scholar
  24. MacLennan, D.H., Holland, P.C.: The calcium transport ATPase of sarcoplasmic reticulum. In: The Enzymes of Biological Membranes, Martonosi, A. (ed.). New York: Plenum 1976, Vol. III, pp. 221–259Google Scholar
  25. Markham, R., Frey, S., Hills, G.J.: Methods for the enhancement of image detail and accentuation of structure in electron microscopy. Virology 20, 88–102 (1963)CrossRefGoogle Scholar
  26. Martonosi, A.: Role of phospholipids in ATPase activity and Ca transport of fragmented sarcoplasmic reticulum. Federation Proc. 23, 913–921 (1964)Google Scholar
  27. Martonosi, A.: The structure and function of sarcoplasmic reticulum membranes. In: Biomembranes. Manson, L.A. (ed.). New York: Plenum Press 1971, Vol. I, pp. 191–256Google Scholar
  28. Martonosi, A.: Biochemical and clinical aspects of sarcoplasmic reticulum function. In: Current Topics in Membranes and Transport. Bronner, F., Kleinzeller, A. (eds.). New York: Academic Press 1972, Vol. III, pp. 84–195Google Scholar
  29. Martonosi, A.: The mechanism of Ca2+ transport in sarcoplasmic reticulum. In: Calcium Transport in Contraction and Secretion. Carafoli et al. (eds.). Amsterdam: North Holland Publ. Corp. 1975, pp. 313–327Google Scholar
  30. Martonosi, A., Halpin, R.A.: Sarcoplasmic reticulum X. The protein composition of sarcoplasmic reticulum membranes. Arch. Biochem. Biophys. 144, 66–77 (1971)PubMedCrossRefGoogle Scholar
  31. Martonosi, A., Fortier, F.: The effect of anti-ATPase antibodies upon the Ca++ transport of sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 60, 382–389 (1974)PubMedCrossRefGoogle Scholar
  32. Murphy, A.J.: Crosslinking of the sarcoplasmic reticulum ATPase protein. Biochem. Biophys. Res. Commun. 70, 160–166 (1976)PubMedCrossRefGoogle Scholar
  33. Peachey, L.E.: Electrical events in the T-system of frog skeletal muscle. Cold Spring Harbor Symp. Quant. Biol. 37, 479–488 (1972)Google Scholar
  34. Saffman, P.G., Delbruck, M.: Brownian motion in biological membranes. Proc. Natl. Acad. Sci. U.S. 72, 3111–3113 (1975)CrossRefGoogle Scholar
  35. Schneider, M.F., Chandler, W.K.: Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature (London) 242, 244–246 (1973)CrossRefGoogle Scholar
  36. Stein, W.D., Eilam, Y., Lieb, W.R.: Active transport of cations across biological membranes. Ann. N.Y. Acad. Sci. 227, 328–336 (1974)PubMedCrossRefGoogle Scholar
  37. Stryer, L., Hoagland, R.P.: Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. U.S. 58, 719–726 (1967)CrossRefGoogle Scholar
  38. Tillack, T.W., Boland, R., Martonosi, A.: The ultrastructure of developing sarcoplasmic reticulum. J. Biol. Chem. 249, 624–633 (1974)PubMedGoogle Scholar
  39. Van der Kloot, W.G.: The effect of disruption of the T-tubules on calcium efflux from frog skeletal muscle. Comp. Biochem. Physiol. 26, 377–379 (1968)PubMedCrossRefGoogle Scholar
  40. Veatch, W., Stryer, L.: The dimeric nature of the gramicidin A transmembrane channel: conductance and fluorescence energy transfer studies of hybrid channels. J. Mol. Biol. (1976, in press)Google Scholar
  41. Weber, G.: Uses of fluorescence in biophysics: some recent developments. Ann. Rev. Biophys. Bioeng. 1, 553–569 (1972)CrossRefGoogle Scholar
  42. Winegrad, S.: The possible role of calcium in excitation-contraction coupling of heart muscle. Circulation 24, No. 2, Part 2, 523–529 (1961)PubMedGoogle Scholar
  43. Winegrad, S.: Autoradiographic studies of intracellular calcium in frog skeletal muscle. J. Gen. Physiol. 48, 455–479 (1965a)PubMedCrossRefGoogle Scholar
  44. Winegrad, S.: The location of muscle calcium with respect to the myofibrils. J. Gen. Physiol. 48, 997–1002 (1965b)PubMedCrossRefGoogle Scholar
  45. Wu, C.W., Stryer, L.: Proximity relationships in Rhodopsin. Proc. Natl. Acad. Sci. U.S. 69, 1104–1108 (1972)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1977

Authors and Affiliations

  • A. Martonosi
  • H. Nakamura
  • R. L. Jilka
  • J. H. Vanderkooi

There are no affiliations available

Personalised recommendations