The Journal of Membrane Biology

, Volume 50, Issue 1, pp 1–14 | Cite as

Microtubules inside the plasma membrane of squid giant axons and their possible physiological function

  • Gen Matsumoto
  • Hikoichi Sakai


The effects of application of the microtubule-disassembling reagents to squid giant axons upon resting potential, the height of the propagated action potential, and the threshold to evoke action potential were studied using colchicine, podophyllotoxin, vinblastine, griseofulvin, sulfhydryl reagents including NEM, diamide, DTNB and PCMB, and Ca2+ ions. At the same time, the effects of concentrations of K halides and K glutamate on the above physiological properties were studied in comparison within vitro characteristics of microtubule assembly from purified axoplasmic tubulin.

It was found that there was good correlation between conditions supporting maintenance of membrane excitability and microtubule assembly. The experiments suggest that associated with the internal surface of the plasma membrane there are microtubules which regulate in part both resting and action potentials.


Plasma Membrane Glutamate Colchicine Physiological Function Halide 
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. Abe, T., Haga, T., Kurokawa, M. 1973. Rapid transport of phosphatidylcholine occurring simultaneously with protein transport in the frog sciatic nerve.Biochem. J. 136:731Google Scholar
  2. Baker, P.F., Hodgkin, A.L., Meves, H. 1964. The effect of diluting the internal solution on the electrical properties of a perfused giant axon.J. Physiol. (London) 170:541Google Scholar
  3. Baumgold, J., Matsumoto, G., Tasaki, I. 1978. Biochemical studies of nerve excitability: The use of protein modifying reagents for characterizing sites involved in nerve excitation.J. Neurochem. 30:91Google Scholar
  4. Begenisich, T., Lynch, C. 1974. Effects of internal divalent cations on voltage-clamped squid axon.J. Gen. Physiol. 63:675Google Scholar
  5. Chandler, W.K., Hodgkin, A.L., Meves, H. 1965. The effect of changing the internal solution on sodium inactivation and related phenomena in giant axons.J. Physiol. (London) 180:821Google Scholar
  6. Davison, P.F., Huneeus, F.C. 1970. Fibrillar proteins from squid axons: II. Microtubule protein.J. Mol. Biol. 52:429Google Scholar
  7. Frankenhaeuser, B., Hodgkin, A.L. 1957. The action of calcium on the electrical properties of squid axons.J. Physiol. (London) 137:218Google Scholar
  8. Gainer, H., Carbone, E., Singer, I., Sisco, K., Tasaki, I. 1974. Depolarization-induced change in the enzymatic radio-iodination of a protein on the internal surface of the squid giant axon membrane.Comp. Biochem. Physiol. 47 A:477Google Scholar
  9. Gainer, H., Gainer, V. S. 1976. Proteins in the squid giant axons.In: Electrobiology of Nerve, Synapse and Muscle. J.P., Reuben, D.P. Purpura, M.V.L. Bennett and E.R. Kandel, editors. p. 155. Raven Press, New YorkGoogle Scholar
  10. Haga, T., Kurokawa, M. 1975. Microtubule formation from two components separated by gel filtration of a tubulin preparation.Biochim. Biophys. Acta 392:335.Google Scholar
  11. Hodgkin, A.L., Katz, B. 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid.J. Physiol. (London) 108:37Google Scholar
  12. Huneeus, F.C., Davison, P.F. 1970. Fibrillar proteins from squid axons. I. Neurofilament protein.J. Mol. Biol. 52:415Google Scholar
  13. Inoue, I., Pant, H.C., Tasaki, I., Gainer, H. 1976. Release of proteins from the inner surface of squid axon membrane labeled with tritiated N-ethylmaleimide.J. Gen. Physiol. 68:385Google Scholar
  14. James, K.A.C., Bray, J.J., Morgan, I.G., Austin, L. 1970. The effect of colchicine on the transport of axonal protein in the chicken.Biochem. J. 117:767Google Scholar
  15. Kobayashi, T., Shimizu, T. 1976. Roles of nucleoside triphosphates in microtubule assembly.J. Biochem. (Tokyo) 79:1357Google Scholar
  16. Kuriyama, R., Sakai, H. 1974. Role of tubulin-SH groups in polymerization to microtubules. Functional-SH groups in tubulin for polymerization.J. Biochem. (Tokyo) 76:651Google Scholar
  17. Matsumoto, G. 1976. Transportation and maintenance of adult squid (Doryteuthis bleekeri) for physiological studies.Biol. Bull. 150:279Google Scholar
  18. Metuzals, J., Tasaki, I. 1978. Subaxolemmal filamentous network in the giant nerve fiber of the squid (Loligo pealei 1.) and its possible role in excitability.J. Cell Biol. 78:597Google Scholar
  19. Mohri, H. 1976. The function of tubulin in motile systems.Biochim. Biophys. Acta 456:85Google Scholar
  20. Olmsted, J. B., Borisy, G. G. 1975. Ionic and nucleotide requirements for microtubule polymerizationin vitro.Biochemistry 14:2996Google Scholar
  21. Pant, H. C., Terakawa, S., Baumgold, J., Tasaki, I., Gainer, H. 1978. Protein release from the internal surface of the squid giant axon membrane during excitation and potassium depolarization.Biochim. Biophys. Acta 513:132Google Scholar
  22. Roobol, A., Gull, K., Pogson, C. I. 1976. Inhibition by griseofulvin of microtubule assemblyin vitro.FEBS Lett. 67:248Google Scholar
  23. Sakai, H., Matsumoto, G. 1978. Tubulin and other proteins from squid giant axons.J. Biochem. (Tokyo) 83:1413Google Scholar
  24. Schauf, C. L. 1975. The interaction of calcium withmyxicola giant axons and a description in terms of a simple surface charge model.J. Physiol. (London) 248:613Google Scholar
  25. Snyder, J.A., McIntosh, J.R. 1976. Biochemistry and physiology of microtubules.Annu. Rev. Biochem. 45:699Google Scholar
  26. Stadler, J., Franke, W.W. 1974. Characterization of the colchicine binding of membrane fractions from rat and mouse liver.J. Cell Biol. 60:297Google Scholar
  27. Takahashi, K., Yoshii, M. 1978. Effects of internal free calcium upon the sodium and calcium channels in the tunicate egg analyzed by the internal perfusion technique.J. Physiol. (London) 279:519Google Scholar
  28. Takenaka, T., Yoshioka, T., Horie, H., Watanabe, F. 1976. Changes in125I-labeled membrane proteins during excitation of the squid giant axon.Comp. Biochem. Physiol. 55B:89Google Scholar
  29. Tasaki, I. 1968. Nerve Excitation: A Macromolecular Approach. Charles C. Thomas, Springfield, Ill.Google Scholar
  30. Tasaki, I., Singer, I., Takenaka, T. 1965. Effects of internal and external ionic environment on excitability of squid giant axon; a macromolecular approach.J. Gen. Physiol. 48:1095Google Scholar
  31. Tasaki, I., Watenabe, A., Lerman, L. 1967. Role of divalent cations in excitation of squid giant axons.Am. J. Physiol. 213:1465Google Scholar
  32. Terakawa, S., Nagano, M., Watanabe, A., 1977. Intracellular divalent cations and plateau duration of squid giant axons treated with tetraethylammonium.Jpn. J. Physiol. 27:785Google Scholar
  33. Weber, K., Wehland, J., Herzog, W. 1976. Griseofulvin interacts with microtubules bothin vivo andin vitro.J. Mol. Biol. 102:817Google Scholar
  34. Weisenberg, R.C. 1972. Microtubule formationin vitro in solutions containing low calcium concentrations.Science 177:1104Google Scholar
  35. Wilson, L., Bamburg, J.R., Mizel, S.B., Grisham, L.M., Creswell, K.M. 1974. Interaction of drugs with microtubule proteins.Fed. Proc. 33:158Google Scholar
  36. Yoshioka, T., Pant, H.C., Tasaki, I., Baumgold, J., Matsumoto, G., Gainer, H. 1978. An approach to the study of intracellular proteins related to the excitability of the squid giant axon.Biochim. Biophys. Acta 538:616Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1979

Authors and Affiliations

  • Gen Matsumoto
    • 1
    • 2
  • Hikoichi Sakai
    • 1
    • 2
  1. 1.Optoelectronics SectionElectrotechnical LaboratoryTanashi, TokyoJapan
  2. 2.Department of Biophysics and Biochemistry, Faculty of ScienceUniversity of TokyoTokyoJapan

Personalised recommendations