Summary
Permeabilities of squid axon membranes to various cations at rest and during activity have been measured by voltage clamp before and during internal perfusion of 4×10−5 m grayanotoxin I. The resting sodium and potassium permeabilities were estimated to be 6.85×10−8 cm/sec and 2.84×10−6 cm/sec, respectively. Grayanotoxin I increased the resting sodium permeability to 7.38×10−7 cm/sec representing an 11-fold increase. The potassium permeability was increased only by a factor of 1.24. The resting permeability ratios as estimated by the voltage clamp method before application of grayanotoxin I were Na (1): Li (0.83): formamidine (1.34): guanidine (1.49): Cs (0.87): methylguanidine (0.86): methylamine (0.78). Grayanotoxin I did not drastically change the resting permeability ratios with a result of Na (1): Li (0.95): formamidine (1.27): guanidine (1.16): Cs (0.47): methylguanidine (0.72): methylamine (0.46). The membrane potential method gave essentially the same resting permeability ratios before and during application of grayanotoxin I if corrections were made for permeability to choline as the cation substitute and for changes in potassium permeability caused by test cations. The permeability ratio choline/Na was estimated to be 0.72 by the voltage clamp method and 0.65 by the membrane potential method. Grayanotoxin I decreased the ratio to 0.43. The permeability ratios during peak transient current were estimated to be Na (1): Li (1.12): formamidine (0.20): guanidine (0.20): Cs (0.085): methylguanidine (0.061): methylamine (0.036). Thus the sodium channels for the peak current are much more selective to cations than the resting sodium channels. It appears that the resting sodium channels in normal and grayanotoxin I-treated axons are operationally different from the sodium channels that undergo a conductance increase upon stimulation.
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References
Adelman, W. J., Jr., Senft, J. P. 1968. Dynamic asymmetries in axon membrane.J. Gen. Physiol. 51:102s
Albuquerque, E. X., Seyama, I., Narahashi, T. 1973. Characterization of batrachotoxin-induced depolarization of the squid giant axons.J. Pharmacol. Exp. Ther. 184:308
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) 170:541
Baker, P. F., Hodgkin, A. L., Shaw, T. I. 1962. The effects of changes in internal ionic concentrations on the electrical properties of perfused giant axons.J. Physiol. (London) 164:355
Cahalan, M. D., Begenisich, T. 1975. Internal K+ alters sodium channel selectivity.Biophys. J. 15 (2):261a
Chandler, W. K., Meves, H. 1965. Voltage clamp experiments on internally perfused giant axons.J. Physiol. 180:788
Cuervo, L. A., Adelman, W. J., Jr. 1970. Equilibrium and kinetic properties of the interaction between tetrodotoxin and the excitable membrane of the squid giant axon.J. gen. Physiol. 55:309
Eisenman, G. 1967. Particular properties of cation-selective glass electrodes containing Al2O3.In: Glass Electrodes for Hydrogen and Other Cations. G. Eisenman, editor. p. 268. Marcel Dekker, New York
Eisenman, G., Szabo, G., Ciani, S., McLaughlin, S., Kranse, S. 1973. Ion binding and ion transport produced by neutral lipid-soluble molecules.Prog. Surf. Membr. Sci. 6:139
Goldman, D. E. 1943. Potential, impedance, and rectification in membranes.J. Gen. Physiol. 27:37
Goldman, L., Binstock, L. 1969. Current separations inMyxicola giant axons.J. Gen. Physiol. 54:741
Hagiwara, S., Eaton, D. C., Stuart, A. E., Rosenthal, N. P. 1972. Cation selectivity of the resting membrane of squid axon.J. Membrane Biol. 9:373
Hagiwara, S., Toyama, K., Hayashi, H. 1971. Mechanisms of anion and cation permeations in the resting membrane of a barnacle muscle fiber.J. Gen. Physiol. 57:408
Hille, B. 1971. The permeability of the sodium channel to organic cations in myelinated nerve.J. Gen. Physiol. 58:599
Hille, B. 1972. The permeability of the sodium channel to metal cations in myelinated nerve.J. Gen. Physiol. 59:637
Hironaka, T., Narahashi, T. 1975. Ionic permeability profile of the resting axon membrane as affected by grayanotoxin I.Fed. Proc. 34:360
Hironaka, T., Narahasi, T. 1976. Cation permeability ratios of normal and grayanotoxintreated squid axon membranes.Biophys. J. 16 (2):187a
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) 108:37
Hodgkin, A. L., Keynes, R. D. 1955. The potassium permeability of a giant nerve fibre.J. Physiol. (London) 128:61
Hodgkin, A. L., Keynes, R. D. 1957. Movements of labelled calcium in squid giant axons.J. Physiol. (London) 138:253
Narahashi, T. 1974. Chemicals as tools in the study of excitable membranes.Physiol. Rev. 54:813
Narahashi, T., Albuquerque, E. X., Deguchi, T. 1971. Effects of batrachotoxin on membrane potential and conductance of squid giant axons.J. Gen. Physiol. 58:54
Narahashi, T., Anderson, N. C. 1967. Mechanism of excitation block by the insecticide allethrin applied externally and internally to squid giant axins.Toxic. Appl. Pharmacol. 10:529
Narahashi, T., Deguchi, T., Albuquerque, E. X. 1971. Effects of batrachotoxin on nerve membrane potential and conductances.Nature New Biol. 229:221
Narahashi, T., Seyama, I. 1974. Mechanism of nerve membrane depolarization caused by grayanotoxin I.J. Physiol. (London) 242:471
Ohta, M., Narahashi, T., Keeler, R. F. 1973. Effects of veratrum alkaloids on membrane potential and conductance of squid and crayfish giant axons.J. Pharmacol. Exp. Ther. 184:143
Robinson, R. A., Stokes, R. H. 1965. Electrolyte Solutions. (2nd ed.) Butterworth, London
Scudder, H. 1914. The electrical conductivity and ionization constants of organic compounds. D. Van Nostrand, Princeton
Seyama, I., Narahashi, T. 1973. Increase in sodium permeability of squid axon membranes by α-dihydrograyanotoxin IL.J. Pharmacol. Exp. Ther. 184:299
Seyama, I., Narahashi, T. 1976. Sodium conductance kinetics of squid axon membranes poisoned by grayanotoxin I.Biophys. J. 16 (2):187a
Shanes, A. M., Berman, M. D. 1955. Kinetics of ion movement in the squid giant axon.J. Gen. Physiol. 39:279
Ulbricht, W. 1969a. The effect of veratridine on excitable membranes of nerve and muscle.Ergeb. Physiol. 61:17
Ulbricht, W. 1969b. Effect of temperature on the slowly changing sodium permeability of veratrinized nodes of Ranvier.Pflügers Arch. Gesamte Physiol. 311:73
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Hironaka, T., Narahashi, T. Cation permeability ratios of sodium channels in normal and grayanotoxin-treated squid axon membranes. J. Membrain Biol. 31, 359–381 (1977). https://doi.org/10.1007/BF01869413
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DOI: https://doi.org/10.1007/BF01869413