Summary
Oscillation and activated hyperpolarizing responses induced by electrical stimuli (H.A. responses) were studied in large nondividing L cells (giant L cells) under a variety of ionic conditions. When Cl− in the bathing fluid was partially replaced with SO 2−4 at fixed external Na+ and K+ concentrations, the membrane potential depolarized transiently, but recovered to the original potential level after about 10 min. Under such a steady state in a low-Cl− medium, the amplitudes of oscillations and H.A. responses remained almost identical with those in the control medium. On exposure to a low-Na+ medium, both membrane potentials in the resting and hyperpolarized states were slightly hyperpolarized, but the pattern and the amplitude of oscillations and H.A. responses remained much the same. Changes in external K+ concentrations remarkably affected the amplitudes of oscillations and H.A. responses: the amplitudes decreased with increases in external K+ concentration. Calculation of the changes in K+, Na+ and Cl− conductances during oscillations and H.A. responses under these various ionic conditions showed that the change in K+ conductance is the only factor responsible for the oscillation and the H.A. response. The reversal potential for the potential oscillation is about −94 mV under normal conditions, this value being quite close to that of the equilibrium potential of K+. The reversal potentials in various external K+ concentrations satisfied the Nernst equation for a K+ electrode. Valinomycin induced remarkable hyperpolarization of the resting potential, resulting in an inhibition of oscillations. The level of valinomycin-induced hyperpolarization of the resting potential required to inhibit H.A. responses was the same as that of the peak potentials of the oscillation and H.A. response. In the light of these observations, it is concluded that the spontaneous potential oscillation and the H.A. response are caused solely by increase in the K+ conductance of the cell membrane.
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References
Evans, M.H. 1972. Tetrodotoxin, saxitoxin, and related substances: Their applications in neurobiology.Int. Rev. Neurobiol. 15:83
Gallin, E.K., Wiederhold, M.L., Lipsky, P.E., Rosenthal, A.S. 1975. Spontaneous and induced membrane hyperpolarizations in macrophages.J. Cell. Physiol. 86:653
Hagiwara, S., Saito, N. 1959. Voltage-current relations in nerve cell membrane ofOnchidium verruculatum.J. Physiol. (London) 148:161
Harris, E.J., Pressman, B.C. 1967. Obligate cation exchanges in red cells.Nature (London) 216:918
Hille, S. 1967. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion.J. Gen. Physiol. 50:1287
Hodgkin, A.L., Horowicz, P. 1959. The influence of potassium and chloride ions on the membrane potential of single muscle fibres.J. Physiol. (London) 148:127
Hoffman, J.F., Laris, P.C. 1974. Determinations of membrane potentials in human andAmphiuma red blood cells by means of a fluorescent probe.J. Physiol. (London) 239:519
Koppenhöfer, E., Weymann, D. 1965. Voltage clamp am bespülten Ranvierschen Schnürring.Arch. Ges. Physiol. 283:R7
Lamb, J.F., MacKinnon, M.G.A. 1971. The membrane potential and permeabilities of the L cell membrane to Na, K and chloride.J. Physiol. (London) 213:683
Lev, A.A., Buzhinsky, E.P. 1967. Cation specificity of the model bimolecular phospholipid membranes with incorporated valinomycin.Cytology (USSR) 9:102
Levinson, C. 1967. Effect of valinomycin on net sodium and potassium transport in Ehrlich ascites tumour cells.Nature (London) 216:74
Mueller, P., Rudin, D.O. 1967. Development of K+−Na+ discrimination in experimental bimolecular lipid membranes by macrocyclic antibiotics.Biochem. Biophys. Res. Commun. 26:398
Narahashi, T., Deguchi, T., Urakawa, N., Ohkubo, Y. 1960. Stabilization and rectification of muscle fiber membrane by tetrodotoxin.Am. J. Physiol. 198:934
Nelson, P.G., Peacock, J., Minna, J. 1972. An active electrical response in fibroblasts.J. Gen. Physiol. 60:58
Okada, Y., Doida, Y., Roy, G., Tsuchiya, W., Inouye, K., Inouye, A. 1977. Oscillations of membrane potential in L cells. I. Basic characteristics.J. Membrane Biol. 35:319
Okada, Y., Irimajiri, A., Inouye, A. 1976. Permeability properties and intracellular ion concentrations of epithelial cells in rat duodenum.Biochim. Biophys. Acta 436:15
Pressman, B.C., Harris, E.J., Jagger, W.S., Johnson, J.H. 1967. Antibiotic-mediated transport of alkali ions across lipid barriers.Proc. Nat. Acad. Sci. USA 58:1949
Schmidt, H., Stämpfli, R. 1966. Die Wirkung von Tetraäthylammoniumchlorid auf den einzelnen Ranvierschen Schnürring.Arch. Ges. Physiol. 287:311
Schneider, J.A., Sperelakis, N. 1974. Valinomycin blockade of slow channels in guinea pig hearts perfused with elevated K+ and isoproterenol.Eur. J. Pharmacol. 27:349
Tosteson, D.C., Cook, P., Andreoli, T., Tiefenberg, M. 1967. The effect of valinomycin on potassium and sodium permeability of HK and LK sheep red cells.J. Gen. Physiol. 50:2513
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Okada, Y., Roy, G., Wakoh, T. et al. Oscillations of membrane potential in L cells. J. Membrain Biol. 35, 337–350 (1977). https://doi.org/10.1007/BF01869958
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DOI: https://doi.org/10.1007/BF01869958