Summary
The slow inward current carried by Na+ through potential-dependent calcium channels in conditions when divalent cations were removed from the extracellular solution by EDTA has been investigated on isolated internally perfused neurons of the snailHelix pomatia. The calcium channels also acquire the capability to pass monovalent cations if other calcium-binding substances are added to the extracellular solution. Based on these facts the conclusion is made that the immediate reason for the modification of the channel selectivity is the absence of divalent cations in the extracellular medium. All potential-dependent characteristics of the modified calcium channel are shifted by 60 to 70 mV in the hyperpolarizing direction compared with those of the original calcium channel. The series of relative permeabilities for modified calcium channels towards monovalent cations (\(P_{Na^ + } :P_{Li^ + } :P_{N_2 H_5 ^ + } :P_{NH_3 OH^ + }\)=1.0∶0.8∶0.55∶0.21) is close to that of common “fast” sodium channels (\(P_{Na^ + } :P_{Li^ + } :P_{N_2 H_5 ^ + } :P_{NH_3 OH^ + }\)=1.0∶1.04∶0.44∶0.21). The induced sodium current decreases immediately when the concentration of divalent cations in the extracellular solution is elevated. This decrease is not potential dependent and can be approximated by Langmuir's isotherm with dissociation constants pKCa∶pKSr∶pKBa∶pKMg=6.6∶5.5∶4.8∶4.2. The conclusion is drawn that the calcium channels in the somatic membrane have two ion-selecting filters with different functions —an external one consisting, probably, of several carboxylic groups which bind divalent cations in a highly specific manner and determine the impermeability of the channel to monovalent cations in physiological conditions, and the channel ion-selecting filter including a single carboxylic group normally determining the channel selectivity for different divalent cations.
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Akaike, N., Lee, K.S., Brown, A.M. 1978. The calcium current ofHelix neuron.J. Gen. Physiol. 71:509–531
Butler, J.N. 1964. Ionic Equilibrium (A Mathematical Approach). Reading, Massachusetts
Curtis, B.A., Prosser, C.L. 1977. Calcium and cat intestinal smooth muscle.In. Excitation-Contraction Coupling in Smooth Muscle. R. Casteels et al., edition. pp. 123–129.
Doroshenko, P.A., Kostyuk, P.G., Martynyuk, A.E. 1982. Intracellular metabolism of adenosine 3′,5′-cyclic monophosphate and calcium inward current in perfused neurones ofHelix pomatia.Neuroscience 7:2125–2134
Hille, B. 1975. Ionic selectivity of Na and K channels of nerve membranes.In: Membranes. A Series of Advances. G. Eisenman, editor. Vol. 3, pp. 255–323. Marcel Dekker, New York
Kostyuk, P.G. 1981. Calcium channels in the neuronal membrane.Biochim. Biophys. Acta 650:128–150
Kostyuk, P.G., Krishtal, O.A. 1977a. Separation of sodium and calcium currents in the somatic membrane of mollusc neurons.J. Physiol. (London) 270:545–568
Kostyuk, P.G., Krishtal, O.A. 1977b. Effects of calcium and calcium-chelating agents on the inward and outward currents in the membrane of mollusc neurons.J. Physiol. (London) 270:569–580
Kostyuk, P.G., Krishtal, O.A., Doroshenko, P.A. 1974. Calcium currents in snail neurons. Identification of calcium currents.Pfluegers Arch. 348:83–93
Kostyuk, P.G., Krishtal, O.A., Pidoplichko, V.I. 1981. Intracellular perfusion.J. Neurosci. Methods 4:201–210
Kostyuk, P.G., Mironov, S.L., Doroshenko, P.A., Ponomaryov, V.N. 1982b. Surface charges on the outer side of mollusc neuron membrane.J. Membrane Biol. 70:171–179
Krishtal, O.A. 1976. Calcium in biological systems.Coord. Chem. Rev. 18:29–125
Krishtal, O.A. 1976. Blocking effect of cadmium ions on a calcium invward current in a nerve cell membrane.Dokl. Akad. Nauk SSSR 231:1003–1005
Krishtal, O.A. 1978. Modification of Ca channels in nerve cell membrane using EGTA.Dokl. Akad. Nauk SSSR 238:482–485
Martell, A.E., Smith, R.M. 1977. Critical Stability Constants. Academic Press, New York
Mironov, S.L. 1983. The comparison of the selective filters of sodium and calcium channels in excitable membrane.Dokl. Akad. Nauk SSSR 268:731–735
Palade, P.T., Almers, W. 1978. Slow Na+ and Ca2+ currents across the membrane of frog skeletal muscle fibres.Biophys. J. 21:168a
Yamamoto, D., Washio, H. 1979. Permeation of sodium through calcium channels of an insect muscle membrane.Can. J. Physiol. Pharmacol. 57:220–223
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Kostyuk, P.G., Mironov, S.L. & Shuba, Y.M. Two ion-selecting filters in the calcium channel of the somatic membrane of mollusc neurons. J. Membrain Biol. 76, 83–93 (1983). https://doi.org/10.1007/BF01871455
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DOI: https://doi.org/10.1007/BF01871455