Summary
A model is presented for “anomalous rectification” based upon electrical measurements on the egg cell membrane of the starfish. The objective is to postulate a plausible molecular mechanism which yields an expression for the conductance similar to that deduced empirically by Hagiwara and Takahashi (1974), i.e.,
whereB, ΔV h andv are constant,c K is the external K+ concentration, and ΔV(=V−V 0) is the displacement of the membrane potential from its resting value. It is shown that a similar dependence of the conductance on ΔV is expected for a particular class of models in which the K+ ions are also implicated in “gating”. To give a specific example, we consider the case in which the formation of ion-permeable pores requires a voltage-induced orientation of membrane-bound, electrically-charged groups and subsequent complexation of these groups with the external cations. Furthermore, the proportionality betweenG K andc 2/K1 , when the internal K+ concentration is constant, is accounted for by conventional descriptions of the ionic fluxes using Eyring's rate reaction theory. In terms of the present model,B and ΔV h are explicit functions of the internal K+ concentrations and are thus constant only as long as this is unvaried. The particular value ofv required to fit the data (v≃8.4 mV) is rationalized by the assumption that each of the orientable groups carries three negative elementary charges. In addition, the predictions of the present model are compared with those deduced from an alternative viewpoint, which is related to Armstrong's “blocking particle hypothesis”, in that the probability for opening and closing of the pore is assumed to depend on whether the pore is occupied or empty. Differences and similarities between the two models, as well as ways to discriminate between them, are discussed.
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References
Adrian, R.H. 1964. The rubidium and potassium permeability of frog muscle membrane.J. Physiol. (London) 175:134
Adrian, R.H. 1969. Rectification in muscle membrane.Proc. Biophys. Mol. Biol. 19:339
Adrian, R.H., Chandler, W.K., Hodgkin, A.L. 1970. Slow changes in potassium permeability in skeletal muscle.J. Physiol. (London) 208:645
Adrian, R.H., Freygang, W.H. 1962a. Potassium and chloride conductance of frog muscle membrane.J. Physiol. (London) 163:61
Adrian, R.H., Freygang, W.H. 1962b. Potassium conductance of frog muscle membrane under controlled voltage.J. Physiol. (London) 163:104
Almers, W. 1971. The Potassium Permeability of Frog Muscle Membrane. Ph.D. Thesis. University of Rochester, Rochester
Almers, W. 1972. Potassium conductance changes in skeletal muscle and the potassium concentration in the transverse tubules.J. Physiol. (London) 225:33
Armstrong, C.M. 1975. K pores of nerve and muscle membranes.In: Membranes—A Series of Advances. Vol. 3, pp. 325–358. G. Eisenman, editor. Marcel Dekker. New York
Baumann, G., Mueller, P. 1974. A molecular model of membrane excitability.J. Supramol. Struct. 2:538
Boheim, G. 1974. Statistical analysis of alamethicin channels in black lipid membranes.J. Membrane Biol. 19:277
Boheim, G., Kolb, H.-A. 1978. Analysis of the multi-pore system of alamethicin in a lipid membrane. I. Voltage-jump current-relaxation measurements.J. Membrane Biol. 38:99
Gordon, L.G.M., Haydon, D.A. 1975. Potential-dependent conductances in lipid membranes containing alamethicin.Phil. Trans. R. Soc. Lond. B. 270:433
Hagiwara, S., Miyazaki, S., Krasne, S., Ciani, S. 1977. Anomalous permeabilities of the egg cell membrane of a starfish in K+-Tl+ mixtures.J. Gen. Physiol. 70:269
Hagiwara, S., Miyazaki, S., Rosenthal, P. 1976. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish.J. Gen. Physiol. 67:621
Hagiwara, S., Takahashi, K. 1974. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell.J. Membrane Biol. 18:61
Hodgkin, A.L., Horowicz, P. 1959. The influence of potassium and chloride ions on the membrane potentials of single muscle fibers.J. Physiol. (London) 148:127
Horowicz, P., Gage, P.W., Eisenberg, R.S. 1968. The role of electro-chemical gradient in determining potassium fluxes in frog striated muscle.J. Gen. Physiol. 51:193
Katz, B. 1949. Les contance électriques de la membrane du muscle.Arch. Sci. Physiol. 3:285
Kolb, H.-A., Boheim, G. 1978. Analysis of the multi-pore system of alamethicin in a lipid membrane. I. Autocorrelation analysis and power spectral density.J. Membrane Biol. 38:151
Miyazaki, S., Ohmori, H., Sasaki, S. 1975. Potassium rectification of starfish oocyte membrane and their changes during oocyte maturation.J. Physiol. (London) 246:55
Miyazaki, S., Takahashi, K., Tsuda, K., Yoshii, M. 1974. Analysis of nonlinearity observed in the current-voltage relation of the tunicate embryo.J. Physiol. (London) 238:55
Nakajima, S., Iwasaki, S., Obata, K. 1962. Delayed rectification and anomalous rectification in frog's skeletal muscle membrane.J. Gen. Physiol. 46:97
Nakamura, Y., Nakajima, S., Grundfest, H. 1965. Analysis of spike electrogenesis and depolarizing K inactivation in electroplaques ofElectrophorus electricus, L.J. Gen. Physiol. 49:321
Ohmori, H. 1978. Inactivation kinetics and steady state current noise in the anomalous rectifier of tunicate egg cell membranes.J. Physiol. (London) (in press)
Stark, G., Ketterer, B., Benz, R., Läuger, P. 1971. The rate constants of valinomycinmediated ion transport through thin lipid membranes.Biophys. J. 11:981
Takahashi, K., Miyazaki, S., Kidakoro, Y. 1971. Development of excitability in embryonic muscle cell membranes in certain tunicates.Science 171:415
Takahashi, K., Yoshii, M. 1978. Effects of internal free Ca upon the Na and Ca channels in the tunicate egg analyzed by the internal perfusion technique.J. Physiol. (London) (in press)
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Ciani, S., Krasne, S., Miyazaki, S. et al. A model for anomalous rectification: Electrochemical-potential-dependent gating of membrane channels. J. Membrain Biol. 44, 103–134 (1978). https://doi.org/10.1007/BF01976035
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DOI: https://doi.org/10.1007/BF01976035