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«THE RUBIDIUM AND POTASSIUM PERMEABILITY OF FROG MUSCLE MEMBRANE BY R. H. ADRIAN From the Physiological Laboratory, University of Cambridge (Received ...»

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Lubin & Schneider (1957) and Bolingbroke, Harris & Sjodin (1961) report much faster replacement of potassium by rubidium. Some of the difference in rates can be accounted for by the high temperature coefficient of the replacement which was observed by both sets of authors. Lubin & Schneider used relatively low (5 and 10 mM) external rubidium concentrations. Bolingbroke et al. used solutions containing RbCl or RbHCO3, at both high and low concentrations. It is not always clear how far they were justified in ignoring net movements of RbCl, It seems probable that the differences in the rubidium-entry rate can be accounted for by the different conditions in which it has been observed. Although the rubidium conductance appears to be much less dependent on the membrane potential than the potassium conductance, it is possible that the rubidium permeability may be different under different circumstances.

The conclusion that rubidium interferes with the movement ofpotassium has been reached by a number of authors (Solomon, 1952; Sjodin, 1959, 1961; Bolingbroke et al. 1961). Solomon has studied the inward movement of potassium into red cells in the presence and absence of rubidium, and his conclusions probably apply to metabolically driven potassium movements. Sjodin (1961) is concerned mainly with inward cation movements in muscle, and he proposes a mechanism for the interaction of potassium, rubidium, and caesium. The ions are supposed to compete for a limited number of membrane sites, and the equations derived for the influxes of each cation under various circumstances are independent of membrane potential. Sjodin is fully aware that his model 'does not contain the means to handle cases in which the membrane potential has been altered by the passage of an electric current'. But since it seems likely that in many of his experiments there is an undetermined anion current, it is hardly safe to ignore the effects of membrane potential.

For muscle it is necessary to stress that a distinction must be made between the effects of removing external potassium and the effects of adding external rubidium. In circumstances where the internal potential is held less negative than the new potassium equilibrium potential, for instance, by an unchanged chloride potential, removing external potassium will, by itself, reduce the outward movement of potassium (Adrian, 1958, 1962). It appears that if the potential is such that there is an outward driving force on the potassium ion, substitution of external potassium R. H. ADRIAN 156 by sodium, lithium, choline, or rubidium reduces the efflux of 42K from a muscle. The efflux of potassium appears to depend on the presence of external potassium. The dependence is reminiscent of the exchangediffusion of sodium (Ussing, 1949; Keynes & Swan, 1959), but the reduction of the potassium efflux cannot be due to the type of mechanism postulated by Ussing because that mechanism cannot carry any current.

If the greater part of the efflux of 42K into a solution with a high potassium concentration were an exchange-diffusion efflux, which disappeared when the external potassium was removed, one would expect the electrical conductance, calculated from the measured efflux (G = MF2/RT), to be much greater than the measured conductance. The rate constant for the loss of 42K into a sulphate solution containing 140 m-equiv/l. of potassium is 0x13 min-' (unpublished experiment with W. K. Chandler). Making the usual assumptions about fibre diameter (80,t) and internal concentration (140 mM) the efflux is 63 p-mole/cm2/sec. In the absence of exchangediffusion and single-filing (Hodgkin & Keynes, 1955) an equilibrium flux of this magnitude leads to a calculated conductance of 2-5 x 10-4 mho/cm2.

Adrian & Freygang (1962b) meastired the conductance of fibres in a sulphate solution containing 100 m-equiv/l. of potassium. For very small currents the average conductance was 3-6 x 10-4 mho/cm2. The discrepancy between the measured conductance and the conductance predicted from the efflux is small, and if it is real it is in the direction produced by single-filing rather than exchange-diffusion.

In the experiment illustrated in Fig. 11, 10 m-equiv/l. Rb+ were added to the external solution without altering the external potassium concentration. The membrane potential was not altered by this addition, but the resistance to inward current, almost entirely an inward potassium movement, was more than doubled. Both the membrane potential and the external potassium concentration can affect the potassium conductance, but in this experiment neither was altered, and one must conclude that rubidium itself interferes with the movement of potassium.

Sjodin (1961) measured the 42K and 86Rb influx into muscles from 2-5 mm-K Ringer's solution and from a similar Rb-Ringer's solution. The potassium influx was 4X1 p-mole/cm2/sec and the rubidium influx was 1X9 p-mole/cm2/sec. The value of the rubidium influx, only half the potassium influx, is much greater than would be expected for the passive influx of rubidium on the basis of the experiments in Figs. 5 and 6. The discrepancy could be explained if a substantial part of both influxes was driven by an electrically neutral pump which did not discriminate strongly between potassium and rubidium. Several transport ATPases have been shown to. be activated by rubidium almost as well as by potassium (Skou, 1960; Aldridge, 1962).

Rb AND K IN MUSCLE 157 If the repolarization of the action potential depends on large outward potassium currents it follows that similar large outward movements of rubidium are possible. However, in circumstances where the conductance increase of delayed rectification is not produced, rubidium can only carry small currents in either direction though potassium can carry large inward currents. On the basis of the ability to discriminate between potassium and rubidium it seems clear that the mechanism responsible for the movement of potassium and rubidium during the action potential must differ from the mechanisms involved when the external potassium concentration is high or for inward currents when the external concentration is in the physiological range. This latter mechanism, which behaves like a valve for potassium ions, is remarkable for its ability to distinguish potassium from rubidium, and for distinguishing inward from outward potassium movement even in the absence of a potential difference or of a potassium concentration gradient across the membrane.





If the mechanisms for potassium movement differ, they need not be in the same membrane, though their differing is not evidence that the two potassium pathways are separate at more than molecular levels. Adrian & Freygang (1962a, b) have suggested a morphological basis for the separation of the two potassium pathways. They supposed that the potassium pathways used for the action potential were in the surface membrane, and that the T-system tubules of the endoplasmic reticulum were responsible for the valve-like potassium pathways. More recently Freygang and his co-workers have produced evidence which can be interpreted in terms of an accumulation of potassium in the T-system tubules after a train of impulses (Freygang, Goldstein & Hellam, 1964). If this is the case it would imply that the action potential mechanism for potassium exists in the wall of the T-system tubules, as well as, presumably, in the surface membrane of the fibre. Adrian (1964) has discussed some of the implications of separating two potassium pathways for hypotheses about the coupling of electrical events at the membrane and the initiation of contraction.

SUMMARY

1. Muscles have been prepared with 80-85 % of the internal potassium replaced by rubidium.

2. Provided the internal potential is more negative than about -80 mV, a Rb-containing muscle fibre in a Rb-Ringer's solution can conduct an action potential with a normal appearance, and when it does so it twitches.

3. The following evidence is consistent with the view that rubidium

does not pass through the channel responsible for anomalous rectification:

(a) When the concentrations of potassium on each side of the membrane R. H. ADRIAN 158 are nearly equal ([K] = 100 mM, [K1] = 140 mm), large inward currents can be carried by potassium, but only very small outward currents. With similar concentrations of rubidium on each side of the membrane only very small rubidium currents can be carried in either direction. With rubidium outside and potassium inside, the current carried by both ions is small.

With potassium outside and rubidium inside, large inward potassium currents are possible.

(b) When the external rubidium concentration is low (2.5 mM), hyperpolarizing a Rb-containing muscle fibre does not produce the voltage or time dependent conductance changes characteristic of a K-containing muscle fibre in a K-Ringer's solution. These conductance changes are also not produced by hyperpolarizing a K-containing muscle fibre in a RbRinger's solution.

4. Rubidium (10 mM) in the external solution interferes with the inward movement of potassium from a potassium concentration of 100 mm.

5. When potassium and rubidium are present potassium appears to be more permeable than rubidium, but the potassium permeability is substantially less than the potassium permeability in the absence of rubidium.

The expenses of the work described in this paper were met by grants from the Nuffield Foundation and the Medical Research Council. I am indebted to Dr R. D. Keynes for the use of apparatus at the Institute of Animal Physiology, Babraham, and to Dr Keynes and Professor A. L. Hodgkin for helpful discussion throughout the course of this work.

REFERENCES ADRIAN, R. H. (1958). The effects of membrane potential and external potassium concentration on the potassium permeability of muscle fibres. J. Phy8iol. 143, 59-60P.

ADRIAN, R. H. (1960). Potassium chloride movement and the membrane potential of frog muscle. J. Physiol. 151, 154-185.

ADRIAN, R. H. (1962). Movement of inorganic ions across the membrane of striated muscle.

Circulation, 26, 1214-1223.

ADRIAN, R. H. (1963). The replacement of potassium by rubidium in striated muscle fibres. J. Phy8iol. 169, 16-18P.

ADRIAN, R. H. (1964). Membrane properties of striated muscle and the initiation of contraction. In Cellular Function of Membrane Transport, ed. HOFFMAN, J. New York:

Prentice-Hall.

ADRIAN, R. H. & FREYGANG, W. H. (1962a). Potassium and chloride conductance of frog muscle membrane. J. Physiol. 163, 61-103.

ADRIAN, R. H. & FREYGANG, W. H. (1962b). Potassium conductance of frog muscle membrane under controlled voltage. J. Physiol. 163, 104-114.

ALDRIDGE, W. N. (1962). Adenosine triphosphatase in the microsomal fraction from rat brain. Biochem. J. 83, 527-533.

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. 164, 335-374.

BOLINGBROKE, VALERIE, HARRIS, E. J. & SJODIN, R. A. (1961). Rubidium and caesium entry, and cation interaction in frog skeletal muscle. J. Physiol. 157, 289-305.

DESMEDT, J. E. (1953). Electrical activity and intracellular sodium concentration in frog muscle. J. Physiol. 121, 191-205.

FENG, T. P. & Lru, Y. M. (1949). The concentration-effect relationship in the depolarization of amphibian nerve by potasium and other agents. J. cell. comnp. Physiol. 34, 33-42.

Rb AND K IN MUSCLE 159 FREYGAANG, W. H., GOLDSTEIN, D. A. & HELLAM, D. C. (1964). The after-potential that follows trains of impulses in frog muscle. J. gen. Phy8iol. 47, 929-952.

HODGKIN, A. L. & HOROWICZ, P. (1959). The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J. Phy8iol. 148, 127-160.

HODGKIN, A. L. & KEYNES, R. D. (1955). The potassium permeability of a giant nerve fibre. J. Physiol. 128, 61-88.

HUTTER, 0. F. & NOBLE, D. (1960). The chloride conductance of frog skeletal muscle.

J. Physiol. 151, 89-102.

KATZ, B. (1949). Les constantes electriques de la membrane du muscle. Arch. Sci. physiol. 3, 285-300.

KEYNES, R. D. & SWAN, R. C. (1959). The effect of external sodium concentration on the sodium fluxes in frog skeletal muscle. J. Physiol. 147, 591-625.

LUBIN, M. & SCHNEIDER, P. B. (1957). The exchange of potassium for caesium and rubidium in frog muscle. J. Physiol. 138, 140-155.

NASTUK, W. & HODGKIN, A. L. (1950). The electrical activity of single muscle fibres. J. cell.

comp. Physiol. 35, 39-73.

RELMAN, A. S., LAMBIE, ANNE T., BURROWS, B. A. & Roy, ARLENE M. (1957). Cation accumulation by muscle tissue: the displacement of potassium by rubidium and caesium in the living animal. J. clin. Invest. 36, 1249-1256.

SANDOW, A. & MANDEL, H. (1951). Effects of potassium and rubidium on the resting potential of muscle. J. cell. comp. Physiol. 38, 271-291.

SJODIN, R. A. (1959). Rubidium and caesium fluxes in muscle as related to the membrane potential. J. gen. Physiol. 42, 983-1003.

SJODIN, R. A. (1961). Some cation interactions in muscle. J. gen. Physiol. 44, 929-962.

SKOU, J. C. (1960). Further investigations on a Mg++ + Na+-activated adeninetriphosphatase, possibly related to the active, lined transport of Na+ and K+ across the nerve membrane. Biochim. biophys. Acta, 42, 6-23.

SOLOMON, A. K. (1952). The permeability of the human erythrocyte to sodium and potassium. J. gen. Physiol. 36, 57-110.

USSING, H. H. (1949). Transport of ions across cellular membranes. Physiol. Rev. 29, 127- 155.

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