Summary
We have studied the hyperpolarizing, electrogenic pump located on the apical membrane of the retinal pigment epithelium (RPE) in anin vitro preparation of bullfrog RPE-choroid. Changes in RPE [K+] i alter the current produced by this pump. Increasing [K+] o in the solution perfusing thebasal membrane increases RPE [K+] i (measured with a K+-specific microelectrode), and also depolarizes theapical membrane. This depolarization is due to a decrease in electrogenic pump current flowing across the apical membrane resistance, since it is abolished when the pump is inhibited by apical ouabain, by cooling the tissue, or by 0mm [K+] o outside the apical membrane. Removal of Cl− from the solution perfusing the basal membrane abolishes the K+-evoked apical depolarization by preventing the entry of K+ (as KCl) into the cell. We conclude that the increase in [K+] i causes the decrease in pump current. This result is consistent with the finding that [K+] i is a competitive inhibitor of the Na+−K+ pump in red blood cells.
It is possible that the light-evoked changes in [K+] o in the distal retina could alter RPE [K+] i , and thus could affect the pump from both sides of the apical membrane. Any change in pump current is likely to influence retinal function, since this pump helps to determine the composition of the photoreceptor extracellular space.
Similar content being viewed by others
References
Blostein, R., Chu, L. 1977. Sidedness of (sodium, potassium)-adenosine triphosphatase of inside-out red cell membrane vesicles.J. Biol. Chem. 252:3035
Bodemann, H.H., Hoffman, J.F. 1976. Side-dependent effects of internal versus external Na and K on ouabain binding to reconstituted human red blood cell ghosts.J. Gen. Physiol. 67:497
Brown, K.T., Flaming, D.G. 1975. Instrumentation and technique for beveling fine micropipette electrodes.Brain Res. 86:172
Garay, R.P., Garrahan, P.J. 1973. The interaction of sodium and potassium with the sodium pump in red cells.J. Physiol. (London) 231:297
Glynn, I.M. 1962. Activation of adenosinetriphosphatase activity in a cell membrane by external potassium and internal sodium.J. Physiol. (London) 160:18p
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
Kimura, G., Fujimoto, M. 1977. Estimation of the physical state of potassium in frog bladder cells by ion exchanger microelectrode.Jpn. J. Physiol. 27:291
Knight, A.B., Welt, L.G. 1974. Intracellular potassium: A determinant of the sodiumpotassium pump rate.J. Gen. Physiol. 63:351
Miller, S.S., Steinberg, R.H. 1977a. Passive ionic properties of frog retinal pigment epithelium.J. Membrane Biol. 36:337
Miller, S.S., Steinberg, R.H. 1977b. Active transport of ions across frog retinal pigment epithelium.Exp. Eye Res. 25:235
Miller, S.S., Steinberg, R.H., Oakley, B., II. 1978. The electrogenic sodium pump of the frog retinal pigment epithelium.J. Membrane Biol. 44:259
Neher, E., Lux, H.D. 1973. Rapid changes of potassium concentration at the outer surface of exposed single neurons during membrane current flow.J. Gen. Physiol. 61:385
Oakley, B., II. 1977. Potassium and the photoreceptor-dependent pigment epithelial hyperpolarization.J. Gen Physiol. 70:405
Oakley, B., II., Green, D.G. 1976. Correlation of light-induced changes in retinal extracellular potassium concentration withc-wave of the electroretinogram.J. Neurophysiol. 39:1117
Oakley, B., II., Steinberg, R.H., Miller, S.S., Nilsson, S.E. 1977. Thein vitro frog pigment epithelial cell hyperpolarization in response to light.Invest. Ophthalmol. 16:771
Robinson, R.A., Stokes, R.H. 1968. Electrolyte Solutions. (2nd Ed. revised.) Butterworths, London
Schwartz, A., Lindenmayer, G.E., Allen, J.C. 1975. The sodium-potassium adenosine triphosphatase: Pharmacological, physiological and biochemical aspects.Pharmacol. Rev. 27:3
Simons, T.J.B. 1974. Potassium: potassium exchange catalysed by the sodium pump in human red cells.J. Physiol. (London) 237:123
Skou, J.C. 1975. The (Na++K+) activated enzyme system and its relationship to transport of sodium and potassium.Q. Rev. Biophys. 7:401
Walker, J.L., Jr. 1971. Ion specific liquid ion exchanger microelectrodes.Anal. Chem. 43:89A
Watlington, C.O., Jessee, F., Jr. 1975. Net Cl− flux in short-circuited skin ofRana pipiens: Ouabain sensitivity and Na+−K+ dependence.Biochim. Biophys. Acta 382:204
Watlington, C.O., Jessee, S.D., Baldwin, G. 1977. Ouabain, acetazolamide, and Cl− flux in isolated frog skin: Evidence for two distinct active Cl− transport mechanisms.Am. J. Physiol. 232:F550
Wise, W.M., Kurey, M.J., Baum, G. 1970. Direct potentiometric measurement of potassium in blood serum with liquid ion-exchange electrode.Clin. Chem. 16:103
Wright, E.M. 1978. Anion transport by choroid plexus.In: Membrane Transport Processes. Vol. I. J.F. Hoffman, editor. Raven Press, New York
Wright, F.S., McDougal, W.S. 1972. Potassium-specific ion-exchanger microelectrodes to measure K+ activity in the renal distal tubule.Yale J. Biol. Med. 45:373
Zeuthen, T., Hiam, R.C., Silver, I.A. 1974. Microelectrode recording of ion activity in brain.In: Ion-Selective Microelectrodes. pp. 145–156. H.J. Berman and N.C. Hebert, editors. Plenum Press, New York
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Oakley, B., Miller, S.S. & Steinberg, R.H. Effect of intracellular potassium upon the electrogenic pump of frog retinal pigment epithelium. J. Membrain Biol. 44, 281–307 (1978). https://doi.org/10.1007/BF01944225
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01944225