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. 1969 Feb;200(2):459–496. doi: 10.1113/jphysiol.1969.sp008703

The ouabain-sensitive fluxes of sodium and potassium in squid giant axons

P F Baker, M P Blaustein, R D Keynes, Jacqueline Manil, T I Shaw, R A Steinhardt
PMCID: PMC1350477  PMID: 5812424

Abstract

1. Fifty to ninety per cent of the Na efflux from axons of Loligo forbesi is inhibited by ouabain. The properties of the ouabain-sensitive component of the Na efflux are different from those of the ouabain-insensitive component.

2. In unpoisoned axons with an average Na content of 75 m-mole/kg axoplasm the bulk of the ouabain-sensitive Na efflux is dependent on external K.

3. In the presence of 460 mM Na in the external medium, raising the external K concentration from 0 to 100 mM increases the ouabain-sensitive Na efflux along a sigmoid curve which shows signs of saturating at high K concentrations.

4. The curve relating ouabain-sensitive K influx to external K concentration is similar in shape to that for the ouabain-sensitive Na efflux. At all K concentrations examined the ouabain-sensitive K influx was less than the ouabain-sensitive Na efflux.

5. Potassium-free sea water acts rapidly in reducing the Na efflux. There is no appreciable difference between the rates of action of K-free sea water on the Na pump and Na-free sea water on the action potential.

6. Caesium and Rb can replace external K in activating the ouabain-sensitive Na efflux. Both the affinity and maximum rate of the Na efflux mechanism are lower when Cs replaces K as the activating cation.

7. Isosmotic replacement of external Na by either choline or dextrose, but not Li, increases the affinity of the ouabain-sensitive Na efflux mechanism for external K without appreciably affecting the maximum rate of pumping. External Li behaves like external Na and exerts an inhibitory action on the Na efflux.

8. There is a large ouabain-sensitive Na efflux into K-free choline or dextrose sea waters. Addition of either Na or Li to the external medium reduces this efflux along a section of a rectangular hyperbola. The properties of this efflux suggest that there is a residual K concentration of up to 2 mM immediately external to the pumping sites in the axolemma.

9. Over the range of internal Na concentrations studied (16-140 m-mole/kg axoplasm) the ouabain-sensitive Na efflux increased linearly with Na concentration.

10. Tetrodotoxin (10-6 g/ml.) reduces the Na influx by about half, but does not affect the ouabain-sensitive Na efflux.

11. Isobutanol (1% v/v) reversibly decreases both the ouabain-sensitive and ouabain-insensitive components of the Na efflux.

12. Application of 2 mM cyanide to axons immersed in K-free sea water produces a transient rise in the Na efflux. This rise is not seen if ouabain is included in the sea water. The rise in efflux occurs at a time when the axons are partially poisoned and contain adenosine triphosphate (ATP) but no arginine phosphate (ArgP). A similar, but maintained rise can be obtained after application of dinitrophenol (DNP) at pH 8·0. The increased Na efflux in these partially poisoned axons is also inhibited by ouabain.

13. Under conditions of partial-poisoning by alkaline DNP, there is a ouabain-sensitive Na influx from K-free sea water. The ouabain-sensitive Na influx is of similar size to the ouabain-sensitive Na efflux. These results show that in partially-poisoned axons immersed in K-free sea water intracellular Na exchanges with extracellular Na in a one-for-one manner by a ouabain-sensitive route. External Li cannot replace external Na in maintaining this process.

14. Axons partially poisoned with alkaline DNP are not insensitive to external K. In the absence of external Na their response to external K is essentially the same as that seen in unpoisoned axons.

15. Possible mechanisms are discussed for the appearance of Na-Na exchange in partially poisoned axons.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BAKER P. F. AN EFFLUX OF NINHYDRIN-POSITIVE MATERIAL ASSOCIATED WITH THE OPERATION OF THE NA+ PUMP IN INTACT CRAB NERVE IMMERSED IN NA+-FREE SOLUTIONS. Biochim Biophys Acta. 1964 Sep 25;88:458–460. doi: 10.1016/0926-6577(64)90208-6. [DOI] [PubMed] [Google Scholar]
  2. Baker P. F., Blaustein M. P., Hodgkin A. L., Steinhardt R. A. The influence of calcium on sodium efflux in squid axons. J Physiol. 1969 Feb;200(2):431–458. doi: 10.1113/jphysiol.1969.sp008702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baker P. F., Connelly C. M. Some properties of the external activation site of the sodium pump in crab nerve. J Physiol. 1966 Jul;185(2):270–297. doi: 10.1113/jphysiol.1966.sp007987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baker P. F., Foster R. G., Gilbert D. S., Shaw T. I. Sodium transport and perfused axons. Biochim Biophys Acta. 1968 Dec 10;163(4):560–562. doi: 10.1016/0005-2736(68)90086-2. [DOI] [PubMed] [Google Scholar]
  5. Baker P. F., Manil J. The rates of action of K+ and ouabain on the sodium pump in squid axons. Biochim Biophys Acta. 1968 Mar 1;150(2):328–330. doi: 10.1016/0005-2736(68)90181-8. [DOI] [PubMed] [Google Scholar]
  6. Baker P. F. Phosphorus metabolism of intact crab nerve and its relation to the active transport of ions. J Physiol. 1965 Sep;180(2):383–423. doi: 10.1113/jphysiol.1965.sp007709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Baker P. F. Recent experiments on the properties of the na efflux from squid axons. J Gen Physiol. 1968 May 1;51(5):172–179. [PMC free article] [PubMed] [Google Scholar]
  8. Baker P. F., Shaw T. I. A comparison of the phosphorus metabolism of intact squid nerve with that of the isolated axoplasm and sheath. J Physiol. 1965 Sep;180(2):424–438. doi: 10.1113/jphysiol.1965.sp007710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Blaustein M. P., Hodgkin A. L. The effect of cyanide on the efflux of calcium from squid axons. J Physiol. 1969 Feb;200(2):497–527. doi: 10.1113/jphysiol.1969.sp008704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brinley F. J., Jr, Mullins L. J. Sodium fluxes in internally dialyzed squid axons. J Gen Physiol. 1968 Aug;52(2):181–211. doi: 10.1085/jgp.52.2.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. CALDWELL P. C., HODGKIN A. L., KEYNES R. D., SHAW T. I. Partial inhibition of the active transport of cations in the giant axons of Loligo. J Physiol. 1960 Jul;152:591–600. doi: 10.1113/jphysiol.1960.sp006510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. CALDWELL P. C., HODGKIN A. L., KEYNES R. D., SHAW T. L. The effects of injecting 'energy-rich' phosphate compounds on the active transport of ions in the giant axons of Loligo. J Physiol. 1960 Jul;152:561–590. doi: 10.1113/jphysiol.1960.sp006509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. CALDWELL P. C. The phosphorus metabolism of squid axons and its relationship to the active transport of sodium. J Physiol. 1960 Jul;152:545–560. doi: 10.1113/jphysiol.1960.sp006508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Caldwell P. C. Factors governing movement and distribution of inorganic ions in nerve and muscle. Physiol Rev. 1968 Jan;48(1):1–64. doi: 10.1152/physrev.1968.48.1.1. [DOI] [PubMed] [Google Scholar]
  15. FRANKENHAEUSER B., HODGKIN A. L. The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol. 1956 Feb 28;131(2):341–376. doi: 10.1113/jphysiol.1956.sp005467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fahn S., Hurley M. R., Koval G. J., Albers R. W. Sodium-potassium-activated adenosine triphosphatase of Electrophorus electric organ. II. Effects of N-ethylmaleimide and other sulfhydryl reagents. J Biol Chem. 1966 Apr 25;241(8):1890–1895. [PubMed] [Google Scholar]
  17. Fahn S., Koval G. J., Albers R. W. Sodium-potassium-activated adenosine triphosphatase of Electrophorus electric organ. I. An associated sodium-activated transphosphorylation. J Biol Chem. 1966 Apr 25;241(8):1882–1889. [PubMed] [Google Scholar]
  18. GLYNN I. M. The action of cardiac glycosides on sodium and potassium movements in human red cells. J Physiol. 1957 Apr 3;136(1):148–173. doi: 10.1113/jphysiol.1957.sp005749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Garrahan P. J., Glynn I. M. Facftors affecting the relative magnitudes of the sodium:potassium and sodium:sodium exchanges catalysed by the sodium pump. J Physiol. 1967 Sep;192(1):189–216. doi: 10.1113/jphysiol.1967.sp008296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Garrahan P. J., Glynn I. M. The behaviour of the sodium pump in red cells in the absence of external potassium. J Physiol. 1967 Sep;192(1):159–174. doi: 10.1113/jphysiol.1967.sp008294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Garrahan P. J., Glynn I. M. The sensitivity of the sodium pump to external sodium. J Physiol. 1967 Sep;192(1):175–188. doi: 10.1113/jphysiol.1967.sp008295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Garrahan P. J., Glynn I. M. The stoicheiometry of the sodium pump. J Physiol. 1967 Sep;192(1):217–235. doi: 10.1113/jphysiol.1967.sp008297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. HODGKIN A. L., KEYNES R. D. Active transport of cations in giant axons from Sepia and Loligo. J Physiol. 1955 Apr 28;128(1):28–60. doi: 10.1113/jphysiol.1955.sp005290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. HODGKIN A. L., KEYNES R. D. Experiments on the injection of substances into squid giant axons by means of a microsyringe. J Physiol. 1956 Mar 28;131(3):592–616. doi: 10.1113/jphysiol.1956.sp005485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. HODGKIN A. L., KEYNES R. D. The potassium permeability of a giant nerve fibre. J Physiol. 1955 Apr 28;128(1):61–88. doi: 10.1113/jphysiol.1955.sp005291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. KEYNES R. D. SOME FURTHER OBSERVATIONS ON THE SODIUM EFFLUX IN FROG MUSCLE. J Physiol. 1965 May;178:305–325. doi: 10.1113/jphysiol.1965.sp007629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. KEYNES R. D., SWAN R. C. The effect of external sodium concentration on the sodium fluxes in frog skeletal muscle. J Physiol. 1959 Oct;147:591–625. doi: 10.1113/jphysiol.1959.sp006264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. KEYNES R. D., SWAN R. C. The permeability of frog muscle fibres to lithium ions. J Physiol. 1959 Oct;147:626–638. doi: 10.1113/jphysiol.1959.sp006265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kao C. Y. Tetrodotoxin, saxitoxin and their significance in the study of excitation phenomena. Pharmacol Rev. 1966 Jun;18(2):997–1049. [PubMed] [Google Scholar]
  31. Keynes R. D., Steinhardt R. A. The components of the sodium efflux in frog muscle. J Physiol. 1968 Oct;198(3):581–599. doi: 10.1113/jphysiol.1968.sp008627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. MAIZELS M., REMINGTON M. Cation exchanges of human erythrocytes. J Physiol. 1959 Mar 12;145(3):641–657. doi: 10.1113/jphysiol.1959.sp006168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. McConaghey P. D., Maizels M. Cation exchanges of lactose-treated human red cells. J Physiol. 1962 Aug;162(3):485–509. doi: 10.1113/jphysiol.1962.sp006946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mullins L. J., Brinley F. J., Jr Some factors influencing sodium extrusion by internally dialyzed squid axons. J Gen Physiol. 1967 Nov;50(10):2333–2355. doi: 10.1085/jgp.50.10.2333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. POST R. L., SEN A. K., ROSENTHAL A. S. A PHOSPHORYLATED INTERMEDIATE IN ADENOSINE TRIPHOSPHATE-DEPENDENT SODIUM AND POTASSIUM TRANSPORT ACROSS KIDNEY MEMBRANES. J Biol Chem. 1965 Mar;240:1437–1445. [PubMed] [Google Scholar]
  36. Priestland R. N., Whittam R. The influence of external sodium ions on the sodium pump in erythrocytes. Biochem J. 1968 Sep;109(3):369–374. doi: 10.1042/bj1090369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rang H. P., Ritchie J. M. On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol. 1968 May;196(1):183–221. doi: 10.1113/jphysiol.1968.sp008502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rang H. P., Ritchie J. M. The dependence on external cations of the oxygen consumption of mammalian non-myelinated fibres at rest and during activity. J Physiol. 1968 May;196(1):163–181. doi: 10.1113/jphysiol.1968.sp008501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sachs J. R., Welt L. G. The concentration dependence of active potassium transport in the human red blood cell. J Clin Invest. 1967 Jan;46(1):65–76. doi: 10.1172/JCI105512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sjodin R. A., Beaugé L. A. Coupling and selectivity of sodium and potassium transport in squid giant axons. J Gen Physiol. 1968 May 1;51(5):152–161. [PMC free article] [PubMed] [Google Scholar]
  41. Sjodin R. A., Beaugé L. A. The ion selectivity and concentration dependence of cation coupled active sodium transport in squid giant axons. Curr Mod Biol. 1967 May;1(2):105–115. doi: 10.1016/0303-2647(67)90022-6. [DOI] [PubMed] [Google Scholar]
  42. Stone A. J. A proposed model for the Na+ pump. Biochim Biophys Acta. 1968 Jun 11;150(4):578–586. doi: 10.1016/0005-2736(68)90047-3. [DOI] [PubMed] [Google Scholar]
  43. Whittam R., Ager M. E. Vectorial aspects of adenosine-triphosphatase activity in erythrocyte membranes. Biochem J. 1964 Nov;93(2):337–348. doi: 10.1042/bj0930337. [DOI] [PMC free article] [PubMed] [Google Scholar]

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