Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1979 Jun 1;73(6):801–818. doi: 10.1085/jgp.73.6.801

Chloride and sodium influx: a coupled uptake mechanism in the squid giant axon

PMCID: PMC2215202  PMID: 479816

Abstract

The squid giant axon was internally dialyzed while the unidirectional fluxes of either Cl or Na were measured. The effects of varying the internal or external concentration of either Na or Cl were studied. Chloride influx was directly proportional to the external Na concentration whereas Cl efflux was unaffected by changes of the external Na concentration between 0 and 425 mM. Neither Cl influx nor efflux were affected by changes of internal Na concentration over the range of 8-158 mM. After ouabain and TTX treatment a portion of the remaining Na influx was directly dependent on the extracellular Cl concentration. Furthermore, when the internal Cl concentration was increased from 0 to 150 mM, the influxes of Cl and Na were decreased by 14 and 11 pmol/cm2.s, respectively. The influx of both ions could be substantially reduced when the axon was depleted of ATP. The influxes of both ions were inhibited by furosemide but unaffected by ouabain. It is concluded that the squid axolemma has an ATP-dependent coupled Na-Cl co-transport uptake mechanism.

Full Text

The Full Text of this article is available as a PDF (932.9 KB).

Selected References

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

  1. BRINLEY F. J., Jr, MULLINS L. J. ION FLUXES AND TRANSFERENCE NUMBER IN SQUID AXONS. J Neurophysiol. 1965 May;28:526–544. doi: 10.1152/jn.1965.28.3.526. [DOI] [PubMed] [Google Scholar]
  2. Baker P. F., Blaustein M. P., Keynes R. D., Manil J., Shaw T. I., Steinhardt R. A. The ouabain-sensitive fluxes of sodium and potassium in squid giant axons. J Physiol. 1969 Feb;200(2):459–496. doi: 10.1113/jphysiol.1969.sp008703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blaustein M. P., Santiago E. M. Effects of internal and external cations and of ATP on sodium-calcium and calcium-calcium exchange in squid axons. Biophys J. 1977 Oct;20(1):79–111. doi: 10.1016/S0006-3495(77)85538-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boron W. F., Russell J. M., Brodwick M. S., Keifer D. W., Roos A. Influence of cyclic AMP on intracellular pH regulation and chloride fluxes in barnacle muscle fibers. Nature. 1978 Nov 30;276(5687):511–513. doi: 10.1038/276511a0. [DOI] [PubMed] [Google Scholar]
  5. Brazy P. C., Gunn R. B. Furosemide inhibition of chloride transport in human red blood cells. J Gen Physiol. 1976 Dec;68(6):583–599. doi: 10.1085/jgp.68.6.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brinley F. J., Jr, Mullins L. J. Sodium extrusion by internally dialyzed squid axons. J Gen Physiol. 1967 Nov;50(10):2303–2331. doi: 10.1085/jgp.50.10.2303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Burg M., Stoner L., Cardinal J., Green N. Furosemide effect on isolated perfused tubules. Am J Physiol. 1973 Jul;225(1):119–124. doi: 10.1152/ajplegacy.1973.225.1.119. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Candia O. A. Short-circuit current related to active transport of chloride in frog cornea: effects of furosemide and ethacrynic acid. Biochim Biophys Acta. 1973 Apr 16;298(4):1011–1014. doi: 10.1016/0005-2736(73)90407-0. [DOI] [PubMed] [Google Scholar]
  11. Crane R. K. The gradient hypothesis and other models of carrier-mediated active transport. Rev Physiol Biochem Pharmacol. 1977;78:99–159. doi: 10.1007/BFb0027722. [DOI] [PubMed] [Google Scholar]
  12. DEFFNER G. G. The dialyzable free organic constituents of squid blood; a comparison with nerve axoplasm. Biochim Biophys Acta. 1961 Feb 18;47:378–388. doi: 10.1016/0006-3002(61)90298-0. [DOI] [PubMed] [Google Scholar]
  13. De Weer P. Effects of intracellular adenosine-5'-diphosphate and orthophosphate on the sensitivity of sodium efflux from squid axon to external sodium and potassium. J Gen Physiol. 1970 Nov;56(5):583–620. doi: 10.1085/jgp.56.5.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dipolo R. Effect of ATP on the calcium efflux in dialyzed squid giant axons. J Gen Physiol. 1974 Oct;64(4):503–517. doi: 10.1085/jgp.64.4.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. KEYNES R. D. CHLORIDE IN THE SQUID GIANT AXON. J Physiol. 1963 Dec;169:690–705. doi: 10.1113/jphysiol.1963.sp007289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Karnaky K. J., Jr, Degnan K. J., Zadunaisky J. A. Chloride transport across isolated opercular epithelium of killifish: a membrane rich in chloride cells. Science. 1977 Jan 14;195(4274):203–205. doi: 10.1126/science.831273. [DOI] [PubMed] [Google Scholar]
  17. Llinas R., Baker R., Precht W. Blockage of inhibition by ammonium acetate action on chloride pump in cat trochlear motoneurons. J Neurophysiol. 1974 May;37(3):522–532. doi: 10.1152/jn.1974.37.3.522. [DOI] [PubMed] [Google Scholar]
  18. Lux H. D. Ammonium and chloride extrusion: hyperpolarizing synaptic inhibition in spinal motoneurons. Science. 1971 Aug 6;173(3996):555–557. doi: 10.1126/science.173.3996.555. [DOI] [PubMed] [Google Scholar]
  19. Marchbanks R. M., Campbell C. W. Sodium and chloride fluxes in synaptosomes in vitro. J Neurochem. 1976 May;26(5):973–980. doi: 10.1111/j.1471-4159.1976.tb06480.x. [DOI] [PubMed] [Google Scholar]
  20. Mullins L. J., Brinley F. J., Jr, Spangler S. G., Abercrombie R. F. Magnesium efflux in dialyzed squid axons. J Gen Physiol. 1977 Apr;69(4):389–400. doi: 10.1085/jgp.69.4.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nadarajah A., Leese B., Joplin G. F. Triton X-100 scintillant for counting calcium-45 in biological fluids. Int J Appl Radiat Isot. 1969 Oct;20(10):733–735. doi: 10.1016/0020-708x(69)90071-4. [DOI] [PubMed] [Google Scholar]
  22. Nellans H. N., Frizzell R. A., Schultz S. G. Coupled sodium-chloride influx across the brush border of rabbit ileum. Am J Physiol. 1973 Aug;225(2):467–475. doi: 10.1152/ajplegacy.1973.225.2.467. [DOI] [PubMed] [Google Scholar]
  23. Russell J. M. ATP-Dependent chloride influx into internally dialyzed squid giant axons. J Membr Biol. 1976 Sep 17;28(4):335–349. doi: 10.1007/BF01869704. [DOI] [PubMed] [Google Scholar]
  24. Russell J. M., Boron W. F. Role of choloride transport in regulation of intracellular pH. Nature. 1976 Nov 4;264(5581):73–74. doi: 10.1038/264073a0. [DOI] [PubMed] [Google Scholar]
  25. Russell J. M., Brown A. M. Active transport of chloride by the giant neuron of the Aplysia abdominal ganglion. J Gen Physiol. 1972 Nov;60(5):499–518. doi: 10.1085/jgp.60.5.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Silva P., Stoff J., Field M., Fine L., Forrest J. N., Epstein F. H. Mechanism of active chloride secretion by shark rectal gland: role of Na-K-ATPase in chloride transport. Am J Physiol. 1977 Oct;233(4):F298–F306. doi: 10.1152/ajprenal.1977.233.4.F298. [DOI] [PubMed] [Google Scholar]
  27. Thomas R. C. The role of bicarbonate, chloride and sodium ions in the regulation of intracellular pH in snail neurones. J Physiol. 1977 Dec;273(1):317–338. doi: 10.1113/jphysiol.1977.sp012096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Webb D. A., Young J. Z. Electrolyte content and action potential of the giant nerve fibres of loligo. J Physiol. 1940 Jul 24;98(3):299–313. doi: 10.1113/jphysiol.1940.sp003851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zadunaisky J. A. Sodium activation of chloride transport in the frog cornea. Biochim Biophys Acta. 1972 Sep 1;282(1):255–257. doi: 10.1016/0005-2736(72)90331-8. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES