Skip to main content
Log in

Investigations of Electrogenic Ion Transport by Na+,K+-ATPase in Bilayer Lipid Membranes by Impedance Method

  • REVIEWS
  • Published:
Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract—

The results of investigation of electrogenic transport by the Na+,K+-ATPase, the enzyme providing the active transport of Na+ and K+ ions through cell membrane, are reviewed. The main contribution to electric current generated through the functioning of the Na+,K+-ATPase is assigned to the movements of ions in access channels—the channel-like structures connecting the ion binding sites with the solutions. The electrogenic transport was studied in a model system consisting of a bilayer lipid membrane with adsorbed membrane fragments containing the Na+,K+-ATPase. The impedance method applied to this study allowed the investigation of access channels in the Na+,K+-ATPase. The review notes a significant contribution of Yu.A. Chizmadzhev to the development of the theoretical model of transport processes in the Na+,K+-ATPase.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Mueller P., Rudin D.O., Tien H.T., Wescott W.C. 1963. Methods for the formation of single bimolecular lipid membranes in aqueous solution. J. Phys. Chem. 67, 534–535.

    Article  CAS  Google Scholar 

  2. Markin V.S., Chizmadzhev Yu.A. 1974. Indutsirovannyi ionny transport (Induced ion transport). Moscow: Nauka.

  3. Markin V.S., Sokolov V.S. 1986. Membrane potential during coupled electrogenic transport. Thermodynamic consideration. Biol. Membrany (Rus.). 3, 638–649.

    Google Scholar 

  4. Sokolov V.S., Markin V.S. 1984. Electrogenic transport of potassium and hydrogen ions across the membrane performed by antibiotics nigericin and grizorixin. Biol. Membrany (Rus.). 1 (10), 1071–1086.

    CAS  Google Scholar 

  5. Markin V.S., Sokolov V.S. 1990. A new concept of electrochemical membrane equilibrium. Coupled transport and membrane potential. Bioelectrochem. Bioenerg. 23, 1–16.

    Article  CAS  Google Scholar 

  6. Portnov V.I., Mirsky V.M., Markin V.S. 1990. Bacteriorhodopsin: Current-voltage characteristics. Bioelectrochem. Bioenerg. 23, 45–63.

    Article  CAS  Google Scholar 

  7. Post R.L., Hegyvary C., Kame S. 1972. Activation by adenosine triphosphate in the phosphorylation kinetics of sodium and potassium ion transport adenosine triphosphatase. J. Biol. Chem. 247, 6530–6540.

    Article  CAS  Google Scholar 

  8. Morth J.P., Pedersen B.P., Toustrup-Jensen M.S., Sorensen T.L., Petersen J., Andersen J.P., Vilsen B., Nissen P. 2007. Crystal structure of the sodium-potassium pump. Nature. 450 (7172), 1043–1049.

    Article  CAS  Google Scholar 

  9. Ogawa H., Shinoda T., Cornelius F., Toyoshima C. 2009. Crystal structure of the sodium-potassium pump (Na+,K+-ATPase) with bound potassium and ouabain. Proc. Natl. Acad. Sci. USA. 106 (33), 13742–13747.

    Article  CAS  Google Scholar 

  10. Shinoda T., Ogawa H., Cornelius F., Toyoshima C. 2009. Crystal structure of the sodium-potassium pump at 2.4 A resolution. Nature. 459 (7245), 446–450.

    Article  CAS  Google Scholar 

  11. Kanai R., Ogawa H., Vilsen B., Cornelius F., Toyoshima C. 2013. Crystal structure of a Na+-bound Na+,K+-ATPase preceding the E1P state. Nature. 502 (7470), 201–206.

    Article  CAS  Google Scholar 

  12. Toyoshima C., Kanai R., Cornelius F. 2011. First crystal structures of Na+,K+-ATPase: New light on the oldest ion pump. Structure. 19 (12), 1732–1738.

    Article  CAS  Google Scholar 

  13. Nyblom M., Poulsen H., Gourdon P., Reinhard L., Andersson M., Lindahl E., Fedosova N., Nissen P. 2013. Crystal structure of Na+,K+-ATPase in the Na+-bound state. Science. 342 (6154), 123–127.

    Article  CAS  Google Scholar 

  14. Bublitz M., Morth J.P., Nissen P. 2011. P-type ATPases at a glance. J. Cell Sci. 124 (Pt 15), 2515–2519.

    Article  CAS  Google Scholar 

  15. Axelsen K.B., Palmgren M.G. 1998. Evolution of substrate specificities in the P-type ATPase superfamily. J. Mol. Evol. 46 (1), 84–101.

    Article  CAS  Google Scholar 

  16. Palmgren M.G., Axelsen K.B. 1998. Evolution of P-type ATPases. Biochim. Biophys. Acta. 1365 (1–2), 37–45.

    Article  CAS  Google Scholar 

  17. Pedersen C.N., Axelsen K.B., Harper J.F., Palmgren M.G. 2012. Evolution of plant p-type ATPases. Front. Plant Sci. 3, 31.

    Article  CAS  Google Scholar 

  18. Wuddel I., Apell H.J. 1995. Electrogenicity of the sodium transport pathway in the Na,K-ATPase probed by charge-pulse experiments. Biophys. J. 69 (3), 909–921.

    Article  CAS  Google Scholar 

  19. Lauger P. 1991. Electrogenic ion pumps. Sunderland, Massachusets, USA: Sinauer Associates, Inc.

  20. De Weer P., Gadsby D.C., Rakowski R.F. 1988. Voltage dependence of the Na-K pump. Ann. Rev. Physiol. 50, 225–241.

    Article  CAS  Google Scholar 

  21. Gadsby D.C., Rakowski R.F., De Weer P. 1993. Extracellular access to the Na,K-pump: Pathway similar to ion channel. Science. 260, 100–103.

    Article  CAS  Google Scholar 

  22. Apell H.-J., Borlinghaus R., Lauger P. 1989. Electrogenic properties of the Na/K pump-voltage dependence and kinetics of charge translocation. Curr. Top. Membr. Transp. 34, 229–252.

    Article  CAS  Google Scholar 

  23. Nakao M., Gadsby D.C. 1986. Voltage dependence of Na translocation by the Na/K pump. Nature. 323 (6089), 628–630.

    Article  CAS  Google Scholar 

  24. Apell H.J., Borlinghaus R., Lauger P. 1987. Fast charge translocations associated with partial reactions of the Na,K-pump: II. Microscopic analysis of transient currents. J. Membrane Biol. 97 (3), 179–191.

    Article  CAS  Google Scholar 

  25. Pavlov K.V., Sokolov V.S. 2000. Electrogenic ion transport by Na+,K+-ATPase. Membr. Cell Biol. 13 (6), 745–788.

    CAS  Google Scholar 

  26. Holmgren M., Wagg J., Bezanilla F., Rakowski R.F., De Weer P., Gadsby D.C. 2000. Three distinct and sequential steps in the release of sodium ions. Nature. 403, 898–901.

    Article  CAS  Google Scholar 

  27. Rakowski R.F., Paxson C.L. 1988. Voltage dependence of Na/K pump current in Xenopus oocytes. J. Membrane Biol. 106, 173–182.

    Article  CAS  Google Scholar 

  28. Holmgren M., Rakowski R.F. 2006. Charge translocation by the Na+/K+ pump under Na+/Na+ exchange conditions: Intracellular Na+ dependence. Biophys. J. 90 (5), 1607–1616.

    Article  CAS  Google Scholar 

  29. Hilgemann D.W. 1994. Channel-like function of the Na,K pump probed at microsecond resolution in giant membrane patches. Science. 263, 1429–1432.

    Article  CAS  Google Scholar 

  30. Lu C.-C., Kabakov A., Markin V.S., Mager S., Frazier S., Frazier G.A., Hilgemann D.W. 1995. Membrane transport mechanisms probed by capacitance measurements with megahertz voltage clamp. Proc. Natl. Acad. Sci. USA. 1995, 11220–11224.

    Article  Google Scholar 

  31. Fendler K., Grell E., Haubs M., Bamberg E. 1985. Pump currents generated by the Na+,K+-ATPase from kidney on black lipid membranes. EMBO J. 4, 3079–3085.

    Article  CAS  Google Scholar 

  32. Borlinghaus R., Apell H.J., Lauger P. 1987. Fast charge translocations associated with partial reactions of the Na,K-pump: I. Current and voltage transients after photochemical release of ATP. J. Membrane Biol. 97 (3), 161–178.

    Article  CAS  Google Scholar 

  33. McCray J.A., Trentham D.R. 1989. Properties and uses of photoreactive caged compounds. Annu. Rev. Biophys. Biophys. Chem. 18, 239–270.

    Article  CAS  Google Scholar 

  34. Apell H.J., Roudna M., Corrie J.E., Trentham D.R. 1996. Kinetics of the phosphorylation of Na,K-ATPase by inorganic phosphate detected by a fluorescence method. Biochemistry. 35 (33), 10922–10930.

    Article  CAS  Google Scholar 

  35. Sokolov V.S., Pavlov K.V., Dzhandzhugazyan K.N., Bamberg E. 1992. Capacitance and conductivity changes during Na+,K+-ATPase action in model membranes. Biol. Membranes. 6 (9), 1263–1272.

    Google Scholar 

  36. Shcherbakov A.A., Chizmadzhev Yu.A., Lenz A.A., Sokolov V.S. 2005. Impedance spectroscopy of sodium ion transport in Na+,K+-ATPase. Biol. Membrany (Rus.). 22 (6), 511–523.

    Google Scholar 

  37. Sokolov V.S., Shcherbakov A.A., Lenz A.A., Chizmadzhev Yu.A., Apell H.J. 2008. Electrogenic transport of sodium ions in cytoplasmic and extracellular ion access channels of Na+,K+-ATPase probed by admittance measurement technique. Biochem. (Moscow) Suppl. Series A: Membr. Cell Biol. 2 (2), 161–180.

    Google Scholar 

  38. Post R.L., Suzuki K. 1991. The sodium pump: Structure, mechanism and regulation. Ed. De Weer P., Kaplan J.H. New York: Rockfeller University Press, p. 202–209.

  39. Sokolov V.S., Ayuyan A.G., Apell H.J. 2001. Assignment of charge movements to electrogenic reaction steps of Na,K-ATPase by analysis of salt effects on the kinetics of charge movements. Eur. Biophys. J. 30 (7), 515–527.

    Article  CAS  Google Scholar 

  40. Schneeberger A., Apell H.J. 2001. Ion selectivity of the cytoplasmic binding sites of the Na,K-ATPase: II. Competition of various cations. J. Membrane Biol. 179 (3), 263–273.

    Article  CAS  Google Scholar 

  41. Schneeberger A., Apell H.J. 1999. Ion selectivity of the cytoplasmic binding sites of the Na,K-ATPase: I. Sodium binding is associated with a conformational rearrangement. J. Membrane Biol. 168 (3), 221–228.

    Article  CAS  Google Scholar 

  42. Heyse S., Wuddel I., Apell H.J., Sturmer W. 1994. Partial reactions of the Na,K-ATPase: Determination of rate constants. J. Gen. Physiol. 104 (2), 197–240.

    Article  CAS  Google Scholar 

  43. Domaszewicz W., Apell H. 1999. Binding of the third Na+ ion to the cytoplasmic side of the Na,K-ATPase is electrogenic. FEBS Lett. 458 (2), 241–246.

    Article  CAS  Google Scholar 

  44. Apell H.J., Diller A. 2002. Do H+ ions obscure electrogenic Na+ and K+ binding in the E1 state of the Na,K-ATPase? FEBS Lett. 532 (1–2), 198–202.

    Article  CAS  Google Scholar 

  45. Apell H.J., Benz G., Sauerbrunn D. 2011. Proton diet for the sodium pump. Biochemistry. 50 (3), 409–418.

    Article  CAS  Google Scholar 

  46. Vasilyev A., Khater K., Rakowski R.F. 2004. Effect of extracellular pH on pre-steady-state and steady-state current mediated by the Na+/K+ pump. J. Membrane Biol. 198 (2), 65–76.

    Article  CAS  Google Scholar 

  47. Vedovato N., Gadsby D.C. 2014. Route, mechanism, and implications of proton import during Na+/K+ exchange by native Na+/K+-ATPase pumps. J. Gen. Physiol. 143 (4), 449–464.

    Article  CAS  Google Scholar 

  48. Polvani C., Blostein R. 1988. Protons as substitutes for sodium and potassium in the sodium pump reaction. J. Biol. Chem. 263 (32), 16 757–16 763.

    Article  Google Scholar 

  49. Polvani C., Sachs G., Blostein R. 1989. Sodium ions as substitutes for protons in the gastric H,K-ATPase. J. Biol. Chem. 264 (30), 17 854–17 859.

    Article  Google Scholar 

  50. Grishanin K.O., Tashkin V.Yu., Lenz A.A., Apell H.-J., Sokolov V.S. 2010. On potential involvement of protons in the functioning of Na+,K+-ATPase. Biol. Membrany (Rus.). 27 (6), 512–518.

    CAS  Google Scholar 

  51. Tashkin V.Yu., Gavril’chik A.N., Ilovaysky A.I., Apell H.-J., Sokolov V.S. 2015. Electrogenic binding of ions at the cytoplasmic side of Na+,K+-ATPase. Biochem. (Moscow) Suppl. Series A: Membr. Cell Biol. 9 (2), 92–99.

    Google Scholar 

  52. Tashkin V.Yu., Shcherbakov A.A., Apell H.-J., Sokolov V.S. 2013. The competition transport of sodium ions and protons at the cytoplasmic side of Na,K-ATPase. Biochem. (Moscow) Suppl. Series A: Membr. Cell Biol. 7 (2), 113–121.

    Google Scholar 

  53. Vishnyakova V.E., Tashkin V.Yu., Terentjev A.O., Apell H.-J., Sokolov V.S. 2018. Binding of potassium ions inside the access channel at the cytoplasmic side of Na+,K+-ATPase. Biochem. (Moscow) Suppl. Series A: Membr. Cell Biol. 12 (4), 344–351.

    Google Scholar 

Download references

Funding

The work was supported by the Ministry of Science and Higher Education of the Russian Federation (registration number of the project, 122011300058-3).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. S. Sokolov.

Ethics declarations

The authors declare that they have no conflict of interest.

This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Makeeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sokolov, V.S. Investigations of Electrogenic Ion Transport by Na+,K+-ATPase in Bilayer Lipid Membranes by Impedance Method. Biochem. Moscow Suppl. Ser. A 16, 282–290 (2022). https://doi.org/10.1134/S1990747822050117

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747822050117

Keywords:

Navigation