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Binding of Potassium Ions Inside the Access Channel at the Cytoplasmic Side of Na+,K+-ATPase

  • V. Ye. Vishnyakova
  • V. Yu. Tashkin
  • A. O. Terentjev
  • H.-J. Apell
  • V. S. Sokolov
ARTICLES
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Abstract

Binding of potassium ions through an access channel from the cytoplasmic side of Na+,K+-ATPase and the effect of pH and magnesium ions on this process have been studied. The studies were carried out by a previously developed method of measuring small increments of the admittance (capacitance and conductivity) of a compound membrane consisting of a bilayer lipid membrane with adsorbed membranes fragments containing Na+,K+-ATPase. The capacitance change of the membrane with the Na+,K+-ATPase was induced abruptly by release of protons from a bound form (caged H+) upon a UV-light flash in the absence of magnesium ions. The change of admittance consisted of an initial fast jump and a slow relaxation to a stationary value within a time of about 1–2 s. The kinetics of the capacitance relaxation depended on pH and the concentration of magnesium and potassium ions. The dependence of the rapid capacitance jump on the potassium concentration corresponded to the predictions of the model developed earlier that describes binding of sodium or potassium ions in competition with protons. The effect of magnesium ions can be explained by the assuming that they bind to the Na+,K+-ATPase and affect binding of potassium ions because of either changes in protein conformation or the creation of an electrostatic field in the access channel on the cytoplasmic side.

Keywords:

Na+,K+-ATPase sodium pump electrogenic ion transport caged proton admittance measurement K+ binding by the Na+,K+-ATPase 

Notes

ACKNOWLEDGMENTS

The work was supported by Russian Foundation for Basic Research (project no. 16-04-01162).

COMPLIANCE WITH ETHICAL STANDARDS

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.

REFERENCES

  1. 1.
    Albers R.W. 1967. Biochemical aspects of active transport. Annu. Rev. Biochem. 36, 727–756.CrossRefGoogle Scholar
  2. 2.
    Hegyvary C., Post R.L. 1971. Binding of adenosine triphosphate to sodium and potassium ion-stimulated adenosine triphosphatase. J. Biol.Chem. 246, 5234–5240.Google Scholar
  3. 3.
    Axelsen K.B., Palmgren M.G. 1998. Evolution of substrate specificities in the P-type ATPase superfamily. J. Mol. Evol. 46 (1), 84–101.CrossRefGoogle Scholar
  4. 4.
    Palmgren M.G., Axelsen K.B. 1998. Evolution of P-type ATPases. Biochim. Biophys. Acta. 1365 (1–2), 37–45.CrossRefGoogle Scholar
  5. 5.
    Pedersen C.N., Axelsen K.B., Harper J.F., Palmgren M.G. 2012. Evolution of plant P-type ATPases. Front. Plant Sci. 3 (31), 1–19.CrossRefGoogle Scholar
  6. 6.
    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.CrossRefGoogle Scholar
  7. 7.
    Vasilyev A., Khater K., Rakowski R.F. 2004. Effect of extracellular pH on presteady-state and steady-state current mediated by the Na+/K+ pump. J. Membr. Biol. 198 (2), 65–76.CrossRefGoogle Scholar
  8. 8.
    Apell H.J., Benz G., Sauerbrunn D. 2011. Proton diet for the sodium pump. Biochemistry. 50 (3), 409–418.CrossRefGoogle Scholar
  9. 9.
    Grishanin K.A., Tashkin V.Y., Lenz A., Apell H.-J., Sokolov V.S. 2010. On the possible participation of protons in the functioning of Na+,K+-ATPase. Biol. membrany (Rus.). 27 (6), 512–518.Google Scholar
  10. 10.
    Polvani C., Blostein R. 1988. Protons as substitutes for sodium and potassium in the sodium pump reaction. J. Biol. Chem. 263 (32), 16757–16763.Google Scholar
  11. 11.
    Polvani C., Sachs G., Blostein R. 1989. Sodium ions as substitutes for protons in the gastric H,K-ATPase. J. Biol. Chem. 264 (30), 17854–17859.Google Scholar
  12. 12.
    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.CrossRefGoogle Scholar
  13. 13.
    Bublitz M., Poulsen H., Morth J.P., Nissen P. 2010. In and out of the cation pumps: P-type ATPase structure revisited. Curr. Opin. Struct. Biol. 20 (4), 431–439.CrossRefGoogle Scholar
  14. 14.
    Morth J.P., Pedersen B.P., Buch-Pedersen M.J., Andersen J.P., Vilsen B., Palmgren M.G., Nissen P. 2011. A structural overview of the plasma membrane Na+,K+-ATPase and H+-ATPase ion pumps. Nat. Rev. Mol. Cell Biol. 12 (1), 60–70.CrossRefGoogle Scholar
  15. 15.
    Schack V.R., Morth J.P., Toustrup-Jensen M.S., Anthonisen A.N., Nissen P., Andersen J.P., Vilsen B. 2008. Identification and function of a cytoplasmic K+ site of the Na+,K+-ATPase. J. Biol.Chem. 283 (41), 27982–27990.CrossRefGoogle Scholar
  16. 16.
    Ogawa H., Toyoshima C. 2002. Homology modeling of the cation binding sites of Na+,K+-ATPase. Proc. Natl. Acad. Sci. USA. 99 (25), 15977–15982.CrossRefGoogle Scholar
  17. 17.
    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.CrossRefGoogle Scholar
  18. 18.
    Shinoda T., Ogawa H., Cornelius F., Toyoshima C. 2009. Crystal structure of the sodium-potassium pump at 2.4 Å resolution. Nature. 459 (7245), 446–450.CrossRefGoogle Scholar
  19. 19.
    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.CrossRefGoogle Scholar
  20. 20.
    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.CrossRefGoogle Scholar
  21. 21.
    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.CrossRefGoogle Scholar
  22. 22.
    Shainskaya A., Schneeberger A., Apell H.J., Karlish S.J. 2000. Entrance port for Na+ and K+ ions on Na+,K+-ATPase in the cytoplasmic loop between trans-membrane segments M6 and M7 of the alpha subunit. Proximity of the cytoplasmic segment of the beta subunit. J. Biol. Chem. 275 (3), 2019–2028.CrossRefGoogle Scholar
  23. 23.
    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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 25.
    Apell H.-J., Sokolov V.S. 2015. Pumps, channels and transporters: Methods of functional analysis. Eds. Clarke R.J., Khalid M.A.A. Hoboken, New Jersey: Wiley, p. 23–49.Google Scholar
  26. 26.
    Tashkin V.Yu., Shcherbakov A.A., Apell, H.-J., Sokolov V.S. 2013. Competitive transport of sodium ions and protons in the cytoplasmic channel of Na+,K+-ATPase. Biol. membrany (Rus.). 30 (2), 105–114.Google Scholar
  27. 27.
    Tashkin V.Yu., Gavrilchik A.N., Ilovaysky A.I., Apell H.-J., Sokolov V.S. 2015. Electrogenic binding of ions from the cytoplasmic side of Na+,K+-ATPase. Biol. membrany (Rus.). 32 (2), 110–118.Google Scholar
  28. 28.
    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.CrossRefGoogle Scholar
  29. 29.
    Fibich A., Janko K., Apell H.J. 2007. Kinetics of proton binding to the sarcoplasmic reticulum Ca-ATPase in the E1 state. Biophys. J. 93 (9), 3092–3104.CrossRefGoogle Scholar
  30. 30.
    Jørgensen P.L. 1974. Isolation of the Na,K-ATPase. Meth. Enzymol. 32, 277–290.CrossRefGoogle Scholar
  31. 31.
    Karlish S.J. 1980. Characterization of conformational changes in (Na,K) ATPase labeled with fluorescein at the active site. J. Bioenerg. Biomembr. 12 (3–4), 111–136.CrossRefGoogle Scholar
  32. 32.
    Heyse S., Wuddel I., Apell H.J., Stürmer W. 1994. Partial reactions of the Na,K-ATPase: Determination of rate constants. J. Gen. Physiol. 104 (2), 197–240.CrossRefGoogle Scholar
  33. 33.
    Glynn I.M., Richards D.E. 1989. Evidence for the ordered release of rubidium ions occluded within individual protomers of dog kidney Na+,K+-ATPase. J. Physiol. (London). 408, 57–66.CrossRefGoogle Scholar
  34. 34.
    Forbush B., III. 1987. Rapid release of 42K and 86Rb from an occluded state of the Na,K-pump in the presence of ATP or ADP. J. Biol. Chem. 262 (23), 11104–11115.Google Scholar
  35. 35.
    Forbush B., III. 1988. Rapid 86Rb release from an occluded state of the Na,K-pump reflects the rate of dephosphorylation or dearsenylation. J. Biol. Chem. 263 (17), 7961–7969.Google Scholar
  36. 36.
    Garay R.P., Garrahan P.J. 1973. The interaction of sodium and potassium with the sodium pump in red cells. J. Physiol. 231 (2), 297–325.CrossRefGoogle Scholar
  37. 37.
    Homareda H., Matsui H., Nozaki T. 1987. Interaction of sodium and potassium-ions with Na+,K+-ATPase. 3. Cooperative effect of ATP and Na+ on complete release of K+ from E2K. J. Biochem. 101, 789–793.CrossRefGoogle Scholar
  38. 38.
    Matsui H., Hayashi Y., Homareda H., Kimimura M. 1977. Ouabain-sensitive 42K binding to Na+,K+-ATPase purified from canine kidney outer medulla. Biochem. Biophys. Res. Commun. 75 (2), 373–380.CrossRefGoogle Scholar
  39. 39.
    Hegyvary C., Jørgensen P.L. 1981. Conformational changes of renal sodium plus potassium ion-transport adenosine triphosphatase labeled with fluorescein. J. Biol. Chem. 256 (12), 6296–6303.Google Scholar
  40. 40.
    Forbush B., III. 1987. Rapid release of 42K or 86Rb from two distinct transport sites on the Na,K-pump in the presence of Pi or vanadate. J. Biol. Chem. 262 (23), 11116–11127.Google Scholar
  41. 41.
    Apell H.J., Hitzler T., Schreiber G. 2017. Modulation of the Na,K-ATPase by magnesium ions. Biochemistry. 56 (7), 1005–1016.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • V. Ye. Vishnyakova
    • 1
  • V. Yu. Tashkin
    • 1
  • A. O. Terentjev
    • 2
  • H.-J. Apell
    • 3
  • V. S. Sokolov
    • 1
  1. 1.Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of SciencesMoscowRussia
  2. 2.Zelinsky Institute of Organic Chemistry, Russian Academy of SciencesMoscowRussia
  3. 3.Department of Biology, University of KonstanzKonstanzGermany

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