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. 1997 Dec;23(4):195–208. doi: 10.1023/A:1005013802448

Ion Regulation of the Kinetics of Potential-Dependent Potassium Channels

OV Grishchenko 1, VN Kharkyanen 1, NI Kononenko 2, GE Weinreb 1
PMCID: PMC3456498  PMID: 23345661

Abstract

We apply a theoretical approach developed earlier. The interaction ofions that permeate a channel with slowly relaxing charged channel-forminggroups (ion-conformational interaction – ICI) is addressed by thisapproach. One can describe the ion concentration influence (ion regulation)on channel functioning in this manner. A patch-clamp method in a’whole-cell‘ configuration is used to study the ICI. For this purpose theinfluence of an external concentration of potassium ions on thepotential-dependent potassium current (IA) in the externalmembrane of GH3 cells was studied. The increase of[K+out] from 5 mM to 100 mM causes anon-monotonous shift of current-voltage dependencies. The dependence of bothan activation time constant tgrn and a steady-state activation(n∞) on [K+]out have a minimum andmaximum respectively. The analysis of the results suggests that the observedeffects are caused by ICI. A physical model is developed to describe thedependence of the potassium channel kinetics on the external concentrationof the ions and the membrane potential. The ’deformation‘ of the closedstate of the gate and the corresponding energy shifts cause the observednon-monotonous dependencies due to ICI. Thus, the general theoreticalapproach has an experimental confirmation and is applied to concreteexamples. Formulas for concentrational dependencies of the channel kineticsare given for practical uses.

Keywords: Potential-dependent ion channels, Channel kinetics, Concentrational dependencies, Ion-conformational interaction (ICI)

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References

  • 1.Aggarwal S.K., MacKinnon R. Contribution of the S4 segment to gating charge in the shaker K+ channel. Neuron. 1996;16:1169–1177. doi: 10.1016/s0896-6273(00)80143-9. [DOI] [PubMed] [Google Scholar]
  • 2.Armstrong C.M., Bezanilla F. Currents related to movement of the gating particles of the sodium channels. Nature(Lond.) 1973;242:459–461. doi: 10.1038/242459a0. [DOI] [PubMed] [Google Scholar]
  • 3.Bystrov V.S., Lakhno V.D., Molchanov M. Ferroelectric active models of ion channels in biomembranes. J. Theor. Biol. 1994;168:383–393. doi: 10.1006/jtbi.1994.1118. [DOI] [PubMed] [Google Scholar]
  • 4.Chinarov V.A., Gaididei Y., Kharkyanen V.N., Sit’ko S.P. Ion pores in biological membranes as selforganized bistable systems. Phys. Rev. A. 1992;46:5232–5241. doi: 10.1103/physreva.46.5232. [DOI] [PubMed] [Google Scholar]
  • 5.Ciani, S.:Coupling between fluxes in oneparticle pores with fluctuating energy profiles, Biophys. J.46(1984), 249–252. [DOI] [PMC free article] [PubMed]
  • 6.Demchenko A.P., Kositsky N.N., Teslenko V.I. The influence of dynamics of ionic channel protein on its selectivity function. Biophys. Chem. 1990;35:25–35. doi: 10.1016/0301-4622(90)80057-e. [DOI] [PubMed] [Google Scholar]
  • 7.Eisenman, G. and Dani, J.A.: Characterising the electrical behavior of an open channel via the energy profile for ion permeation: A prototype using a fluctuating barrier model for the acetylcholine receptor channel. In: Ionic channels in cells and model systems, ed. by Ramon Latorre (1986), pp. 53–87.
  • 8.Fahlke C., Ruppersberg J.P. Saturation effects and rectifier properties of sodium channels in human skeletal muscle. Eur. Biophys. J. 1988;16:307–312. doi: 10.1007/BF00254067. [DOI] [PubMed] [Google Scholar]
  • 9.Hamill O.P., Marty A., Neher E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cell and cell-free membrane patches. Pflüger Arch. 1981;391:85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  • 10.Hille B. Ionic channels of excitable membranes. 2nd edn. Sunderland, Massachusetts: University of Washington. Sinauer Associates Inc. Publishers; 1992. [Google Scholar]
  • 11.Hodgkin A.L., Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol.(Lond.) 1952;117:500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Imoto K. Ion channels: molecular basis of ion selectivity. FEBS Lett. 1993;325:100–103. doi: 10.1016/0014-5793(93)81422-v. [DOI] [PubMed] [Google Scholar]
  • 13.Jordan P.C. Interactions of ions with membrane proteins. In: Jackson M.B., editor. Thermodynamics of membrane receptors and channels. Boston: CRC Press; 1993. pp. 27–80. [Google Scholar]
  • 14.Kharkyanen V.N., Panchouk A.S., Weinreb G.E. Self-organization effects induced by ion-conformational interaction in biomembrane channels. J. Biol. Phys. 1994;19:259–272. [Google Scholar]
  • 15.Kononenko N.I., Shcherbatko A.D. The influence of calcium ions on the deactivation of calcium current in the neurones of Helix pomatia. Doklady Akademii Nauk SSSR (Moscow) 1989;602:167–180. [PubMed] [Google Scholar]
  • 16.Lauger P., Stephan W., Frehland E. Fluctuations of barrier structure in ionic channels. Biochim. Biophys. Acta. 1980;602:167–180. doi: 10.1016/0005-2736(80)90299-0. [DOI] [PubMed] [Google Scholar]
  • 17.Larsson H.P., Baker O.S., Dhillon D.S., Isacoff E.Y. Transmembrane movement of the shaker K+-channel S4. Neuron. 1996;16:387–397. doi: 10.1016/s0896-6273(00)80056-2. [DOI] [PubMed] [Google Scholar]
  • 18.Leuchtag H.R. A proposed physical explanation of the activation of sodium channels. Ferroelectrics. 1988;86:105–113. [Google Scholar]
  • 19.Leuchtag H.R. Long-range interactions, voltage sensitivity, and ion conduction in S4 segments of excitable channels. Biophys. J. 1994;66:217–224. doi: 10.1016/S0006-3495(94)80757-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Liu Y., Jurman M.E., Yellen G. Dynamic rearrangement of the outer mouth of a K+-channel during gating. Neuron. 1996;16:859–867. doi: 10.1016/s0896-6273(00)80106-3. [DOI] [PubMed] [Google Scholar]
  • 21.Logothetis D.E., Kammen B.F., Lindpaintner K., Bisbas D., Nadal-Ginard B. Gating charge differences between two voltage-gated K+-channels are due to the specific charge content of their respective S4 regions. Neuron. 1993;10:1121–1129. doi: 10.1016/0896-6273(93)90060-5. [DOI] [PubMed] [Google Scholar]
  • 22.Magura I.S., Zachar J., Prevarskaya N.B. Interaction of sodium ions with potassium channels of mollusc neuronal somatic membrane. Gen. Physiol. Biophys. 1985;4:93–96. [PubMed] [Google Scholar]
  • 23.Partenskii M.B., Jordan P.C. Theoretical perspectives on ion-channel electrostatics: continuum and microscopic approaches. Quarterly Reviews of Biophysics. 1992;25:477–510. doi: 10.1017/s0033583500004388. [DOI] [PubMed] [Google Scholar]
  • 24.Rogawski M. A. Transient outward current (Ia) in clonal auterior pituitary cells: blockade by aminopyridine analogs. Arch. of Pharmacology. 1988;338:125–132. doi: 10.1007/BF00174859. [DOI] [PubMed] [Google Scholar]
  • 25.Schagina L.V., Grinfeldt A.E., Lev A.A. Concentration dependence of bidirectional flux ration as a characteristic of transmembrane ion transporting mechanism. J. Membrane Biol. 1983;73:203–216. [Google Scholar]
  • 26.Shuba Y.M., Teslenko V.I., Savchenko A.N., Pogorelaya N.H. The effect of permeant ions on single calcium channel activation in mouse neuroblastoma cells: ionchannel interaction. J. Physiol. 1991;443:25–44. doi: 10.1113/jphysiol.1991.sp018820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Tseyeb V.E., Geletyuk V.I., Kazatchenko V.N., Ilyasov F.E. Relationship between the activity of a fast K+-channel and the current value through it. Biologicheskiye membrany. 1992;9:518–527. [Google Scholar]
  • 28.Warshel A., Aqvist J. Electrostatic energy and macromolecular function. Ann. Rev. Biophys. Chem. 1991;20:267–298. doi: 10.1146/annurev.bb.20.060191.001411. [DOI] [PubMed] [Google Scholar]
  • 29.Weinreb G.E. Effects of ion-conformational interaction in biomembrane channels. Physics of the Alive. 1994;2:26–34. [Google Scholar]
  • 30.Weinreb G.E., Kharkyanen V.N. A new phenomenon induced by ion-conformational interaction in the channels of biomembranes. Biophysics. 1995;40:83–91. [PubMed] [Google Scholar]
  • 31.White P.J., Martin S., Thiel G. Characterisation of ion channels from Acetabulariaplasma membrane in planar lipid bilayer. J. Membr. Biol. 1993;133:145–160. doi: 10.1007/BF00233795. [DOI] [PubMed] [Google Scholar]
  • 32.Yang N., George A.L., Horn R. Molecular basis of charge movement in voltage-gated sodium channels. Neuron. 1996;16:113–122. doi: 10.1016/s0896-6273(00)80028-8. [DOI] [PubMed] [Google Scholar]
  • 33.Zilberter Y., Burnashev N.A., Papin A.A., Khodorov B.I. Interaction of potassium ions with gating structures of ATP-dependent potassium channels in myocardial cells. Biologicheskiye membrany. 1987;4:738–746. [Google Scholar]

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