Abstract
A physico-mathematical model of the gating machinery of single ionic channels in biological membranes has been developed. In the paradigm of this model, gating particles are subjected to: (i) deterministic friction force responsible for interactions of gating particles with the surrounding solution; (ii) deterministic potential force depending on the structure and conformational state of the channel pore (the latter is controlled by the transmembrane voltage V and regulates the motion of particles overcoming potential barriers on going from the closed (open) to the open (closed) state of the channel); (iii) deterministic force responsible for interactions of water molecules with hydrophobic sites in the channel pore, and, finally, (iv) stochastic thermal fluctuation force. The model affords adequate approximation of experimental data.
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Kazachenko, V.N. and Kochetkov, K.V., Maxi-Ca2+-Activated K+ Channels: Structure and Gating Machinery, Biologicheskie Membrany (Rus.), 2003, vol. 20, pp. 99–120.
Liebovitch, L.S., Fischbarg, J., and Koniarek, J., Ion Channel Kinetics: A Model Based on Fractal Scaling Rather than Multistate Markov Process, Math. Biosci., 1987, vol. 84, pp. 37–68.
Liebovitch, L.S. and Lullivan, J.M., Fractal Analysis of a Voltage-Dependent Potassium Channel from Cultured Mouse Hippocampal Neurons, Biophys. J., 1987, vol. 52, pp. 979–988.
Liebovitch, L.S. and Krekora, P., The Physical Basis of Ion Channel Kinetics: The Impotance of Dynamics, Proc. Inst. Math. And Its Appl. Univer. Minnessota, 2002, vol. 129, pp. 27–52.
Mcmanus, O.B., Blatz, A.L., and Magleby, K.L., Inverse Relationship of the Durations of Adjacent Open and Shut Intervals for Cl− and K+ Channels, Nature (Lond.), 1985, vol. 317, pp. 625–627.
Varanda, W.A., Liebovitch, L.S., Figueiroa, J.N., and Nogueira, R.A., Hurst Analysis Applied to the study of Single Calcium-Activated Potassium Channel Kinetics, J. Theor. Biol., 2000, vol. 206, pp. 343–353.
Nogueira, R.A., Varanda, W.A., and Liebovitch, L.S., Hurst Analysis in the Study of Ion Current Kinetics, Brasilian J. Med. Biol., 1995, vol. 28, pp. 491–496.
Kochetkov, K.V., Kazachenko, V.N., Aslanidi, O.V., Chemeris, N.K., and Gapeev, A.B., Non-Markovian Gating of Ca2+-Activated K+-Channels Kidney Cells Vero. Rescaled Range Analysis, J. Biol. Phys., 1999, vol. 25, pp. 211–222.
Kochetkov, K.V., Kazachenko, V.N., and Aslanidi, O.V., Time Course of Reactions Related to Gating Activity of Ionic Channels as Established by the Rescaled Range Method, Biologicheskie Membrany (Rus.), 2001, vol. 18, pp. 51–66.
Kazachenko, V.N., Kochetkov, K.V., Astashev, M.E., and Grinevich, A.A., Fractal Characteristics of the Gating Machinery of Voltage-Dependent K+ Channels in L. stagnalis Neurons, Biofizika (Rus.), 2004, vol. 49, pp. 852–865.
Kazachenko, V.N., Kochetkov, K.V., Aslanidi, O.V., and Grinevich, A.A., Analysis of Fractal Characteristics of the “Gating” Machinery of Single Ionic Channels Using Fast Fourier Transform, Biofizika (Rus.), 2001, vol. 46, pp. 1062–1070.
Kochetkov, K.V., Kazachenko, V.N., and Aslanidi, O.V., Wavelet Transform As a Method of Choice for the Study of Single Ionic Channel Activity, Biologicheskie Membrany (Rus.), 2003, vol. 20, pp. 359–368.
Brazhe, A.R., Astashev, M.E., Maximov, G.V., Kazachenko, V.N., and Rubin, A.B., Calculation of Local Hurst Exponents in Lifetime Sequences of Ca2+-Activated K+-Channels, Biofizika (Rus.), 2004, vol. 49, pp. 1075–1083.
Colquhoun, D. and Hawkes, A.G., Relaxation and Fluctuations of Membrane Currents that Flow through Drug-Operated Channels, Proc. R. Soc. London Ser. B., 1977, vol. 199, pp. 231–262.
Croxton, T.L., A Model of the Gating of Ion Channels, Biochem. Biophys. Acta, 1988, vol. 946, pp. 19–24.
Horn, R., Statistical Methods for Model Discrimination. Applications to Gating Kinetics and Permeation of the Acetylholine Receptor Channel, Biophys. J., 1987, vol. 51, pp. 255–263.
Mcmanus, O.B. and Magleby, K.L., Accounting for the Ca2+-Depended Kinetics of Single Large-Conductance Ca2+-Activated K+-Channels in Rat Skeletal Muscle, J. Physiol. (London), 1994, vol. 443, pp. 739–777.
Liebovitch, L.S., Analysis of Fractal Ion Channel Gating Kinetics: Kinetics Rates Energy Levels and Activation Energies, Math. Biosci., 1989, vol. 93, pp. 97–115.
Liebovitch, L.S. and Toth, T.I., Fractal Activity in Cell Membrane Ion Channels, Math. Approach. Cardiac. Arrythmias, 1990, vol. 591, pp. 375–391.
Millhauser, G.L., Salpeter, E.E., and Oswald, R.E., Diffusion Models of Ion Channel Gating and the Origin of Power-Law Distributions from Single Channel Recording, Proc. Natl. Acad. Sci. USA, 1988, vol. 85, pp. 1503–1507.
Oswald, R.E., Millhause, G.L., and Carter, A.A., Diffusion Model in Ion Channel Gating. Extension to Agonist-Activated Ion Channels, Biophys. J., 1991, vol. 59, pp. 1136–1142.
Liebovitch, L.S. and Yang, W., Transition from Persistent to Antipersistent Correlation in Biological Systems, Phys. Rev. E, 1997, vol. 56, pp. 4557–4566.
Kurzynski, M., Palacz, K., and Chelminiak, P., Time Course of Reactions Controlled and Gated by Intramolecular Dynamics of Proteins: Predictions of the Model of Random Walk on Fractal Lattices, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 11685–11690.
Liebovitch, L.S. and Toth, T.I., A Model of Ionic Channel Kinetics Using Deterministic Chaotic Rather Than Stochastic Processes, J. Theor. Biol., 1991, vol. 148, pp. 243–267.
Liebovitch, L.S. and Czegledy, F., A Model of Ion Channel Kinetics Based on Deterministic Motion in a Potential with Two Local Minima, Ann. Biomed. Engr., 1992, vol. 84, pp. 37–68.
Cavalcanti, S. and Fontanazzi, F., Deterministic Model of Ion Channel Flipping ith Fractal Scaling of Kinetics Rates, Ann. Biomed. Engr., 1999, vol. 27, pp. 682–695.
Jiang, Y., Lee, A., Chen, J., Cadene, M., Chalt, B.T., and Mackinnon, R., The Open Pore Conformation of Potassium Channels, Nature, 2002, vol. 417, pp. 523–526.
Gazzarrini, S., Severino, M., Lombardi, M., Morandi, M., Difrancesco, D., Etten, J.L.V., Thiel, G., and Moroni, A., The Viral Potassium Channel Kcv: Structural and Functional Features, FEBS Lett., 2003, vol. 552, pp. 12–16.
Beckstein, O.B., Biggin, P.C., Bond, P., Bright, N., Domene, C., Grottesi, A., Holyoake, J., and Sansom, M.S.P., Ion Channel Gating: Insights via Molecular Simulation, FEBS Lett., 2003, vol. 555, pp. 85–90.
Ide, T., Takeuchi, Y., Aoki, T., and Yanagida, T., Simultaneous Optical and Electrical Recording of a Single Ion-Channel, Japan. J. Physical., 2002, vol. 52, pp. 429–434.
Rubin, A.B., Biofizika (Biophysics) (Moscow: Knizhny Dom Universitet Press, 1999), vol. 1.
Colquhoun, D. and Sigworth, F.J., Processing and Statistic Analysis of the Activity of Single Channels, Recording Single Channel Activity, Sackmann, B. and Neher, E., Eds. (Moscow: Mir Press, 1987), pp. 241–338.
Bassingthwaighte, J.B. and Raymond, G.M., Evaluating Rescaled Range Analysis for Time Series, Ann. Biomed. Eng., 1994, vol. 22, pp. 432–444.
Peng, C.-K., Buldyrev, S.V., Havlin, S., Simons, M., Stanley, H.E., and Goldberger, A.L., Mosaic Organization of DNA Nucleotides, Phys. Rev., 1994, vol. 49, pp. 1685–1689.
Kantelhardt, J.W., Zschiegner, S.A., Koscienly-Bunde, E., Bunde, A., Halvin, S., and Stanley, H.E., Multifractal Detrended Fluctuation Analysis of Nonstationary Time Series, Physica A: Stat. Mechanics Appl., 2002, vol. 316, pp. 87–114.
Hurst, H.E., Long-Term Storage: An Experimental Study, Trans. Am. Soc. Civ. Engr., 1951, vol. 116, pp. 770.
Mandelbrot, B.B. and Van Ness, J.W., Fractional Brownian Motions, Fractional Noises and Applications, Siam Rev., 1968, vol. 10, pp. 422–437.
Teich, M.C., Fractal Character of the Auditory Neural Spike Train, IEEE Trans. Biomed. Engr., 1989, vol. 36, pp. 150–160.
Karplus, M. and Mccammon, J.A., Dynamic of Proteins: Elements and Function, Ann. Rev. Biochem., 1983, vol. 52, pp. 263–300.
Monticelli, L., Robertson, K.M., Maccallum, J.L., and Tieleman, D.P., Computer Simulation of the KvAP Voltage-Gated Potassium Channel: Steered Molecular Dynamics of the Voltage Sensor, FEBS Lett., 2004, vol. 564, pp. 325–332.
Guidoni, L., Torre, V., and Carloni, P., Water and Potassium Dynamics inside the KcsA K Channel, FEBS Lett., 2000, vol. 477, pp. 37–42.
Chung, S., Allen, T.W., and Kuyucak, S., Conducting-State Properties of the KcsA Potassium Channel from Molecular and Brownian Dynamics Simulations, Biophys. J. 2002, vol. 82, pp. 628–645.
Sigg, D. and Bezanilla, F., A Physical Model of Potassium Channel Activation: From Energy Landscape to Gating Kinetics, Biophys. J., 2003, vol. 84, pp. 3703–3716.
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Original Russian Text © A.A. Grinevich, M.E. Astashev, V.N. Kazachenko, 2007, published in Biologicheskie Membrany, 2007, Vol. 24, No. 4, pp. 316–332.
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Grinevich, A.A., Astashev, M.E. & Kazachenko, V.N. Model of multifractal gating of single ionic channels in biological membranes. Biochem. Moscow Suppl. Ser. A 1, 253–269 (2007). https://doi.org/10.1134/S1990747807030099
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DOI: https://doi.org/10.1134/S1990747807030099