Ion Channel Electrostatics and the Shapes of Channel Proteins

  • Peter C. Jordan

Abstract

The accelerating progress that is being made in channel reconstitution will eventually lead to the determination of protein structures, i.e., of channel shapes. These will surely not all be right circular cylinders, and a pore’s structure can affect ion passage through it in two ways. Short-range forces govern selectivity and the detailed nature of the potential energy profile for ion permeation. Long-range electrostatic forces control ion access to the channel, influence the relationship of apparent electrical distance to structure, and provide a slowly varying background potential, which modifies channel kinetics.

Keywords

Channel Protein Potential Profile Mouth Region Image Energy Double Occupancy 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Almers, W., and McCleskey, E. W., 1984, Non-selective conductance in calcium channels of frog muscle: Calcium selectivity in a single-file pore, J. Physiol. (Lond.) 353:585-608.Google Scholar
  2. Andersen, O. S., 1978, Ion transport across simple membranes, in: Renal Function (G. H. Giebiseh and E. F. Purcell, eds.), pp. 71–99, Josiah Macy Foundation, New York.Google Scholar
  3. Andersen, O. S., 1983, Ion movement through gramicidin A channels. Studies on the diffusion controlled association step, Biophys. J. 41:147–165.PubMedCrossRefGoogle Scholar
  4. Andersen, O. S., Finkelstein, A., Katz, I., and Cass, A., 1976, Effect of phloretin on the permeability of thin lipid membranes, J. Gen. Physiol. 67:749–771.PubMedCrossRefGoogle Scholar
  5. Armstrong, C. M., 1975, Ionic pores, gates and gating currents, Q. Rev. Biophys. 7:179–210.CrossRefGoogle Scholar
  6. Armstrong, C. M., and Taylor, S., 1980, Interaction of barium ions with potassium channels in squid giant axons, Biophys. J. 30:473–488.PubMedCrossRefGoogle Scholar
  7. Bamberg, E., and Läuger, P., 1977, Blocking of the gramicidin channel by divalent cations, J. Membr. Biol. 35:351–375.CrossRefGoogle Scholar
  8. Bamberg, E., Noda, K., Gross, E., and Lauger, P., 1976, Single channel parameters of gramicidin A, B and C., Biochim. Biophys. Acta 418:223–228.Google Scholar
  9. Benz, R., Ishii, J., and Takae, T., 1980, Determination of ion permeability through channels made of porins from the outer membrane of Salmonella typhimurium in lipid bilayer membranes, J. Membr. Biol. 56:19–29.PubMedCrossRefGoogle Scholar
  10. Coronado, R., Rosenberg, R. L., and Miller, C., 1980, Ionic selectivity, saturation and block in a K channel from sarcoplasmic reticulum, J. Gen. Physiol. 76:425–446.PubMedCrossRefGoogle Scholar
  11. French, R. J., and Shoukimas, J. J., 1981, Blockage of squid axon potassium conductance by internal tetra-N-alkylammonium ions of various sizes, Biophys. J. 34:271–292.PubMedCrossRefGoogle Scholar
  12. Getzoff, E. D., and Tainer, J. A., 1986, Superoxide dismutase as a model ion channel, in: Ion Channel Reconstitution (C. M. Miller, ed.), pp. 57-73, Plenum Press, New York.Google Scholar
  13. Getzoff, E. D., Tainer, J. A., Weiner, P. K., Kollman, P. A. Richardson, J. S., and Richardson, D. C., 1983, Electrostatic recognition between Superoxide and copper, zinc Superoxide dismutase, Nature 306:287–290.PubMedCrossRefGoogle Scholar
  14. Hagiwara, S., and Byerly, L. A., 1981, Calcium channel, Annu. Rev. Neurosci. 4:69–125.PubMedCrossRefGoogle Scholar
  15. Heitz, F., Spach, F., and Trudelle, Y., 1982, Single channels of 9,11,13,15-destryptophyl-phenalanyl gramicidin A, Biophys. J. 40:87–89.PubMedCrossRefGoogle Scholar
  16. Heitz, F., Spach, F., and Trudelle, Y., 1984, Single channels of various gramicidins. Voltage effects, Biophys. J. 45:97-99.Google Scholar
  17. Hess, P., and Tsien, P. W., 1984, Mechanism of ion permeation through calcium channels, Nature 309:453–456.PubMedCrossRefGoogle Scholar
  18. Hille, B., 1975, Ionic selectivity of Na and K channels of nerve membranes, in: Membranes, Vol. 3 (G. Eisenman, ed.), pp. 255-323, Marcel Dekker, New York.Google Scholar
  19. Hille, B., and Schwartz, E., 1978, Potassium channels as multi-ion single-file pores, J. Gen. Physiol. 72:409–442.PubMedCrossRefGoogle Scholar
  20. Hladky, S. B., and Haydon, D. A., 1973, Membrane conductance and surface potential, Biochim. Biophys. Acta 318:464–468.CrossRefGoogle Scholar
  21. Jordan, P. C., 1981, Energy barriers for the passage of ions through channels. Exact solution of two electrostatic problems, Biophys. Chem. 13:203–212.PubMedCrossRefGoogle Scholar
  22. Jordan, P. C., 1982, Electrostatic modeling of ion pores. Energy barriers and electric field profiles, Biophys. J. 39:157–164.PubMedCrossRefGoogle Scholar
  23. Jordan, P. C., 1983, Electrostatic modeling of ion pores. II. Effects attributable to the membrane dipole potential, Biophys. J. 41:189–195.PubMedCrossRefGoogle Scholar
  24. Jordan, P. C., 1984a, The total electrostatic potential in a gramicidin channel, J. Membr. Biol. 78:91–102.CrossRefGoogle Scholar
  25. Jordan, P. C., 1984b, The effect of pore structure on energy barriers and applied voltage profiles. I. Symmetrical channels, Biophys. J. 45:1091–1100.PubMedCrossRefGoogle Scholar
  26. Jordan, P. C., 1984c, The effect of pore structure on energy barriers and applied voltage profiles. II. Unsymmetrical channels, Biophys. J. 45:1101–1107.PubMedCrossRefGoogle Scholar
  27. Kirkwood, J. G., 1939, The dielectric polarization of polar liquids, J. Chem. Phys. 7:911–919.CrossRefGoogle Scholar
  28. Kistler, J., and Stroud, R. M., 1981, Crystalline arrays of membrane-bound acetylcholine receptor, Proc. Natl. Acad. Sci. U.S.A. 78:3678–3682.PubMedCrossRefGoogle Scholar
  29. Koeppe, R. C., Hodgson, K. O., and Stryer, L., 1978, Helical channels in crystals of gramicidin A and of a cesium-gramicidin A complex: An X-ray diffraction study, J. Mol. Biol. 121:41–54.PubMedCrossRefGoogle Scholar
  30. Latorre, R., and Miller, C., 1983, Conduction and selectivity in potassium channels, J. Membr. Biol. 71:11–30.PubMedCrossRefGoogle Scholar
  31. Latorre, R., Vergara, C., and Hildalgo, C., 1982, Reconstitution in planar lipid bilayers of a Ca2+ — dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle, Proc. Natl. Acad. Sci. U.S.A. 79:805–809.PubMedCrossRefGoogle Scholar
  32. Läuger, P., 1976, Diffusion-limited ion flow through pores, Biochim. Biophys. Acta 455:493–509.PubMedCrossRefGoogle Scholar
  33. Lee, W. K., and Jordan, P. C., 1984, Molecular dynamics simulation of cation motion in water-filled, gramicidin-like pores, Biophys. J. 46:805–819.PubMedCrossRefGoogle Scholar
  34. Levitt, D. G., 1978, Electrostatic calculations for an ion channel. I. Energy and potential profiles and interaction between ions, Biophys. J. 22:209–219.PubMedCrossRefGoogle Scholar
  35. Lewis, C. A., and Stevens, C. F., 1979, Mechanism of ion permeation through channels in a post-synaptic membrane, in: Membrane Transport Processes Vol. 3 (C. F. Stevens and R. W. Tsien, eds.), pp. 133–151, Raven Press, New York.Google Scholar
  36. MacKay, D. H. J., Berens, P., Wilson, K. R., and Hagler, A. T., 1984, Structure and dynamics of ion transport through gramicidin A, Biophys. J. 46:229–248.PubMedCrossRefGoogle Scholar
  37. Maynard, T., Edwards, C., and Anraku, M., 1977, Permeability of the endplate membrane activated by acetylcholine to some organic cations, J. Neurobiol. 8:173–184.CrossRefGoogle Scholar
  38. Miller, C., 1982, Feeling around inside a channel in the dark, in: Transport in Biological Membranes (R. Antolini, ed.), pp. 99–108, Raven Press, New York.Google Scholar
  39. Parsigian, V. A., 1969, Energy of an ion crossing a low dielectric membrane: Solution to four relevant electrostatic problems, Nature 221:844–846.CrossRefGoogle Scholar
  40. Pickar, A.D., and Benz, R., 1978, Transport of oppositely charged lipophilic ion probes in lipid bilayers having various structures, J. Membr. Biol. 44:353–376.CrossRefGoogle Scholar
  41. Schulz, L. E., and Schirmer, R. H., 1978, Principles of Protein Structure, p. 30, Springer, New York.Google Scholar
  42. Swenson, R. P., Jr., 1981, Inactivation of potassium current in squid axon by a variety of quaternary ammonium ions, J. Gen. Physiol. 77:255-271.Google Scholar
  43. Urry, D. W., 1971, The gramicidin A transmembrane channel: A proposed πl, d helix, Proc. Natl. Acad. Sci. U.S.A. 68:672–676.PubMedCrossRefGoogle Scholar
  44. Urry, D. W., Venkatachalam, C. M., Spisni, A., Bradley, R. J., Trapani, T. L., and Prasad, K. U., 1980a, The malonyl gramicidin channel: NMR-derived rate constants and comparison of calculated and experimental single-channel currents, J. Membr. Biol. 55:29–51.PubMedCrossRefGoogle Scholar
  45. Urry, D. W., Venkatachalam, C. M., Spisni, A., Lauger, P., and Khalid, M. A., 1980b, Rate theory calculation of gramicidin single channel currents using NMR-derived rate constants, Proc. Natl. Acad. Sci. U.S.A. 77:2028–2032.PubMedCrossRefGoogle Scholar
  46. Vergara, C., and Latorre, R., 1983, Kinetics of Ca2+-activated K+ channels from rabbit muscle incorporated into planar bilayers: Evidence for a Ca2+ and Ba2+ blockade, J. Gen. Physiol. 82:543–568.PubMedCrossRefGoogle Scholar
  47. Wall, F. T., 1974, Chemical Thermodynamics, ed. 3, W. H. Freeman, San Francisco.Google Scholar

Copyright information

© Springer Science+Business Media New York 1986

Authors and Affiliations

  • Peter C. Jordan
    • 1
  1. 1.Department of ChemistryBrandeis UniversityWalthamUSA

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