Skip to main content
SpringerLink
Log in

Correlated ion flux through parallel pores: Application to channel subconductance states

  • Articles
  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

Many ion channels that normally gate fully open or shut have recently been observed occasionally to display well-defined subconductance states with conductances much less than those of the fully open channel. One model of this behavior is a channel consisting of several parallel pores with a strong correlation between the flux in each pore such that, normally, they all conduct together but, under special circumstances, the pores may transfer to a state in which only some of them conduct. This paper introduces a general technique for modeling correlated pores, and explores in detail by computer simulation a particular model based upon electric interaction between the pores. Correlation is obtained when the transient electric field of ions passing through the pores acts upon a common set of ionizable residues of the channel protein, causing transient changes in their effective pK and hence in their charged state. The computed properties of such a correlated parallel pore channel with single occupation of each pore are derived and compared to those predicted for a single pore that can contain more than one ion at a time and also to those predicted for a model pore with fluctuating barriers. Experiments that could distinguish between the present and previous models are listed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Berry, R.M., Edmonds D.T. 1992. Carrier-like behaviour from a static but electrically responsive model pore. J. Theoret. Biol. 154:249–260

    Google Scholar 

  • Besprozvanny, I.B., Benevolensky, D.S., Naumov, A.P., 1991. Potassium channels in aortic microsomes: conductance, selectivity, barium induced blockage and subconductance states. Biochim. Biophys. Acta 1064:75–80

    Google Scholar 

  • Edmonds, D.T. 1989. A kinetic role for ionizable sites in membrane channel proteins. Eur. Biophys. J. 17:113–119

    Google Scholar 

  • Edmonds, D.T., Berry, R.M. 1991. The proton ladder, a static mechanism for ion/proton coports and counterports. Eur. Biophys. J. 20:241–245

    Google Scholar 

  • Fox, J.A. 1987. Ion channel subconductance states. J. Membrane Biol. 97:1–8

    Google Scholar 

  • Hamill, O.P., Sakmann, B. 1981. Multiple conductance states of single acetylcholine receptor channels in embryonic muscle cells. Nature 294:462–464

    Google Scholar 

  • Hille, B., Schwarz, W. 1978. Potassium channels as multi-ion single-file pores. J. Gen. Physiol. 72:409–442

    Google Scholar 

  • Hodgkin, A.L., Keynes, R.D. 1955. The potassium permeability of a giant nerve fibre. J. Physiol. 128:61–68

    Google Scholar 

  • Hunter, M., Giebisch, G. 1987. Multi-barreled K channels in renal tubules. Nature 327:522–524

    Google Scholar 

  • Klein, J.K., Meijer, P.H.E. 1954. Principle of minimum entropy production. Phys. Rev. 96:250–255

    Google Scholar 

  • Krouse, M.E., Schneider, G.T., Gage, P.W. 1986. A large anionselective channel has seven conductance levels. Nature 319:58–60

    Google Scholar 

  • Kunze, D.L., Ritchie, A.K. 1990. The DHP-sensitive calcium channel in GH3 cells exhibits multiple conductance levels. Biophys. J. 57:396a

    Google Scholar 

  • Kwok, W.M., Best, P.M. 1990. Ryanodine sensitivity and multiple conductance states of the Ca release channel from native SR membrane. Biophys. J. 57:168a

    Google Scholar 

  • Läuger, P. 1985. Ion channels with conformational substates. Biophys. J. 47:581–591

    Google Scholar 

  • Levitt, D.G. 1984. Kinetics of movement in narrow channels. Curr. Top. Membr. Transp. 21:181–197

    Google Scholar 

  • Liu, Q.Y., Meissner, G., Lai, F.A., Rousseau, E., Jones, R.V. 1989. Multiple conductance states of the purified calcium release channel complex from skeletal sarcoplasmic reticulum. Biophys. J. 55:415–424

    Google Scholar 

  • Lucchesi, K.J., Moczydlowski, E. 1991. On the interaction of bovine pancreatic trypsin inhibitor with maxi Ca2+-activated K+ channels. J. Gen Physiol. 97:1295–1319

    Google Scholar 

  • Matsuda, H., Matsuura, H., Noma, A. 1989. Triple barrel structure of inwardly rectifying K+ channels revealed by Cs+ and Rb+ block in guinea-pig heart cells. J. Physiol. 413:139–157

    Google Scholar 

  • Meves, H., Nagy, N. 1989. Multiple conductance states of the sodium channel and of other ion channels. Biochim. Biophys. Acta 988:99–105

    Google Scholar 

  • Miller, C. 1982. Open-state structure of single chloride channels from Torpedo electroplax. Philos. Trans. R. Soc. B 299:401–411

    Google Scholar 

  • Miller, C. 1991. Annus mirabilis of potassium channels. Science 252:1092–1096

    Google Scholar 

  • Neumcke, B. Läuger, P. 1969. Nonlinear electrical effects in lipid bilayer membranes. Biophys. J. 9:1160–1170

    Google Scholar 

  • Neumcke, B., Weik, R. 1988. Subconductance states of K channels in mouse muscle. Pfluegers Arch. 412 (Suppl. No. 1):R14

    Google Scholar 

  • Parsegian, V.AQ. 1969. Energy of an ion crossing a low dielectric membrane: solutions of four relevant problems. Nature 221:844–846

    Google Scholar 

  • Pottosin, I.I. 1992. Probing of pore in the Chara gymnophylla K+ channel by blocking cations and by streaming potential measurements. FEBS Lett. 298:253–256

    Google Scholar 

  • Ravindran, A., Schild, L., Moczydlowski, E. 1991. Divalent cation selectivity for external block of voltage dependent Na+ channels prolonged by Batrachotoxin. J. Gen. Physiol. 97:89–143

    Google Scholar 

  • Schlichter, L.C., Grygorczyk, R., Pahapill, P.A., Grygorczyk, C. 1990. A large multiple-conductance chloride channel in normal human T-lymphocytes. Pfluegers Arch. 416:413–421

    Google Scholar 

  • Schreibmayer, W., Tritthart, H.A., Schindler, H. 1989. The cardiac sodium channel shows a regular substate pattern indicating synchronized activity of several ion pathways instead of one. Biochim. Biophys. Acta 986:172–186

    Google Scholar 

  • Stockbridge, L.L., French, A.S., Man, S.F.P. 1991. Subconductance states in calcium-activated potassium channels from canine airway smooth muscle. Biochim. Biophys. Acta 1064:212–218

    Google Scholar 

  • Vestergaard-Bogind, B., Stampe, P., Christopherson, P. 1985. Single-file diffusion through the Ca2+-activated K+ channel of human red cells. J. Membrane Biol. 88:67–75

    Google Scholar 

  • Weik, R., Lonnendonker, U., Neumcke, B. 1989. Low-conductance states of K+ channels in adult mouse skeletal muscle. Biochim. Biophys. Acta 983:127–134

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Clarendon Laboratory, OX1 3PU, Oxford, UK

    R. M. Berry & D. T. Edmonds

Authors
  1. R. M. Berry
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. T. Edmonds
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

R.M.B. is grateful to the S.E.R.C. for the award of a graduate studentship.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berry, R.M., Edmonds, D.T. Correlated ion flux through parallel pores: Application to channel subconductance states. J. Membarin Biol. 133, 77–84 (1993). https://doi.org/10.1007/BF00231879

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00231879

Key Words

Search

Navigation