Skip to main content
Log in

Experimental and theoretical studies on TI+ interactions with the cation-selective channel of the sarcoplasmic reticulum

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

Summary

This paper presents an experimental study and a theoretical interpretation of the effects of thallous ion on the electrical properties of the cation-selective channel of the sarcoplasmic reticulum (SR channel). The properties of this channel in solutions which do not contain thallous ion are consistent with the predictions of Läuger's theory for singly occupied pores (P. Läuger, 1973,Biochim. Biophys. Acta 311:423–441). However, this theory does not account for SR channel properties in mixtures containing thallous ion. SR channel conductance is less than predicted in mixed salt solutions of thallium with either potassium or ammonium (J. Fox, 1983,Biochim. Biophys. Acta 736:241–245), yet is greater than expected in mixtures of lithium and thallium. In a simple single-ion pore, the ratio of the products of the single-salt binding constants and maximum conductances is equal to the permeability ratio calculated from zero-current potential experiments under near equilibrium conditions. This is not found for the SR channel when thallous ion is present. SR channel properties in the presence of thallous ion can, however, be explained by a model which postulates the existence of two external modulatory sites on the channel, without implying double-occupancy in the permeation pathway. When thallous ion is bound to a modulatory site the maximum conductance of the channel to all permeating ions is altered (thallous included). Two other models (a three-barrier, two-internal-site pore which allows multiple occupancy, and a pore with fluctuating barriers) are discussed, but are found to be unable to fit our conductance data at different concentrations.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson, O. 1975. Ion-Specificity of Gramicidin Channels.Abstruct, Int. Biophys. Congr., Copenhagen. 112

  • Ashcroft, F., Stanfield, P. 1983. The influence of the permeant ions thallous and potassium on inward rectification in frog skeletal muscle.J. Physiol. (London) 343:407–428

    Google Scholar 

  • Bell, J., Miller, C. 1983. Effects of Phospholipid Surface Charge on Ion Conduction in the K+ Channel of the Sarcoplasmic Reticulum.Fourth Biophysical Discussion (published by the Biophysical Society) pp. 223–228. Airlie House. Airlie (Virginia)

    Google Scholar 

  • Ciani, S. 1984. Coupling between fluxes in one-particle pores with fluctuating energy profiles. A theoretical study.Biophys. J. 46:249–252

    Google Scholar 

  • Ciani, S., Krasne, S., Miyazaki, S., Hagiwara, S. 1978. A model for anomalous rectification: Electrochemical-potential-dependent gating of membrane channels.J. Membrane Biol. 44:103–134

    Google Scholar 

  • Coronado, R., Miller, C. 1979. Voltage-dependent cesium blockade of a cation channel from fragmented sarcoplasmic reticulum.Nature (London) 280:807–810

    Google Scholar 

  • Coronado, R., Miller, C. 1980. Decamethonium and hexamethonium block K+ channels of the sarcoplasmic reticulum.Nature (London) 288:495–497

    Google Scholar 

  • Coronado, R., Miller, C. 1982. Conduction and block by organic cations in a K+-selective channel from sarcoplasmic reticulum incorporated into planar phospholipid bilayers.J. Gen. Physiol. 79:529–547

    Google Scholar 

  • Coronado, R., Rosenberg, R., Miller, C. 1980. Ionic selectivity, saturation, and block in a K+ channel from sarcoplasmic reticulum.J. Gen. Physiol. 76:425–446

    Google Scholar 

  • Eisenman, G., Sandblom, J., Neher, E. 1977. Ionic selectivity, saturation, binding, and block in the gramicidin A channel: A preliminary report.In: Metal-Ligand Interactions in Organic Chemistry and Biochemistry. B. Pullman and N. Goldblum. editors. Pt, 2, pp. 1–36. Reidel, Dordrecht

    Google Scholar 

  • Fox, J. 1983. Thallous ion permeation through the cation-selective channel of the sarcoplasmic reticulum: Anomalous mole fraction dependence.Biochim. Biophys. Acta 736:241–245

    Google Scholar 

  • Fox, J. 1984. Thallous ion interactions with the cation selective channel of the sarcoplasmic reticulum. Ph. D. Dissertation. U.C.L.A., Los Angeles, California

    Google Scholar 

  • Gay, L. 1981. Thallium and the potassium permeability mechanism of resting frog sartorius muscle.J. Physiol. (London) 312:39P

    Google Scholar 

  • Hagiwara, S., Eaton, D.C., Stuart, A.E., Rosenthal, N.P. 1972. Cation selectivity of the resting membrane of squid axon.J. Membrane Biol. 9:373–389

    Google Scholar 

  • Hagiwara, S., Miyazaki, S., Krasne, S., Ciani, S. 1977. Anomalous permeabilities of the egg cell membrane of starfish in K+-Tl+ mixtures.J. Gen. Physiol. 70:269–281

    Google Scholar 

  • Hagiwara, S., Takahashi, K. 1974. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell.J. Membrane Biol. 18:61–80

    Google Scholar 

  • Hamill, O.P., Marty, A., Neher, E., Sakman, B., Sigworth, F.J. 1981. Improved patch-clamp techniques for high-resolution current record from cells and cell-free membrane patches.Pfluegers Arch. 391:85–100

    Google Scholar 

  • Hille, B. 1973. Potassium channels in myelinated nerve.J. Gen. Physiol. 61:669–686

    Google Scholar 

  • Hille, B. 1975. Ionic selectivity of Na and K channels of nerve membranes.In: Membranes—A Series of Advances. G. Eisenman, editor. Vol. 3, pp. 255–323 Dekker. New York

    Google Scholar 

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

    Google Scholar 

  • Hladky, S., Urban, B., Haydon, D. 1979. Ion movements in pores formed by gramicidin A.In: Membrane Transport Processes. C. Stevens and R. Tsien, editors. pp. 89–103. Raven, New York

    Google Scholar 

  • Krasne, S., Ciani, S., Hagiwara, S., Miyazake, S. 1983. A model for ion-composition-dependent permeabilities of K+Tl+ during anomalous rectification.In: The Physiology of Excitable Cells, A. Grinnel and W. Moody, editors, pp. 83–97: Alan R. Liss. New York

    Google Scholar 

  • Labarca, P., Coronado, R., Miller, C. 1980. Thermodynamic and kinetic studies of the gating behavior of a K+-selective channel from the sarcoplasmic reticulum membrane.J. Gen. Physiol. 76:397–424

    Google Scholar 

  • Läuger, P. 1973. Ion transport through pores: A rate theory analysis.Biochim. Biophys. Acta 311:423–441

    Google Scholar 

  • Läuger, P., Stephan, W., Frehland, E. 1980. Fluctuation of barrier structure in ionic channels.Biochim. Biophys. Acta 602:167–180

    Google Scholar 

  • Miller, C. 1978. Voltage-gated cation conductance channel from fragmented sarcoplasmic reticulum: Steady-state electrical properties.J. Membrane Biol. 40:1–23

    Google Scholar 

  • Miller, C. 1982a. Feeling around inside a channel in the dark.In: Transport in Biomembranes. R. Antolini, editor. pp. 99–108. Raven, New York

    Google Scholar 

  • Miller, C. 1982b. Bis-quaternary ammonium blockers as structural probes of the sarcoplasmic reticulum K+ channel.J. Gen. Physiol. 79:869–891

    Google Scholar 

  • Miller, C. 1983. Integral membrane channels: Studies in model membranes.Physiol. Rev. 63:1209

    Google Scholar 

  • Miller, C., Racker, E. 1976. Ca++-induced fusion of fragmented sarcoplasmic reticulum with artificial planar bilayers.J. Membrane Biol. 30:283–300

    Google Scholar 

  • Miller, C., Rosenberg, R. 1979a. A voltage-gated cation conductance channel from fragmented sarcoplasmic reticulum; Effects of transition metal ions.Biochemistry 18:1138–1145

    Google Scholar 

  • Miller, C., Rosenberg, R. 1979b. Modification of a voltage-gated K+ channel from sarcoplasmic reticulum by a pronase-derived endopeptidase.J. Gen. Physiol. 74:457–478

    Google Scholar 

  • Neher, E. 1975. Ionic specificity of the gramicidin channel and the thallous ion.Biochim. Biophys. Acta 401:540–544

    Google Scholar 

  • Neher, E., Sandblom, J., Eisenman, G. 1978. Ionic selectivity, saturation, and block in gramicidin A channels. II.J. Membrane Biol. 40:97–116

    Google Scholar 

  • Robinson, R., Harned, H. 1941. Some aspects of the thermodynamics of strong electrolytes from electromotive force and vapor pressure measurements.Chem. Rev. 28:419–477

    Google Scholar 

  • Sandblom, J., Eisenman, G., Neher, E. 1977. Ionic selectivity, saturation, and block in gramicidin A channels. I. Theory for the electrical properties of ion selective channels having two pairs of binding sites and multiple conductance states.J. Membrane Biol. 31:383–417

    Google Scholar 

  • Urban, B., Hladky, S., Haydon, D. 1978. The kinetics of ion movements in the gramicidin channel.Fed. Proc. 37:2628–2632

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fox, J., Ciani, S. Experimental and theoretical studies on TI+ interactions with the cation-selective channel of the sarcoplasmic reticulum. J. Membrain Biol. 84, 9–23 (1985). https://doi.org/10.1007/BF01871644

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01871644

Key Words

Navigation