Skip to main content
SpringerLink
Log in

Effects of Tetraethylammonium on Kx Channels and Simulated Light Response in Rod Photoreceptorss

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Rod photoreceptors express a unique type of noninactivating potassium channels, Kx channels, which play an important role in setting the dark potential and participate in shaping the light response. Biophysical studies of Kx channels are limited. For example, the effects of a conventional blocker of potassium channels, tetraethylammonium (TEA), on Kx channels have not been extensively studied. Here we demonstrate that TEA blocks Kx channels, one molecule of TEA being sufficient to block the channel. Half of the Kx current was inhibited at K 0.5=5.6 mM. The TEA-induced block of Kx channels depended on extracellular potassium: the higher the potassium concentration, the stronger the block. Using TEA, we blocked potassium channels to reveal their role in shaping the simulated light response (SLR) of rods. We showed that TEA slowed down SLR and sometimes caused generation of action potentials. We developed a complete computer model of the rod, which accurately reproduced the main features of the light response and allowed us to demonstrate that it was suppression of Kx channels that was essential for slowing SLR and increasing excitability of rods. The results reported in this work further establish the importance of Kx channels in rod photoreceptor function.

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

  1. Adams, P. R., D. A. Brown, and A. Constanti. M-currents and other potassium currents in bullfrog sympathetic neurones. J. Physiol. 330:537-572, 1982.

    Google Scholar 

  2. Angstadt, J. D., and R. L. Calabrese. A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. J. Neurosci. 9:2846-2857, 1989.

    Google Scholar 

  3. Attwell, D., and M. Wilson. Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods. J. Physiol. 309:287-315, 1980.

    Google Scholar 

  4. Bader, C. R., D. Bertrand, and E. A. Schwartz. Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J. Physiol. 331:253-284, 1982.

    Google Scholar 

  5. Barnes, S., and B. Hille. Ionic channels of the inner segment of tiger salamander cone photoreceptors. J. Gen. Physiol. 94:719-743, 1989.

    Google Scholar 

  6. Baylor, D. A., G. Matthews, and B. J. Nunn. Location and function of voltage-sensitive conductances in retinal rods of the salamander, Ambystoma tigrinum. J. Physiol. 354:203-223, 1984.

    Google Scholar 

  7. Beech, D. J., and S. Barnes. Characterization of a voltage-gated K+ channel that accelerates the rod response to dim light. Neuron. 3:573-581, 1989.

    Google Scholar 

  8. Brown, D. A. M Currents. In: Ion Channels, edited by T. Narahashi. New York: Plenum, 1988, pp. 55-94.

    Google Scholar 

  9. Brown, K. T., and D. G. Flaming. Opposing effects of calcium and barium in vertebrate rod photoreceptors. Proc. Natl. Acad. Sci. U.S.A. 75:1587-1590, 1978.

    Google Scholar 

  10. Budde, T., J. A. White, and A. R. Kay. Hyperpolarization-activated Na+-K+ current (Ih) in neocortical neurons is blocked by external proteolysis and internal TEA. J. Neurophysiol. 72:2737-2742, 1994.

    Google Scholar 

  11. Corey, D. P., J. M. Dubinsky, and E. A. Schwartz. The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. J. Physiol. 354:557-575, 1984.

    Google Scholar 

  12. Demontis, G. C., B. Longoni, U. Barcaro, and L. Cervetto. Properties and functional roles of hyperpolarization-gated currents in guinea-pig retinal rods. J. Physiol. 515 ( Pt 3):813-828, 1999.

    Google Scholar 

  13. Fain, G. L., H. M. Gerschenfeld, and F. N. Quandt. Calcium spikes in toad rods. J. Physiol. 303:495-513, 1980.

    Google Scholar 

  14. Fain, G. L., and F. N. Quandt. The effects of tetraethylammonium and cobalt ions on responses to extrinsic current in toad rods. J. Physiol. 303:515-533, 1980.

    Google Scholar 

  15. Fain, G. L., F. N. Quandt, and H. M. Gerschenfeld. Calcium-dependent regenerative responses in rods. Nature 269:707-710, 1977.

    Google Scholar 

  16. Hille, B. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. J. Gen. Physiol. 50:1287-1302, 1967.

    Google Scholar 

  17. Kamiyama, Y., T. Ogura, and S. Usui. Ionic current model of the vertebrate rod photoreceptor. Vis. Res. 36:4059-4068, 1996.

    Google Scholar 

  18. Kavanaugh, M. P., M. D. Varnum, P. B. Osborne, M. J. Christie, A. E. Busch, J. P. Adelman, and R. A. North. Interaction between tetraethylammonium and amino acid residues in the pore of cloned voltage-dependent potassium channels. J. Biol. Chem. 266:7583-7587, 1991.

    Google Scholar 

  19. Kolesnikov, S. S., and A. L. Liubarskii. Potassium conductivity of the plasma membrane of frog photoreceptor cells. Biofizika 29:786-789, 1984.

    Google Scholar 

  20. Kourennyi, D. E., X. Liu, and S. Barnes. Modulation of rod photoreceptor potassium Kx current by divalent cations. Ann. Biomed. Eng. 30:1196-1203, 2002.

    Google Scholar 

  21. Kurenny, D. E., and S. Barnes. Proton modulation of M-like potassium current (IKx) in rod photoreceptors. Neurosci. Lett. 170:225-228, 1994.

    Google Scholar 

  22. Kurenny, D. E., L. L. Moroz, R. W. Turner, K. A. Sharkey, and S. Barnes. Modulation of ion channels in rod photoreceptors by nitric oxide. Neuron 13:315-324, 1994.

    Google Scholar 

  23. Kurennyi, D. E., and S. Barnes. Regulation of M-like K+ current, IKx, by Ca2 +-dependent phosphorylation in rod photoreceptors. Am. J. Physiol. 272:C1844-C1853, 1997.

    Google Scholar 

  24. Ludwig, A., X. Zong, M. Jeglitsch, F. Hofmann, and M. Biel. A family of hyperpolarization-activated mammalian cation channels. Nature 393:587-591, 1998.

    Google Scholar 

  25. MacKinnon, R., and G. Yellen. Mutations affecting TEA blockade and ion permeation in voltage-activated K+ channels. Science 250:276-279, 1990.

    Google Scholar 

  26. Malcolm, A. T., D. E. Kourennyi, and S. Barnes. Protons and calcium alter gating of the hyperpolarization-activated cation current (Ih) in rod photoreceptors. Biochim. Biophys. Acta. 1609:183-192, 2003.

    Google Scholar 

  27. Mathie, A., J. R. Wooltorton, and C. S. Watkins. Voltage-activated potassium channels in mammalian neurons and their block by novel pharmacological agents. Gen. Pharmacol. 30:13-24, 1998.

    Google Scholar 

  28. Moriondo, A., B. Pelucchi, and G. Rispoli. Calcium-activated potassium current clamps the dark potential of vertebrate rods. Eur. J. Neurosci. 14:19-26, 2001.

    Google Scholar 

  29. Ogura, T., T. O. Satoh, S. Usui, and M. Yamada. A simulation analysis on mechanisms of damped oscillation in retinal rod photoreceptor cells. Visi on Res. 43:2019-2028, 2003.

    Google Scholar 

  30. Poirazi, P., T. Brannon, and B. W. Mel. Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37:977-987, 2003.

    Google Scholar 

  31. Pongs, O. Structural basis of voltage-gated K+ channel pharmacology. Trends. Pharmacol. Sci. 13:359-365, 1992.

    Google Scholar 

  32. Solomon, J. S., and J. M. Nerbonne. Hyperpolarization-activated currents in isolated superior colliculus-projecting neurons from rat visual cortex. J. Physiol. 462:393-420, 1993.

    Google Scholar 

  33. Taglialatela, M., A. M. Vandongen, J. A. Drewe, R. H. Joho, A. M. Brown, and G. E. Kirsch. Patterns of internal and external tetraethylammonium block in four homologous K+ channels. Mol. Pharmacol. 40:299-307, 1991.

    Google Scholar 

  34. Thoreson, W. B., S. L. Stella, Jr., E. I. Bryson, J. Clements, and P. Witkovsky. D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina. Vis. Neurosci. 19:235-247, 2002.

    Google Scholar 

  35. Tian, L., and M. J. Shipston. Characterization of hyperpolarization-activated cation currents in mouse anterior pituitary, AtT20 D16:16 corticotropes. Endocrinology 141:2930-2937, 2000.

    Google Scholar 

  36. Travagli, R. A., and R. A. Gillis. Hyperpolarization-activated currents, IH and IKIR, in rat dorsal motor nucleus of the vagus neurons in vitro. J. Neurophysiol. 71:1308-1317, 1994.

    Google Scholar 

  37. Werblin, F. S. Time-and voltage-dependent ionic components of the rod response. J. Physiol. 294:613-626, 1979.

    Google Scholar 

  38. White, R. E., A. Schonbrunn, and D. L. Armstrong. Somato-statin stimulates Ca(2+)-activated K+channels through protein dephosphorylation. Nature. 351:570-573, 1991.

    Google Scholar 

  39. Wollmuth, L. P. Mechanism of Ba2+block of M-like K+ channels of rod photoreceptors of tiger salamanders. J. Gen. Physiol. 103:45-66, 1994.

    Google Scholar 

  40. Yan, K., and G. Matthews. Blockers of potassium channels reduce the outward dark current in rod photoreceptor inner segments. Vis. Neurosci. 8:479-481, 1992.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH, 44106

    Xiao-Dong Liu & Dmitri E. Kourennyi

Authors
  1. Xiao-Dong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dmitri E. Kourennyi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, XD., Kourennyi, D.E. Effects of Tetraethylammonium on Kx Channels and Simulated Light Response in Rod Photoreceptorss. Annals of Biomedical Engineering 32, 1428–1442 (2004). https://doi.org/10.1114/B:ABME.0000042230.99614.8d

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1114/B:ABME.0000042230.99614.8d

Search

Navigation