Nonselective voltage-gated ionic channels in type II taste cells

  • R. A. Romanov
  • N. V. Kabanova
  • S. L. Malkin
  • S. S. Kolesnikov
Article
  • 25 Downloads

Abstract

In cells of different types outward voltage-gated (VG) ion currents are generally carried by potassium ions. However, in mouse type II taste cells these currents persist when K+-selective ion channels are inhibited. In this study, we examined the ion channels that provide a pathway for atypical VG outward currents in type II taste cells. These channels are found to be weakly selective and permeabile to large molecules such as NMDG, gluconate, and ATP. According to non-stationary fluctuation analysis, single channel conductance is about 200 pS. The data obtained suggest that the nonselective ion channels are similar to hemichannels formed by connexins, the gap-junction proteins, in the plasma membrane of vertebrate cells.

Key words

nonselective channels voltage-gated channels type II taste cells connexins ATP 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Murray, R.G. and Murray. A., The Anatomy and Ultrastructure of Taste Endings, Taste and Smell in Vertebrates, Wolstenholme, G.E.W., Knight, J., London, J., and Churchill, A., Eds., 1970, pp. 3–30.Google Scholar
  2. 2.
    Kinnamon, J.C., Taylor, B.G., Delay, R.J., and Roper, S.D., Ultrastructure of Mouse Taste Buds. Taste Cells and Their Associated Synapses, J. Comp. Neurol., 1985, vol. 235, pp. 48–60.PubMedCrossRefGoogle Scholar
  3. 3.
    Lindemann, B., Taste Reception, Physiol. Rev., 1996, vol. 76, pp.718–766.PubMedGoogle Scholar
  4. 4.
    Beidler, L.M. and Smallman, R.L., Renewal of Cells within Taste Buds, J. Cell. Biol., 1965, vol. 27, pp. 263–272.PubMedCrossRefGoogle Scholar
  5. 5.
    Farbman, A.I., Renewal of Taste Bud Cells in Rat Circumvallate Papillae, Cell Tissue Kinet., 1980, vol. 13, pp. 349–357.PubMedGoogle Scholar
  6. 6.
    Romanov, R.A. and Kolesnikov, S.S., Electrophysiologicaly Identified Subpopulations of Taste Bud Cells, Neurosci. Lett., 2006, vol. 395, pp. 249–254.PubMedCrossRefGoogle Scholar
  7. 7.
    Medler, K.F., Margolslee, R.F. and Kinnamon, S.C., Electrophysiological Characterization of Voltage-Gated Currents in Defined Taste Cell Types in Mice, J. Neurosci., 2003, vol. 23, pp. 2608–2617.PubMedGoogle Scholar
  8. 8.
    Romanov, R.A., Rogachevskaja, O.A., Bystrova, M.F., Jiang, P., Margolskee, R.F., and Kolesnikov, S.S., Afferent Neurotransmission Mediated by Hemichannels in Mammalian Taste Cells, EMBO J., 2007, vol. 26, pp. 657–667.PubMedCrossRefGoogle Scholar
  9. 9.
    Behe, P., Desimone, J.A., Avenet, P., and Lindemann, B., Membrane Currents in Taste Cells of the Rat Fungiform Papilla. Evidence for Two Types of Ca Currents and Inhibition of K Currents by Saccharin, J. Gen. Physiol., 1990, vol. 96, pp. 1061–1084.PubMedCrossRefGoogle Scholar
  10. 10.
    Furue, H. and Yoshii, K., In-Situ Tight-Seal Recordings of Taste Substance-Elicited Action Currents and Voltage-Gated Ba Currents from Single Taste Bud Cells in the Peeled Epithelium of Mouse Tongue, Brain. Res., 1997, vol. 776, pp. 133–139.PubMedCrossRefGoogle Scholar
  11. 11.
    Romanov, R.A., Khokhlov, A.A., and Kolesnikov, S.S., Outward Current Activated by ATP in Mouse Taste Cells, Biologicheskie Membrany, 2005, vol. 22, no. 5, pp. 390–395.Google Scholar
  12. 12.
    Kolesnikov, S.S. and Margolskee, R.F., Extracellular K+ Activates a K+- and H+-Permeable Conductance in Frog Taste Receptor Cells, J. Physiol., 1998, vol. 507, pp. 415–432.PubMedCrossRefGoogle Scholar
  13. 13.
    Hille, B., Ion Channels of Excitable Membranes, Sunderland, Massachusetts, USA, Sinauer Associates, Inc., 2001.Google Scholar
  14. 14.
    Sigworth, F.J., The Variance of Sodium Current Fluctuations at the Node of Ranvier, J. Physiol., 1980, vol. 307, pp. 97–129.PubMedGoogle Scholar
  15. 15.
    Sáez, J.C., Berthoud, V.M., Brañes, M.C., Martínez, A.D., and Beyer, E.C., Plasma Membrane Channels Formed by Connexins: Their Regulation and Functions, Physiol. Rev., 2003, vol. 83, pp. 1359–1400.PubMedGoogle Scholar
  16. 16.
    Harris, A., Connexin Channel Permeability to Cytoplasmic Molecules, Prog. Biophys. Mol. Biol., 2007, vol. 94, pp. 120–143.PubMedCrossRefGoogle Scholar
  17. 17.
    Cruciani, V. and Mikalsen, S.O., The Vertebrate Connexin Family, Cell Mol. Life Sci., 2006, vol. 63, pp. 1125–1140.PubMedCrossRefGoogle Scholar
  18. 18.
    Martin, P.E., Wall, C., and Griffith, T.M., Effects of Connexin-Mimetic Peptides on Gap Junction Functionality and Connexin Expression in Cultured Vascular Cells, Br. J. Pharmacol., 2005, vol. 144, pp. 617–627.PubMedCrossRefGoogle Scholar
  19. 19.
    Verselis, V.K. and Srinivas, M., Divalent Cations Regulate Connexin Hemichannels by Modulating Intrinsic Voltage-Dependent Gating, J. Gen. Physiol., 2008, vol. 132, pp. 315–327.PubMedCrossRefGoogle Scholar
  20. 20.
    Leybaert, L., Braet, K., Vandamme, W., Cabooter, L., Martin, P.E., and Evans, W.H., Connexin Channels, Connexin Mimetic Peptides and ATP Release, Cell Commun. Adhes., 2003, vol. 10, pp. 251–257.PubMedCrossRefGoogle Scholar
  21. 21.
    Rossier, O., Cao, J., Huque, T., Spielman, A.I., Feldman, R.S., Medrano, J.F., Brand, J.G., and Le Coutre, J., Analysis of a Human Fungiform Papillae cDNA Library and Identification of Taste-Related Genes, Chem. Senses, 2004, vol. 29, pp. 13–23.PubMedCrossRefGoogle Scholar
  22. 22.
    Kim, J.Y., Cho, S.W., Lee, M.J., Hwang, H.J., Lee, J.M., Lee, S.I., Muramatsu, T., Shimono, M., and Jung, H.S., Inhibition of Connexin 43 Alters Shh and Bmp-2 Expression Patterns in Embryonic Mouse Tongue, Cell Tissue Res., 2005, vol. 320, pp. 409–415.PubMedCrossRefGoogle Scholar
  23. 23.
    Huang, Y.J., Maruyama, Y., Dvoryanchikov, G., Pereira, E., Chaudhari, N., and Roper, S.D., The Role of Pannexin 1 Hemichannels in ATP Release and Cell-Cell Communication in Mouse Taste Buds, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 6436–6441.PubMedCrossRefGoogle Scholar
  24. 24.
    Locovei, S., Bao, L., and Dahl, G., Pannexin 1 in Erythrocytes: Function without a Gap, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 7655–7659.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2009

Authors and Affiliations

  • R. A. Romanov
    • 1
  • N. V. Kabanova
    • 1
  • S. L. Malkin
    • 1
  • S. S. Kolesnikov
    • 1
  1. 1.Institute of Cell BiophysicsRussian Academy of SciencesPushchino, Moscow oblastRussia

Personalised recommendations