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Transmembrane currents in frog olfactory cilia

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Summary

We have measured transmembrane currents in intact single cilia from frog olfactory receptor neurons. A single cilium on a neuron was sucked into a patch pipette, and a high-resistance seal was formed near the base of the cilium. Action potentials could be induced by applying suction or a voltage ramp to the ciliary membrane. A transient current was seen in some cells on stimulation with odorants. After excision from the cell, most of the cilia showed increased conductance in a bath containing cAMP, indicating that the cytoplasmic face of the ciliary membrane was accessible to the bath. The estimated resistance of a single cilium was surprisingly low.

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References

  1. Adamek, G.D., Gesteland, R.C., Mair, R.G., Oakley, B. 1984. Transduction physiology of olfactory receptor cilia.Brain Res. 310:87–97

    PubMed  Google Scholar 

  2. Anderson, P.A.V., Ache, B.W. 1985. Voltage-and currentclamp recordings of the receptor potential in olfactory receptor cellsin situ.Brain Res. 338:273–280

    PubMed  Google Scholar 

  3. Anderson, P.A.V., Hamilton, K.A. 1987. Intracellular recordings from isolated salamander olfactory receptor neurons.Neuroscience 21:167–173

    PubMed  Google Scholar 

  4. Fenwick, E.M., Marty, A., Neher, E. 1982. A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine.J. Physiol. (London) 331:577–597

    Google Scholar 

  5. Firestein, S., Shepherd, G.M. 1990. Constraints on transduction mechanisms from analysis of olfactory receptor currents.Chem. Senses 14:699

    Google Scholar 

  6. Firestein, S., Werblin, F. 1989. Odor-induced membrane currents in vertebrate-olfactory receptor neurons.Science 244:79–82

    PubMed  Google Scholar 

  7. Fischmeister, R., Ayer, R.K., Jr., DeHaan, R.L. 1986. Some limitations of the cell-attached patch clamp technique: A twoelectrode analysis.Pfluegers Arch.406:73–82

    Google Scholar 

  8. Frings, S., Lindemann, B. 1988. Odorant response of isolated olfactory receptor cells is blocked by amiloride.J. Membrane Biol.105:233–243

    Google Scholar 

  9. Frings, S., Lindemann, B. 1990. Single unit recording from olfactory cilia.Biophys. J. 57:1091–1094

    PubMed  Google Scholar 

  10. Getchell, T.V. 1977. Analysis of intracellular recordings from salamander olfactory epithelium.Brain Res.123:275–286

    PubMed  Google Scholar 

  11. Graziadei, P.P.C. 1971. The olfactory mucosa of vertebrates.In: Olfaction, Handbook of Sensory Physiology. Vol. IV. L.M. Beidler editor. pp. 27–58. Springer-Verlag, Berlin

    Google Scholar 

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

    Article  Google Scholar 

  13. Kleene, S.J., Gesteland, R.C. 1990. Transmembrane currents in frog olfactory cilia.Chem. Senses (in press)

  14. Kurahashi, T. 1989. Activation by odorants of cation-selective conductance in the olfactory receptor cell isolated from the newt.J. Physiol. (London) 419:177–192

    Google Scholar 

  15. Labarca, P., Simon, S.A., Anholt R.R.H. 1988. Activation by odorants of a multistate cation channel from olfactory cilia.Proc. Natl. Acad. Sci. USA 85:944–947

    PubMed  Google Scholar 

  16. Lowe, G., Gold, G.H. 1990. Cilia are the site of olfactory transduction.Soc. Neurosci. Abstr. 16:25

    Google Scholar 

  17. Maue, R.A., Dionne, V.E. 1987. Patch-clamp studies of isolated mouse olfactory receptor neurons.J. Gen. Physiol. 90:95–125

    PubMed  Google Scholar 

  18. Mittman, S., Flaming, D.G., Copenhagen, D.R., Belgum, J.H. 1987. Bubble pressure measurement of micropipet tip outer diameter.J. Neurosci. Methods 22:161–166

    PubMed  Google Scholar 

  19. Nakamura, T., Gold, G.H. 1987. A cyclic nucleotide-gated conductance in olfactory receptor cilia.Nature (London) 325:442–444

    Google Scholar 

  20. Ottoson, D. 1956. Analysis of the electrical activity of the olfactory epithelium.Acta Physiol. Scand. Suppl. 36,122:1–83

    Google Scholar 

  21. Pace, U., Hanski, E., Salomon, Y., Lancet, D. 1985. Odorant-sensitive adenylate cyclase may mediate olfactory reception.Nature (London) 316:255–258

    Google Scholar 

  22. Reese, T.S. 1965. Olfactory cilia in the frog.J. Cell Biol. 26:209–230

    PubMed  Google Scholar 

  23. Shirley, S.G., Robinson, C.J., Dickinson, K., Aujla, R., Dodd, G.H. 1986. Olfactory adenylate cyclase of the rat: Stimulation by odorants and inhibition by Ca2+ Biochem. J. 240:605–607

    PubMed  Google Scholar 

  24. Sklar, P.B., Anholt, R.R.H., Snyder, S.H. 1986. The odorant-sensitive adenylate cyclase of olfactory receptor cells.J. Biol. Chem. 261:15538–15543

    PubMed  Google Scholar 

  25. Suzuki, N. 1977. Intracellular responses of lamprey olfactory receptors to current and chemical stimulation.In: Food Intake and Chemical Senses. Y. Katsuki, M. Sato, S.F. Takagi, and Y. Oomura, editors. pp. 13–22. Japan Scientific Societies, Tokyo

    Google Scholar 

  26. Trotier, D. 1986. A patch-clamp analysis of membrane currents in salamander olfactory receptor cells.Pfluegers Arch.407:589–595

    Google Scholar 

  27. Trotier, D. 1990. Physiology of transduction in olfaction and taste.Semin. Neurosci. 2:69–76

    Google Scholar 

  28. Trotier, D., MacLeod, P. 1983. Intracellular recordings from salamander olfactory receptor cells.Brain Res.268:225–237

    PubMed  Google Scholar 

  29. Tsien, R.Y. 1980. New calcium indicators and buffers with high selectivity against magnesium and protons: Design, synthesis, and properties of prototype structures.Biochemistry 19:2396–2404

    PubMed  Google Scholar 

  30. Vodyanoy, V., Murphy, R.B. 1983. Single-channel fluctuations in bimolecular lipid membranes induced by rat olfactory epithelial homogenates.Science 220:717–719

    PubMed  Google Scholar 

  31. Vodyanoy, V., Vodyanoy, I. 1987. ATP and GTP are essential for olfactory response.Neurosci. Lett. 73:253–258

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy and Cell Biology, University of Cincinnati, 45267-0521, Cincinnati, Ohio

    Steven J. Kleene & Robert C. Gesteland

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  1. Steven J. Kleene
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  2. Robert C. Gesteland
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Kleene, S.J., Gesteland, R.C. Transmembrane currents in frog olfactory cilia. J. Membrain Biol. 120, 75–81 (1991). https://doi.org/10.1007/BF01868593

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  • DOI: https://doi.org/10.1007/BF01868593

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