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. 1993 Apr 1;101(4):469–485. doi: 10.1085/jgp.101.4.469

Modulation of Cl-, K+, and nonselective cation conductances by taurine in olfactory receptor neurons of the mudpuppy Necturus maculosus

PMCID: PMC2216775  PMID: 7685047

Abstract

Odors are transduced by processes that modulate the membrane conductance of olfactory receptor neurons. Olfactory neurons from the aquatic salamander, Necturus maculosus, were acutely isolated without enzymes and studied with a resistive whole-cell method to minimize loss of soluble intracellular constituents. 55 of 224 neurons responded to the test compound taurine at concentrations between 10 nM and 100 microM. Four different conductance changes were elicited by taurine: an increased Cl- conductance (33%), an increased nonselective cation conductance (15%), a decreased Cl- conductance (15%), and a decreased K+ conductance (15%); in addition, responses too small to be characterized were elicited in some neurons. In most cases, taurine appeared to modulate only a single conductance in any particular cell. Modulation of each conductance was dose dependent, and each response ran down quickly in the normal whole-cell mode, presumably due to washout of a diffusible component in the transduction pathway. Modulation of taurine-sensitive conductances caused either inhibitory or excitatory responses. A similar diversity of responses in vivo would produce a complex pattern of electrical activity that could encode the identity and characteristics of an odor.

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Selected References

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  1. Arzt A. H., Silver W. L., Mason J. R., Clark L. Olfactory responses of aquatic and terrestrial tiger salamanders to airborne and waterborne stimuli. J Comp Physiol A. 1986 Apr;158(4):479–487. doi: 10.1007/BF00603794. [DOI] [PubMed] [Google Scholar]
  2. Betz H., Schmitt B., Becker C. M., Grenningloh G., Rienitz A. The vertebrate glycine receptor protein. Biochem Soc Symp. 1986;52:57–63. [PubMed] [Google Scholar]
  3. Boekhoff I., Tareilus E., Strotmann J., Breer H. Rapid activation of alternative second messenger pathways in olfactory cilia from rats by different odorants. EMBO J. 1990 Aug;9(8):2453–2458. doi: 10.1002/j.1460-2075.1990.tb07422.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bruch R. C. Signal transducing GTP-binding proteins in olfaction. Comp Biochem Physiol A Comp Physiol. 1990;95(1):27–29. doi: 10.1016/0300-9629(90)90005-d. [DOI] [PubMed] [Google Scholar]
  5. Bureau M. H., Olsen R. W. Taurine acts on a subclass of GABAA receptors in mammalian brain in vitro. Eur J Pharmacol. 1991 May 25;207(1):9–16. doi: 10.1016/s0922-4106(05)80031-8. [DOI] [PubMed] [Google Scholar]
  6. Cummings T. A., Kinnamon S. C. Apical K+ channels in Necturus taste cells. Modulation by intracellular factors and taste stimuli. J Gen Physiol. 1992 Apr;99(4):591–613. doi: 10.1085/jgp.99.4.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Derby C. D., Girardot M. N., Daniel P. C. Responses of olfactory receptor cells of spiny lobsters to binary mixtures. I. Intensity mixture interactions. J Neurophysiol. 1991 Jul;66(1):112–130. doi: 10.1152/jn.1991.66.1.112. [DOI] [PubMed] [Google Scholar]
  8. Dhallan R. S., Yau K. W., Schrader K. A., Reed R. R. Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature. 1990 Sep 13;347(6289):184–187. doi: 10.1038/347184a0. [DOI] [PubMed] [Google Scholar]
  9. Dionne V. E. Chemosensory responses in isolated olfactory receptor neurons from Necturus maculosus. J Gen Physiol. 1992 Mar;99(3):415–433. doi: 10.1085/jgp.99.3.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Døving K. B., Selset R., Thommesen G. Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiol Scand. 1980 Feb;108(2):123–131. doi: 10.1111/j.1748-1716.1980.tb06509.x. [DOI] [PubMed] [Google Scholar]
  11. Firestein S., Darrow B., Shepherd G. M. Activation of the sensory current in salamander olfactory receptor neurons depends on a G protein-mediated cAMP second messenger system. Neuron. 1991 May;6(5):825–835. doi: 10.1016/0896-6273(91)90178-3. [DOI] [PubMed] [Google Scholar]
  12. Firestein S., Zufall F., Shepherd G. M. Single odor-sensitive channels in olfactory receptor neurons are also gated by cyclic nucleotides. J Neurosci. 1991 Nov;11(11):3565–3572. doi: 10.1523/JNEUROSCI.11-11-03565.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Frings S., Lindemann B. Current recording from sensory cilia of olfactory receptor cells in situ. I. The neuronal response to cyclic nucleotides. J Gen Physiol. 1991 Jan;97(1):1–16. doi: 10.1085/jgp.97.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Frings S., Lynch J. W., Lindemann B. Properties of cyclic nucleotide-gated channels mediating olfactory transduction. Activation, selectivity, and blockage. J Gen Physiol. 1992 Jul;100(1):45–67. doi: 10.1085/jgp.100.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gesteland R. C., Lettvin J. Y., Pitts W. H. Chemical transmission in the nose of the frog. J Physiol. 1965 Dec;181(3):525–559. doi: 10.1113/jphysiol.1965.sp007781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  17. Kleene S. J., Gesteland R. C. Calcium-activated chloride conductance in frog olfactory cilia. J Neurosci. 1991 Nov;11(11):3624–3629. doi: 10.1523/JNEUROSCI.11-11-03624.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kleene S. J., Gesteland R. C. Transmembrane currents in frog olfactory cilia. J Membr Biol. 1991 Feb;120(1):75–81. doi: 10.1007/BF01868593. [DOI] [PubMed] [Google Scholar]
  19. Kontro P., Oja S. S. Interactions of taurine with GABAB binding sites in mouse brain. Neuropharmacology. 1990 Mar;29(3):243–247. doi: 10.1016/0028-3908(90)90008-f. [DOI] [PubMed] [Google Scholar]
  20. Kuhse J., Schmieden V., Betz H. A single amino acid exchange alters the pharmacology of neonatal rat glycine receptor subunit. Neuron. 1990 Dec;5(6):867–873. doi: 10.1016/0896-6273(90)90346-h. [DOI] [PubMed] [Google Scholar]
  21. Lowe G., Nakamura T., Gold G. H. Adenylate cyclase mediates olfactory transduction for a wide variety of odorants. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5641–5645. doi: 10.1073/pnas.86.14.5641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McClintock T. S., Ache B. W. Histamine directly gates a chloride channel in lobster olfactory receptor neurons. Proc Natl Acad Sci U S A. 1989 Oct;86(20):8137–8141. doi: 10.1073/pnas.86.20.8137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Michel W. C., McClintock T. S., Ache B. W. Inhibition of lobster olfactory receptor cells by an odor-activated potassium conductance. J Neurophysiol. 1991 Mar;65(3):446–453. doi: 10.1152/jn.1991.65.3.446. [DOI] [PubMed] [Google Scholar]
  24. Miyamoto T., Restrepo D., Teeter J. H. Voltage-dependent and odorant-regulated currents in isolated olfactory receptor neurons of the channel catfish. J Gen Physiol. 1992 Apr;99(4):505–529. doi: 10.1085/jgp.99.4.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nakamura T., Gold G. H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. 1987 Jan 29-Feb 4Nature. 325(6103):442–444. doi: 10.1038/325442a0. [DOI] [PubMed] [Google Scholar]
  26. Pace U., Hanski E., Salomon Y., Lancet D. Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature. 1985 Jul 18;316(6025):255–258. doi: 10.1038/316255a0. [DOI] [PubMed] [Google Scholar]
  27. Restrepo D., Miyamoto T., Bryant B. P., Teeter J. H. Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science. 1990 Sep 7;249(4973):1166–1168. doi: 10.1126/science.2168580. [DOI] [PubMed] [Google Scholar]
  28. Sicard G., Holley A. Receptor cell responses to odorants: similarities and differences among odorants. Brain Res. 1984 Feb 6;292(2):283–296. doi: 10.1016/0006-8993(84)90764-9. [DOI] [PubMed] [Google Scholar]
  29. Zufall F., Firestein S., Shepherd G. M. Analysis of single cyclic nucleotide-gated channels in olfactory receptor cells. J Neurosci. 1991 Nov;11(11):3573–3580. doi: 10.1523/JNEUROSCI.11-11-03573.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

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