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J Gen Physiol. 1992 April 1; 99(4): 591–613.
PMCID: PMC2219208

Apical K+ channels in Necturus taste cells. Modulation by intracellular factors and taste stimuli


The apically restricted, voltage-dependent K+ conductance of Necturus taste receptor cells was studied using cell-attached, inside-out and outside-out configurations of the patch-clamp recording technique. Patches from the apical membrane typically contained many channels with unitary conductances ranging from 30 to 175 pS in symmetrical K+ solutions. Channel density was so high that unitary currents could be resolved only at negative voltages; at positive voltages patch recordings resembled whole-cell recordings. These multi-channel patches had a small but significant resting conductance that was strongly activated by depolarization. Patch current was highly K+ selective, with a PK/PNa ratio of 28. Patches containing single K+ channels were obtained by allowing the apical membrane to redistribute into the basolateral membrane with time. Two types of K+ channels were observed in isolation. Ca(2+)-dependent channels of large conductance (135-175 pS) were activated in cell-attached patches by strong depolarization, with a half-activation voltage of approximately -10 mV. An ATP-blocked K+ channel of 100 pS was activated in cell-attached patches by weak depolarization, with a half-activation voltage of approximately -47 mV. All apical K+ channels were blocked by the sour taste stimulus citric acid directly applied to outside-out and perfused cell-attached patches. The bitter stimulus quinine also blocked all channels when applied directly by altering channel gating to reduce the open probability. When quinine was applied extracellularly only to the membrane outside the patch pipette and also to inside-out patches, it produced a flickery block. Thus, sour and bitter taste stimuli appear to block the same apical K+ channels via different mechanisms to produce depolarizing receptor potentials.

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Selected References

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  • Akabas MH, Dodd J, Al-Awqati Q. A bitter substance induces a rise in intracellular calcium in a subpopulation of rat taste cells. Science. 1988 Nov 18;242(4881):1047–1050. [PubMed]
  • Akabas M, Dodd J, al-Awqati Q. Identification of electrophysiologically distinct subpopulations of rat taste cells. J Membr Biol. 1990 Mar;114(1):71–78. [PubMed]
  • Ashcroft FM. Adenosine 5'-triphosphate-sensitive potassium channels. Annu Rev Neurosci. 1988;11:97–118. [PubMed]
  • Ashford ML, Sturgess NC, Trout NJ, Gardner NJ, Hales CN. Adenosine-5'-triphosphate-sensitive ion channels in neonatal rat cultured central neurones. Pflugers Arch. 1988 Aug;412(3):297–304. [PubMed]
  • Avenet P, Hofmann F, Lindemann B. Transduction in taste receptor cells requires cAMP-dependent protein kinase. Nature. 1988 Jan 28;331(6154):351–354. [PubMed]
  • Avenet P, Kinnamon SC. Cellular basis of taste reception. Curr Opin Neurobiol. 1991 Aug;1(2):198–203. [PubMed]
  • Avenet P, Lindemann B. Action potentials in epithelial taste receptor cells induced by mucosal calcium. J Membr Biol. 1987;95(3):265–269. [PubMed]
  • Avenet P, Lindemann B. Patch-clamp study of isolated taste receptor cells of the frog. J Membr Biol. 1987;97(3):223–240. [PubMed]
  • Avenet P, Lindemann B. Amiloride-blockable sodium currents in isolated taste receptor cells. J Membr Biol. 1988 Nov;105(3):245–255. [PubMed]
  • Avenet P, Lindemann B. Perspectives of taste reception. J Membr Biol. 1989 Nov;112(1):1–8. [PubMed]
  • Avenet P, Lindemann B. Noninvasive recording of receptor cell action potentials and sustained currents from single taste buds maintained in the tongue: the response to mucosal NaCl and amiloride. J Membr Biol. 1991 Oct;124(1):33–41. [PubMed]
  • Béhé P, DeSimone JA, Avenet P, 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 Nov;96(5):1061–1084. [PMC free article] [PubMed]
  • Bigiani AR, Roper SD. Mediation of responses to calcium in taste cells by modulation of a potassium conductance. Science. 1991 Apr 5;252(5002):126–128. [PubMed]
  • Bokvist K, Rorsman P, Smith PA. Block of ATP-regulated and Ca2(+)-activated K+ channels in mouse pancreatic beta-cells by external tetraethylammonium and quinine. J Physiol. 1990 Apr;423:327–342. [PubMed]
  • Cook DL, Hales CN. Intracellular ATP directly blocks K+ channels in pancreatic B-cells. Nature. 1984 Sep 20;311(5983):271–273. [PubMed]
  • Fatherazi S, Cook DL. Specificity of tetraethylammonium and quinine for three K channels in insulin-secreting cells. J Membr Biol. 1991 Mar;120(2):105–114. [PubMed]
  • Frank M. An analysis of hamster afferent taste nerve response functions. J Gen Physiol. 1973 May;61(5):588–618. [PMC free article] [PubMed]
  • Gelband CH, Silberberg SD, Groschner K, van Breemen C. ATP inhibits smooth muscle Ca2(+)-activated K+ channels. Proc Biol Sci. 1990 Oct 22;242(1303):23–28. [PubMed]
  • Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. [PubMed]
  • Hanamori T, Miller IJ, Jr, Smith DV. Gustatory responsiveness of fibers in the hamster glossopharyngeal nerve. J Neurophysiol. 1988 Aug;60(2):478–498. [PubMed]
  • Herness MS. A dissociation procedure for mammalian taste cells. Neurosci Lett. 1989 Nov 20;106(1-2):60–64. [PubMed]
  • Kinnamon SC. Taste transduction: a diversity of mechanisms. Trends Neurosci. 1988 Nov;11(11):491–496. [PubMed]
  • Kinnamon SC, Dionne VE, Beam KG. Apical localization of K+ channels in taste cells provides the basis for sour taste transduction. Proc Natl Acad Sci U S A. 1988 Sep;85(18):7023–7027. [PubMed]
  • Kinnamon SC, Roper SD. Passive and active membrane properties of mudpuppy taste receptor cells. J Physiol. 1987 Feb;383:601–614. [PubMed]
  • Kinnamon SC, Roper SD. Membrane properties of isolated mudpuppy taste cells. J Gen Physiol. 1988 Mar;91(3):351–371. [PMC free article] [PubMed]
  • Labarca P, Simon SA, Anholt RR. Activation by odorants of a multistate cation channel from olfactory cilia. Proc Natl Acad Sci U S A. 1988 Feb;85(3):944–947. [PubMed]
  • Latorre R, Miller C. Conduction and selectivity in potassium channels. J Membr Biol. 1983;71(1-2):11–30. [PubMed]
  • McBride DW, Jr, Roper SD. Ca(2+)-dependent chloride conductance in Necturus taste cells. J Membr Biol. 1991 Oct;124(1):85–93. [PubMed]
  • Miyamoto T, Okada Y, Sato T. Membrane properties of isolated frog taste cells: three types of responsivity to electrical stimulation. Brain Res. 1988 May 24;449(1-2):369–372. [PubMed]
  • Noma A. ATP-regulated K+ channels in cardiac muscle. Nature. 1983 Sep 8;305(5930):147–148. [PubMed]
  • Roper SD. The cell biology of vertebrate taste receptors. Annu Rev Neurosci. 1989;12:329–353. [PubMed]
  • Roper SD, McBride DW., Jr Distribution of ion channels on taste cells and its relationship to chemosensory transduction. J Membr Biol. 1989 Jul;109(1):29–39. [PubMed]
  • Spielman AI, Mody I, Brand JG, Whitney G, MacDonald JF, Salter MW. A method for isolating and patch-clamping single mammalian taste receptor cells. Brain Res. 1989 Dec 4;503(2):326–329. [PubMed]
  • Spruce AE, Standen NB, Stanfield PR. Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane. Nature. 1985 Aug 22;316(6030):736–738. [PubMed]
  • Striem BJ, Pace U, Zehavi U, Naim M, Lancet D. Sweet tastants stimulate adenylate cyclase coupled to GTP-binding protein in rat tongue membranes. Biochem J. 1989 May 15;260(1):121–126. [PubMed]
  • Sugimoto K, Teeter JH. Voltage-dependent ionic currents in taste receptor cells of the larval tiger salamander. J Gen Physiol. 1990 Oct;96(4):809–834. [PMC free article] [PubMed]
  • Tang JM, Wang J, Quandt FN, Eisenberg RS. Perfusing pipettes. Pflugers Arch. 1990 May;416(3):347–350. [PubMed]
  • Teeter JH, Brand JG, Kumazawa T. A stimulus-activated conductance in isolated taste epithelial membranes. Biophys J. 1990 Jul;58(1):253–259. [PubMed]
  • Tonosaki K, Funakoshi M. Cyclic nucleotides may mediate taste transduction. Nature. 1988 Jan 28;331(6154):354–356. [PubMed]
  • Wong BS. Quinidine blockade of calcium-activated potassium channels in dissociated gastric smooth muscle cells. Pflugers Arch. 1989 Aug;414(4):416–422. [PubMed]
  • Yeramian E, Trautmann A, Claverie P. Acetylcholine receptors are not functionally independent. Biophys J. 1986 Aug;50(2):253–263. [PubMed]

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