Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1991 Jun;59(6):1218–1234. doi: 10.1016/S0006-3495(91)82337-2

Model for the dynamic responses of taste receptor cells to salty stimuli. I. Function of lipid bilayer membranes.

M Naito 1, N Fuchikami 1, N Sasaki 1, T Kambara 1
PMCID: PMC1281202  PMID: 1873461

Abstract

The dynamic response of the lipid bilayer membrane is studied theoretically using a microscopic model of the membrane. The time courses of membrane potential variations due to monovalent salt stimulation are calculated explicitly under various conditions. A set of equations describing the time evolution of membrane surface potential and diffusion potential is derived and solved numerically. It is shown that a rather simple membrane such as lipid bilayer has functions capable of reproducing the following properties of dynamic response observed in gustatory receptor potential. Initial transient depolarization does not occur under Ringer adaptation but does under water. It appears only for comparatively rapid flows of stimuli, the peak height of transient response is expressed by a power function of the flow rate, and the membrane potential gradually decreases after reaching its peak under long and strong stimulation. The dynamic responses in the present model arise from the differences between the time dependences in the surface potential phi s and the diffusion potential phi d across a membrane. Under salt stimulation phi d cannot immediately follow the variation in phi s because of the delay due to the charging up of membrane capacitance. It is suggested that lipid bilayer in the apical membrane is the most probable agency producing the initial phasic response to the stimulation.

Full text

PDF
1218

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akaike N., Noma A., Sato M. Electrical responses to frog taste cells to chemical stimuli. J Physiol. 1976 Jan;254(1):87–107. doi: 10.1113/jphysiol.1976.sp011223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Akaike N., Sato M. Role of anions and cations in frog taste cell stimulation. Comp Biochem Physiol A Comp Physiol. 1976;55(4A):383–391. doi: 10.1016/0300-9629(76)90066-9. [DOI] [PubMed] [Google Scholar]
  3. Avenet P., Lindemann B. Amiloride-blockable sodium currents in isolated taste receptor cells. J Membr Biol. 1988 Nov;105(3):245–255. doi: 10.1007/BF01871001. [DOI] [PubMed] [Google Scholar]
  4. Brand J. G., Teeter J. H., Silver W. L. Inhibition by amiloride of chorda tympani responses evoked by monovalent salts. Brain Res. 1985 May 20;334(2):207–214. doi: 10.1016/0006-8993(85)90212-4. [DOI] [PubMed] [Google Scholar]
  5. Cafiso D. S., Hubbell W. L. Electrogenic H+/OH- movement across phospholipid vesicles measured by spin-labeled hydrophobic ions. Biophys J. 1983 Oct;44(1):49–57. doi: 10.1016/S0006-3495(83)84276-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DeSimone J. A., Ferrell F. Analysis of amiloride inhibition of chorda tympani taste response of rat to NaCl. Am J Physiol. 1985 Jul;249(1 Pt 2):R52–R61. doi: 10.1152/ajpregu.1985.249.1.R52. [DOI] [PubMed] [Google Scholar]
  7. DeSimone J. A., Heck G. L., DeSimone S. K. Active ion transport in dog tongue: a possible role in taste. Science. 1981 Nov 27;214(4524):1039–1041. doi: 10.1126/science.7302576. [DOI] [PubMed] [Google Scholar]
  8. DeSimone J. A., Price S. A model for the stimulation of taste receptor cells by salt. Biophys J. 1976 Aug;16(8):869–881. doi: 10.1016/S0006-3495(76)85737-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deamer D. W., Nichols J. W. Proton-hydroxide permeability of liposomes. Proc Natl Acad Sci U S A. 1983 Jan;80(1):165–168. doi: 10.1073/pnas.80.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Desimone J. A., Heck G. L., Mierson S., Desimone S. K. The active ion transport properties of canine lingual epithelia in vitro. Implications for gustatory transduction. J Gen Physiol. 1984 May;83(5):633–656. doi: 10.1085/jgp.83.5.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fidelman M. L., Mierson S. Network thermodynamic model of rat lingual epithelium: effects of hyperosmotic NaCl. Am J Physiol. 1989 Sep;257(3 Pt 1):G475–G487. doi: 10.1152/ajpgi.1989.257.3.G475. [DOI] [PubMed] [Google Scholar]
  12. Formaker B. K., Hill D. L. An analysis of residual NaCl taste response after amiloride. Am J Physiol. 1988 Dec;255(6 Pt 2):R1002–R1007. doi: 10.1152/ajpregu.1988.255.6.R1002. [DOI] [PubMed] [Google Scholar]
  13. Grzesiek S., Dencher N. A. Dependency of delta pH-relaxation across vesicular membranes on the buffering power of bulk solutions and lipids. Biophys J. 1986 Aug;50(2):265–276. doi: 10.1016/S0006-3495(86)83460-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Halpern B. P., Marowitz L. A. Taste responses to lick-duration stimuli. Brain Res. 1973 Jul 27;57(2):473–478. doi: 10.1016/0006-8993(73)90152-2. [DOI] [PubMed] [Google Scholar]
  15. Halpern B. P., Tapper D. N. Taste stimuli: quality coding time. Science. 1971 Mar 26;171(3977):1256–1258. doi: 10.1126/science.171.3977.1256. [DOI] [PubMed] [Google Scholar]
  16. Hauser H., Oldani D., Phillips M. C. Mechanism of ion escape from phosphatidylcholine and phosphatidylserine single bilayer vesicles. Biochemistry. 1973 Oct 23;12(22):4507–4517. doi: 10.1021/bi00746a032. [DOI] [PubMed] [Google Scholar]
  17. Heck G. L., Erickson R. P. A rate theory of gustatory stimulation. Behav Biol. 1973 Jun;8(6):687–712. doi: 10.1016/s0091-6773(73)80112-9. [DOI] [PubMed] [Google Scholar]
  18. Heck G. L., Mierson S., DeSimone J. A. Salt taste transduction occurs through an amiloride-sensitive sodium transport pathway. Science. 1984 Jan 27;223(4634):403–405. doi: 10.1126/science.6691151. [DOI] [PubMed] [Google Scholar]
  19. Heck G. L., Persaud K. C., DeSimone J. A. Direct measurement of translingual epithelial NaCl and KCl currents during the chorda tympani taste response. Biophys J. 1989 May;55(5):843–857. doi: 10.1016/S0006-3495(89)82884-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Herness M. S. Effect of amiloride on bulk flow and iontophoretic taste stimuli in the hamster. J Comp Physiol A. 1987 Feb;160(2):281–288. doi: 10.1007/BF00609733. [DOI] [PubMed] [Google Scholar]
  21. Hill D. L., Bour T. C. Addition of functional amiloride-sensitive components to the receptor membrane: a possible mechanism for altered taste responses during development. Brain Res. 1985 Jun;352(2):310–313. doi: 10.1016/0165-3806(85)90121-x. [DOI] [PubMed] [Google Scholar]
  22. Janoff A. S., Pringle M. J., Miller K. W. Correlation of general anesthetic potency with solubility in membranes. Biochim Biophys Acta. 1981 Nov 20;649(1):125–128. doi: 10.1016/0005-2736(81)90017-1. [DOI] [PubMed] [Google Scholar]
  23. Johnson S. M., Bangham A. D. Potassium permeability of single compartment liposomes with and without valinomycin. Biochim Biophys Acta. 1969 Oct 14;193(1):82–91. doi: 10.1016/0005-2736(69)90061-3. [DOI] [PubMed] [Google Scholar]
  24. Jordan P. C. How pore mouth charge distributions alter the permeability of transmembrane ionic channels. Biophys J. 1987 Feb;51(2):297–311. doi: 10.1016/S0006-3495(87)83336-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. KIMURA K., BEIDLER L. M. Microelectrode study of taste receptors of rat and hamster. J Cell Comp Physiol. 1961 Oct;58:131–139. doi: 10.1002/jcp.1030580204. [DOI] [PubMed] [Google Scholar]
  26. Kamo N., Kashiwagura T., Kurihara K., Kobatake Y. A theory of dynamic and steady responses in chemoreception. J Theor Biol. 1980 Mar 7;83(1):111–130. doi: 10.1016/0022-5193(80)90375-6. [DOI] [PubMed] [Google Scholar]
  27. Kamo N., Miyake M., Kurihara K., Kobatake Y. Physicochemical studies of taste reception. I. Model membrane simulating taste receptor potential in response to stimuli of salts, acids and distilled water. Biochim Biophys Acta. 1974 Oct 10;367(1):1–10. doi: 10.1016/0005-2736(74)90129-1. [DOI] [PubMed] [Google Scholar]
  28. Kamo N., Miyake M., Kurihara K., Kobatake Y. Physicochemical studies of taste reception. II. Possible mechanism of generation of taste receptor potential induced by salt stimuli. Biochim Biophys Acta. 1974 Oct 10;367(1):11–23. doi: 10.1016/0005-2736(74)90130-8. [DOI] [PubMed] [Google Scholar]
  29. Kashiwagura T., Kamo N., Kurihara K., Kobatake Y. Interpretation by theoretical model of dynamic and steady components in frog gustatory response. Am J Physiol. 1980 May;238(5):G445–G452. doi: 10.1152/ajpgi.1980.238.5.G445. [DOI] [PubMed] [Google Scholar]
  30. Kashiwagura T., Kamo N., Kurihara K., Kobatake Y. Phasic and tonic components of gustatory response in the frog. Am J Physiol. 1976 Oct;231(4):1097–1104. doi: 10.1152/ajplegacy.1976.231.4.1097. [DOI] [PubMed] [Google Scholar]
  31. Kell D. B., Morris J. G. Formulation and some biological uses of a buffer mixture whose buffering capacity is relatively independent of pH in the range pH 4-9. J Biochem Biophys Methods. 1980 Sep;3(3):143–150. doi: 10.1016/0165-022x(80)90013-5. [DOI] [PubMed] [Google Scholar]
  32. Kinnamon S. C. Taste transduction: a diversity of mechanisms. Trends Neurosci. 1988 Nov;11(11):491–496. doi: 10.1016/0166-2236(88)90010-0. [DOI] [PubMed] [Google Scholar]
  33. Krishnamoorthy G., Hinkle P. C. Non-ohmic proton conductance of mitochondria and liposomes. Biochemistry. 1984 Apr 10;23(8):1640–1645. doi: 10.1021/bi00303a009. [DOI] [PubMed] [Google Scholar]
  34. Kurihara K., Kamo N., Kobatake Y. Transduction mechanism in chemoreception. Adv Biophys. 1978;10:27–95. [PubMed] [Google Scholar]
  35. Kurihara K., Yoshii K., Kashiwayanagi M. Transduction mechanisms in chemoreception. Comp Biochem Physiol A Comp Physiol. 1986;85(1):1–22. doi: 10.1016/0300-9629(86)90455-x. [DOI] [PubMed] [Google Scholar]
  36. MacDonald R. C., Simon S. A., Baer E. Ionic influences on the phase transition of dipalmitoylphosphatidylserine. Biochemistry. 1976 Feb 24;15(4):885–891. doi: 10.1021/bi00649a025. [DOI] [PubMed] [Google Scholar]
  37. MacGillivray A. D., Hare D. Applicability of Goldman's constant field assumption to biological systems. J Theor Biol. 1969 Oct;25(1):113–126. doi: 10.1016/s0022-5193(69)80019-6. [DOI] [PubMed] [Google Scholar]
  38. Mierson S., Heck G. L., DeSimone S. K., Biber T. U., DeSimone J. A. The identity of the current carriers in canine lingual epithelium in vitro. Biochim Biophys Acta. 1985 Jun 27;816(2):283–293. doi: 10.1016/0005-2736(85)90496-1. [DOI] [PubMed] [Google Scholar]
  39. Nakamura M., Kurihara K. Temperature dependence of amiloride-sensitive and -insensitive components of rat taste nerve response to NaCl. Brain Res. 1988 Mar 15;444(1):159–164. doi: 10.1016/0006-8993(88)90923-7. [DOI] [PubMed] [Google Scholar]
  40. Nichols J. W., Deamer D. W. Net proton-hydroxyl permeability of large unilamellar liposomes measured by an acid-base titration technique. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2038–2042. doi: 10.1073/pnas.77.4.2038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Nichols J. W., Hill M. W., Bangham A. D., Deamer D. W. Measurement of net proton-hydroxyl permeability of large unilamellar liposomes with the fluorescent pH probe, 9-aminoacridine. Biochim Biophys Acta. 1980 Mar 13;596(3):393–403. doi: 10.1016/0005-2736(80)90126-1. [DOI] [PubMed] [Google Scholar]
  42. Nozaki Y., Tanford C. Proton and hydroxide ion permeability of phospholipid vesicles. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4324–4328. doi: 10.1073/pnas.78.7.4324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ohki S., Kurland R. Surface potential of phosphatidylserine monolayers. II. Divalent and monovalent ion binding. Biochim Biophys Acta. 1981 Jul 20;645(2):170–176. doi: 10.1016/0005-2736(81)90187-5. [DOI] [PubMed] [Google Scholar]
  44. Ozeki M. Conductance change associated with receptor potentials of gustatory cells in rat. J Gen Physiol. 1971 Dec;58(6):688–699. doi: 10.1085/jgp.58.6.688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ozeki M., Sato M. Responses of gustatory cells in the tongue of rat to stimuli representing four taste qualities. Comp Biochem Physiol A Comp Physiol. 1972 Feb 1;41(2):391–407. doi: 10.1016/0300-9629(72)90070-9. [DOI] [PubMed] [Google Scholar]
  46. Papahadjopoulos D., Nir S., Oki S. Permeability properties of phospholipid membranes: effect of cholesterol and temperature. Biochim Biophys Acta. 1972 Jun 20;266(3):561–583. doi: 10.1016/0006-3002(72)90001-7. [DOI] [PubMed] [Google Scholar]
  47. Pike M. M., Simon S. R., Balschi J. A., Springer C. S., Jr High-resolution NMR studies of transmembrane cation transport: use of an aqueous shift reagent for 23Na. Proc Natl Acad Sci U S A. 1982 Feb;79(3):810–814. doi: 10.1073/pnas.79.3.810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sato T. An initial phasic depolarization exists in the receptor potential of taste cells. Experientia. 1977 Sep 15;33(9):1165–1167. doi: 10.1007/BF01922306. [DOI] [PubMed] [Google Scholar]
  49. Sato T., Beidler L. M. Dependence of gustatory neural response on depolarizing and hyperpolarizing receptor potentials of taste cells in the rat. Comp Biochem Physiol A Comp Physiol. 1983;75(2):131–137. doi: 10.1016/0300-9629(83)90058-0. [DOI] [PubMed] [Google Scholar]
  50. Sato T. Does an initial phasic response exist in the receptor potential of taste cells? Experientia. 1976 Nov 15;32(11):1426–1428. doi: 10.1007/BF01937414. [DOI] [PubMed] [Google Scholar]
  51. Sato T. Recent advances in the physiology of taste cells. Prog Neurobiol. 1980;14(1):25–67. doi: 10.1016/0301-0082(80)90003-9. [DOI] [PubMed] [Google Scholar]
  52. Schiffman S. S., Lockhead E., Maes F. W. Amiloride reduces the taste intensity of Na+ and Li+ salts and sweeteners. Proc Natl Acad Sci U S A. 1983 Oct;80(19):6136–6140. doi: 10.1073/pnas.80.19.6136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Shieh D. D., Ueda I., Lin H., Eyring H. Nuclear magnetic resonance studies of the interaction of general anesthetics with 1,2-dihexadecyl-sn-glycero-3-phosphorylcholine bilayer. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3999–4002. doi: 10.1073/pnas.73.11.3999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Simon S. A., Garvin J. L. Salt and acid studies on canine lingual epithelium. Am J Physiol. 1985 Nov;249(5 Pt 1):C398–C408. doi: 10.1152/ajpcell.1985.249.5.C398. [DOI] [PubMed] [Google Scholar]
  55. Smith D. V., Bealer S. L. Sensitivity of the rat gustatory system to the rate of stimulus onset. Physiol Behav. 1975 Sep;15(3):303–314. doi: 10.1016/0031-9384(75)90098-0. [DOI] [PubMed] [Google Scholar]
  56. Smith D. V., Frank M. Cross adaptation between salts in the chorda tympani nerve of the rat. Physiol Behav. 1972 Feb;8(2):213–220. doi: 10.1016/0031-9384(72)90363-0. [DOI] [PubMed] [Google Scholar]
  57. Smith R. L., Oldfield E. Dynamic structure of membranes by deuterium NMR. Science. 1984 Jul 20;225(4659):280–288. doi: 10.1126/science.6740310. [DOI] [PubMed] [Google Scholar]
  58. Sugawara M., Kashiwayanagi M., Kurihara K. Mechanism of the water response in frog gustation: possible significance of surface potential. Brain Res. 1989 May 8;486(2):269–273. doi: 10.1016/0006-8993(89)90512-x. [DOI] [PubMed] [Google Scholar]
  59. Trudell J. R. A unitary theory of anesthesia based on lateral phase separations in nerve membranes. Anesthesiology. 1977 Jan;46(1):5–10. doi: 10.1097/00000542-197701000-00003. [DOI] [PubMed] [Google Scholar]
  60. Träuble H., Eibl H. Electrostatic effects on lipid phase transitions: membrane structure and ionic environment. Proc Natl Acad Sci U S A. 1974 Jan;71(1):214–219. doi: 10.1073/pnas.71.1.214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Ueda I., Hirakawa M., Arakawa K., Kamaya H. Do anesthetics fluidize membranes? Anesthesiology. 1986 Jan;64(1):67–71. doi: 10.1097/00000542-198601000-00010. [DOI] [PubMed] [Google Scholar]
  62. Ueda I., Kamaya H. Molecular mechanisms of anesthesia. Anesth Analg. 1984 Oct;63(10):929–945. [PubMed] [Google Scholar]
  63. Vanderkooi J. M., Landesberg R., Selick H., 2nd, McDonald G. G. Interaction of general anesthetics with phospholipid vesicles and biological membranes. Biochim Biophys Acta. 1977 Jan 4;464(1):1–18. doi: 10.1016/0005-2736(77)90366-2. [DOI] [PubMed] [Google Scholar]
  64. Wang M. B., Bernard R. A. Adaptation of neural taste responses in cat. Brain Res. 1970 Jun 3;20(2):277–282. doi: 10.1016/0006-8993(70)90294-5. [DOI] [PubMed] [Google Scholar]
  65. West C. H., Bernard R. A. Intracellular characteristics and responses of taste bud and lingual cells of the mudpuppy. J Gen Physiol. 1978 Sep;72(3):305–326. doi: 10.1085/jgp.72.3.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Yokono S., Shieh D. D., Ueda I. Interfacial preference of anesthetic action upon the phase transition of phospholipid bilayers and partition equilibrium of inhalation anesthetics between membrane and deuterium oxide. Biochim Biophys Acta. 1981 Jul 20;645(2):237–242. doi: 10.1016/0005-2736(81)90194-2. [DOI] [PubMed] [Google Scholar]
  67. Yoshii K., Kiyomoto Y., Kurihara K. Taste receptor mechanism of salts in frog and rat. Comp Biochem Physiol A Comp Physiol. 1986;85(3):501–507. doi: 10.1016/0300-9629(86)90437-8. [DOI] [PubMed] [Google Scholar]
  68. Yoshii K., Kurihara K. Mechanism of the water response in carp gustatory receptors: independent generation of the water response from the salt response. Brain Res. 1983 Nov 21;279(1-2):185–191. doi: 10.1016/0006-8993(83)90177-4. [DOI] [PubMed] [Google Scholar]
  69. Yoshikawa K., Sakabe K., Matsubara Y., Ota T. Oscillation of electrical potential in a porous membrane doped with glycerol alpha-monooleate induced by an Na+/K+ concentration gradient. Biophys Chem. 1984 Aug;20(1-2):107–109. doi: 10.1016/0301-4622(84)80010-1. [DOI] [PubMed] [Google Scholar]
  70. Yoshikawa K., Sakabe K., Matsubara Y., Ota T. Self-excitation in a porous membrane doped with sorbitan monooleate (Span-80) induced by an Na+/K+ concentration gradient. Biophys Chem. 1985 Jan;21(1):33–39. doi: 10.1016/0301-4622(85)85004-3. [DOI] [PubMed] [Google Scholar]
  71. el-Mashak E. M., Tsong T. Y. Ion selectivity of temperature-induced and electric field induced pores in dipalmitoylphosphatidylcholine vesicles. Biochemistry. 1985 Jun 4;24(12):2884–2888. doi: 10.1021/bi00333a010. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES