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GABA-Activated Bicarbonate Conductance

Influence on EGABA and on Postsynaptic pH Regulation
  • K. Kaila
  • J. Voipio

Abstract

γ-Aminobutyric acid (GABA) is a transmitter compound with a wide distribution and an exclusively inhibitory role in both vertebrate and invertebrate nervous systems (Gerschenfeld, 1973; Krnjević, 1974). Apart from its action on vertebrate GABAB-type receptors (see Dutar and Nicoll, 1988), the inhibitory effect of GABA is based on the opening of postsynaptic Cl channels (Boistel and Fatt, 1958; Siggins and Gruol, 1986). An increase in postsynaptic Cl conductance is also characteristic of glycine-mediated inhibition in vertebrates (Siggins and Gruol, 1986) and of acetylcholine-mediated inhibition in some invertebrate synapses (e.g., Kerkut and Thomas, 1964). The inhibitory effect of an increase in postsynaptic Cl conductance is due to the fact that in most excitable cells, the equilibrium potential of chloride is at a level more negative than the threshold for action-potential generation.

Keywords

Reversal Potential Rest Membrane Potential Anion Channel Spreading Depression Postsynaptic Membrane 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aickin, C. C., Deisz, R. A., and Lux, H. D., 1982, Ammonium action on post-synaptic inhibition in crayfish neurones: Implications for the mechanism of chloride extrusion, J. Physiol. (London) 329: 319–339.Google Scholar
  2. Alger, E., and Nicoll, R. A., 1979, GABA-mediated biphasic inhibitory responses in hippocampus, Nature 281: 315–317.PubMedCrossRefGoogle Scholar
  3. Alvarez-Leefmans, F. J., Gamino, S. M., Giraldez, F., and Nogueron, I., 1988, Intracellular chloride regulation in amphibian dorsal root ganglion neurones studied with ion-selective microelectrodes, J. Physiol. (London) 406: 225–246.Google Scholar
  4. Ammann, D., 1986, lon-Selective Microelectrodes, Springer-Verlag, Berlin.Google Scholar
  5. Araki, T., Ito, M., and Oscarsson, O., 1961, Anion permeability of the synaptic and non-synaptic motoneurone membrane, J. Physiol. (London) 159: 410–435.Google Scholar
  6. Aronson, P. S., 1985, Kinetic properties of the plasma membrane Na +-H+ exchanger, Annu. Rev. Physiol. 47: 545–560.PubMedCrossRefGoogle Scholar
  7. Atwood, H. L., 1976, Organization and synaptic physiology of crustacean neuromuscular systems, Prog. Neurobiol. 7: 291–391.PubMedCrossRefGoogle Scholar
  8. Balestrino, M., and Somjen, G. G., 1988, Concentration of carbon dioxide, interstitial pH and synaptic transmission in hippocampal formation of the rat, J. Physiol. (London) 396: 247–266.Google Scholar
  9. Ballanyi, K., and Grafe, P., 1985, An intracellular analysis of y-aminobutyric-acid associated ion movements in rat sympathetic neurones, J. Physiol. (London) 365: 41–58.Google Scholar
  10. Barker, J. L., and Ransom, B. R., 1978, Amino acid pharmacology of mammalian central neurones grown in tissue culture, J. Physiol. (London) 280: 331–354.Google Scholar
  11. Boistel, J., and Fatt, P., 1958, Membrane permeability change during inhibitory transmitter action in crustacean muscle, J. Physiol. (London) 144: 176–191.Google Scholar
  12. Bormann, J., Hamill, O. P., and Sakmann, B., 1987, Mechanism of anion permeation through channels gated by glycine and -y-aminobutyric acid in mouse cultured spinal neurones, J. Physiol. (London) 385: 243–286.Google Scholar
  13. Boron, W. F., and Russell, J. M., 1983, Stoichiometry and ion dependencies of the intracellular-pHregulating mechanism in squid giant axons, J. Gen. Physiol. 81: 373–399.PubMedCrossRefGoogle Scholar
  14. Boron, W. F., Hogan, E., and Russell, J. M., 1988, pH-sensitive activation of the intracellular-pH regulation system in squid axons by ATP-y-S, Nature 332: 262–265.Google Scholar
  15. Brodwick, M. S., and Eaton, D. C., 1978, Sodium channel inactivation in squid axon is removed by high internal pH or tyrosine-specific reagents, Science 200: 1494–1496.PubMedCrossRefGoogle Scholar
  16. Busa, W. B., 1986, Mechanisms and consequences of pH-mediated cell regulation, Annu. Rev. Physiol. 48: 389–402.PubMedCrossRefGoogle Scholar
  17. Byerly, L., Meech, R. W., and Moody, W. J., 1984, Rapidly activating hydrogen ion currents in perfused neurones of the snail Lymnaea stagnalis, J. Physiol. (London) 351: 199–216.Google Scholar
  18. Carbone, E., Testa, P. L., and Wanke, E., 1981, Intracellular pH and ionic channels in the Loligo vulgaris giant axon, Biophys. J. 35: 393–413.PubMedCrossRefGoogle Scholar
  19. Chesler, M., and Chan, C. Y., 1988, Stimulus-induced extracellular pH transients in the in vitro turtle cerebellum, Neuroscience 37: 941–948.CrossRefGoogle Scholar
  20. Chesler, M., and Kraig, R. P., 1987, Intracellular pH of astrocytes increases rapidly with cortical stimulation, Am. J. Physiol. 253: R666 - R670.PubMedGoogle Scholar
  21. Coombs, J. S., Eccles, J. C., and Fatt, P., 1955, The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential, J. Physiol. (London) 130: 326–373.Google Scholar
  22. Deisz, R. A., and Lux, H. D., 1982, The role of intracellular chloride in hyperpolarizing post-synaptic inhibition of crayfish stretch receptor neurones, J. Physiol. (London) 326: 123–138.Google Scholar
  23. Dudel, J., 1977, Voltage dependence of amplitude and time course of inhibitory synaptic current in crayfish muscle, Pfluegers Arch. 371: 167–174.CrossRefGoogle Scholar
  24. Dudel, J., and Rüdel, R., 1969, Voltage controlled contractions and current voltage relations of crayfish muscle fibers in chloride-free solutions, Pfluegers Arch. 308: 291–314.CrossRefGoogle Scholar
  25. Dudel, J., Finger, W., and Stettmeier, H., 1980, Inhibitory synaptic channels activated by -y-aminobutyric acid (GABA) in crayfish muscle, Pfluegers Arch. 387: 143–151.CrossRefGoogle Scholar
  26. Dutar, P., and Nicoll, R. A., 1988, A physiological role for GABAB receptors in the central nervous system, Nature 332: 156–158.PubMedCrossRefGoogle Scholar
  27. Eccles, J. C., 1964, The Physiology of Synapses, Springer, Berlin.CrossRefGoogle Scholar
  28. Edwards, C., 1982, The selectivity of ion channels in nerve and muscle, Neuroscience 6: 1335–1366.CrossRefGoogle Scholar
  29. Endres, W., Grafe, P., Bostock, H., and ten Bruggencate, G., 1986, Changes in extracellular pH during electrical stimulation of isolated vagus nerve, Neurosci. Lett. 64: 201–205.PubMedCrossRefGoogle Scholar
  30. Gallagher, J. P., Nakamura, J., and Shinnick-Gallagher, P., 1983, The effects of temperature, pH and CI-pump inhibitors on GABA responses recorded from cat dorsal root ganglia, Brain Res. 267: 249–259.PubMedCrossRefGoogle Scholar
  31. Galler, S., and Moser, H., 1986, The ionic mechanism of intracellular pH regulation in crayfish muscle fibres, J. Physiol. (London) 374: 137–151.Google Scholar
  32. Gerschenfeld, H. M., 1973, Chemical transmission in invertebrate central nervous systems and neuromuscular junctions, Physiol. Rev. 53: 1–119.PubMedGoogle Scholar
  33. Goldman, D. E., 1943, Potential, impedance, and rectification in membranes, J. Gen. Physiol. 27: 37–60.PubMedCrossRefGoogle Scholar
  34. Gruol, D. L., Barker, J. L., Huang, L.-Y.M., MacDonald, J. F., and Smith, T. G., 1980, Hydrogen ions have multiple effects on the excitability of cultured mammalian neurons„ Brain Res. 183: 247–252.PubMedCrossRefGoogle Scholar
  35. Gutknecht, J., and Tosteson, D. C., 1973, Diffusion of weak acids across lipid bilayer membranes: Effects of chemical reactions in the unstirred layers, Science 182: 1258–1261.PubMedCrossRefGoogle Scholar
  36. Hansen, A. J., and Zeuthen, T., 1981, Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex, Acta Physiol. Scand. 113: 437–445.PubMedCrossRefGoogle Scholar
  37. Hodgkin, A. L., and Katz, B., 1949, The effect of sodium ions on the electrical activity of the giant axon of the squid, J. Physiol. (London) 108: 37–77.Google Scholar
  38. Iles, J. F., and Jack, J. J. B., 1980, Ammonia: Assessment of its action on postsynaptic inhibition as a cause of convulsions, Brain 103: 555–578.PubMedCrossRefGoogle Scholar
  39. Ito, M., Kostyuk, P. G., and Oshima, T., 1962, Further study on anion permeability of inhibitory post-synaptic membrane of cat motoneurones, J. Physiol. (London) 164: 150–156.Google Scholar
  40. Iwasaki, S., and Florey, E., 1969, Inhibitory miniature potentials in the stretch receptor neurons of crayfish, J. Gen. Physiol. 53: 666–682.PubMedCrossRefGoogle Scholar
  41. Jack, J. J. B., Noble, D., and Tsien, R. W., 1975, Electric Current Flow in Excitable Cells, Oxford University Press ( Clarendon ), London.Google Scholar
  42. Kaila, K., 1988, GABA-activated movements of formate and acetate: Influence on intracellular pH and surface pH in crayfish skeletal muscle fibres, Ciba Found. Symp. 139: 184–186.Google Scholar
  43. Kaila, K., and Voipio, J., 1987, Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance, Nature 330: 163–165.PubMedCrossRefGoogle Scholar
  44. Kaila, K., Mattsson, K., and Voipio, J., 1989a, Fall in intracellular pH and increase in resting tension induced by a mitochondrial uncoupling agent in crayfish muscle, J. Physiol. (London) 408: 271–293.Google Scholar
  45. Kaila, K., Pasternack, M., Saarikoski, J., and Voipio, J., 1989b, Influence of GABA-gated bicarbonate conductance on potential, current and intracellular chloride in crayfish muscle fibers, J. Physiol. (London) 416: 161–181.Google Scholar
  46. Kaila, K., Saarikoski, J., and Voipio, J., 1990, Mechanism of action of GABA on intracellular pH and on surface pH in crayfish muscle fibers, (submitted).Google Scholar
  47. Katz, B., 1969, The Release of Neural Transmitter Substances, Liverpool University Press, Liverpool.Google Scholar
  48. Kelly, J. S., Kmjevie, K., Morris, M. E., and Yim, G. K. W., 1969, Anionic permeability of cortical neurones, Exp. Brain Res. 7: 11–31.PubMedCrossRefGoogle Scholar
  49. Kerkut, G. A., and Thomas, R. C., 1964, The effect of anion injection and changes in the external potassium and chloride concentration on the reversal potentials of the IPSP and acetylcholine, Comp. Biochem. Physiol. 11: 199–213.PubMedCrossRefGoogle Scholar
  50. Konnerth, A., Lux, H. D., and Morad, M., 1987, Proton-induced transformation of calcium channel in chick dorsal root ganglion cells, J. Physiol. (London) 386: 603–633.Google Scholar
  51. Kraig, R. P., Ferreira-Filho, C. S., and Nicholson, C., 1983, Alkaline and acid transients in cerebellar microenvironment, J. Neurophysiol. 49: 831–850.PubMedGoogle Scholar
  52. Krishtal, O. A., and Pidoplichko, V. 1., 1980, A receptor for protons in the nerve cell membrane, Neuroscience 5: 2325–2327.Google Scholar
  53. Krishtal, O. A., Osipchuk, Y. V., Shelest, T. N., and Smirnoff, S. V., 1987, Rapid extracellular pH transients related to synaptic transmission in rat hippocampal slices, Brain Res. 436: 352–356.PubMedCrossRefGoogle Scholar
  54. Kmjevie, K., 1974, Chemical nature of synaptic transmission in vertebrates, Physiol. Rev. 54: 418–540.Google Scholar
  55. Kuffler, S. W., and Eyzaguirre, C., 1955, Synaptic inhibition in an isolated nerve cell, J. Gen. Physiol. 39: 155–184.PubMedCrossRefGoogle Scholar
  56. Llinas, R., Baker, R., and Precht, W., 1974, Blockage of inhibition by ammonium acetate action on chloride pump in cat trochlear motoneurons, J. Neurophysiol. 37: 522–532.PubMedGoogle Scholar
  57. Lux, H. D., 1971, Ammonium and chloride extrusion: Hyperpolarizing synaptic inhibition in spinal motoneurons, Science 173: 555–557.PubMedCrossRefGoogle Scholar
  58. Lux, H. D., Loracher, C., and Neher, E., 1970, The action of ammonium on postsynaptic inhibition of cat spinal motoneurons, Exp. Brain Res. 11: 431–447.PubMedCrossRefGoogle Scholar
  59. McLaughlin, S. G. A., and Dilger, J. P., 1980, Transport of protons across membranes by weak acids, Physiol. Rev. 60: 825–863.PubMedGoogle Scholar
  60. Mahnensmith, R. L., and Aronson, P. S., 1985, The plasma membrane sodium—hydrogen exchanger and its role in physiological and pathophysiological processes, Circ. Res. 56: 773–788.PubMedCrossRefGoogle Scholar
  61. Mason, M. J., Mattsson, K., Pastemack, M., Voipio, J., and Kaila, K., 1990, Postsynaptic fall in intracellular pH and increase in surface pH caused by efflux of fornate and acetate through GABA-gated channels in crayfish muscle fibres, Neuroscience (in press).Google Scholar
  62. Meech, R. W., 1979, Membrane potential oscillations in molluscan “burster” neurones, J. Exp. Biol. 81: 93–112.PubMedGoogle Scholar
  63. Meech, R. W., and Thomas, R. C., 1987, Voltage-dependent intracellular pH in Helix aspersa neurones, J. Physiol. (London) 390: 433–452.Google Scholar
  64. Meier, P. C., Ammann, D., Morf, W. E., and Simon, W., 1980, Liquid-membrane ion-sensitive electrodes and their biomedical applications, In: Medical and Biomedical Applications of Electrochemical Devices ( J. Koryta, ed.), Wiley, New York, pp. 13–91.Google Scholar
  65. Melnik, V. I., Glebow, R. N., and Kryhanovski, G. N., 1985, ATP-dependent translocation of protons across the membrane of rat brain synaptic vesicles, Bull. Exp. Biol. Med. 99: 35–38.Google Scholar
  66. Moody, W. J., 1980, Appearance of calcium action potentials in crayfish slow muscle fibres under conditions of low intracellular pH, J. Physiol. (London) 302: 335–346.Google Scholar
  67. Moody, W. J., 1984, Effects of intracellular H+ on the electrical properties of excitable cells, Annu. Rev. Neurosci. 7: 257–278.PubMedCrossRefGoogle Scholar
  68. Motokizawa, F., Reuben, J. P., and Grundfest, H., 1969, Ionic permeability of the inhibitory postsynaptic membrane of lobster muscle fibers, J. Gen. Physiol. 54: 437–461.PubMedCrossRefGoogle Scholar
  69. Mutch, W. A. C., and Hansen, A. J., 1984, Extracellular pH changes during spreading depression and cerebral ischemia: Mechanisms of brain pH regulation, J. Cerebr. Blood Flow Metabol. 4: 17–27.CrossRefGoogle Scholar
  70. Phillips, J. M., and Nicholson, C., 1979, Anion permeability in spreading depression investigated with ion-sensitive microelectrodes, Brain Res. 173: 567–571.PubMedCrossRefGoogle Scholar
  71. Phillis, J. W., and Ochs, S., 1971, Excitation and depression of cortical neurones during spreading depression, Exp. Brain Res. 12: 132–149.PubMedCrossRefGoogle Scholar
  72. Pontén, U., and Siesjö, B. K., 1966, Gradients of CO2 tension in brain, Acta Physiol. Scand. 67: 129–140.PubMedCrossRefGoogle Scholar
  73. Raabe, W., and Gumnit, R. J., 1975, Disinhibition in cat motor cortex by ammonia, J. Neurophysiol. 38: 347–355.PubMedGoogle Scholar
  74. Rice, M. E., and Nicholson, C., 1988, Behavior of extracellular K+ and pH in skate (Raja erinacea) cerebellum, Brain Res. 461: 328–334.PubMedCrossRefGoogle Scholar
  75. Robinson, R. A., and Stokes, R. H., 1959, Electrolyte Solutions, Butterworths, London. Roos, A., and Boron, W. F., 1981, Intracellular pH, Physiol. Rev. 61: 296–433.Google Scholar
  76. Russell, J. M., 1983, Cation-coupled chloride influx in squid axon. Role of potassium and stoichiometry of the transport process, J. Gen. Physiol. 81: 909–925.PubMedCrossRefGoogle Scholar
  77. Sharp, A. P., and Thomas, R. C., 1981, The effects of chloride substitution on intracellular pH in crab muscle, J. Physiol. (London) 312: 71–80.Google Scholar
  78. Siggaard-Andersen, O., 1974, The Acid-Base Status of the Blood, 4th ed., Munskgaard, Copenhagen.Google Scholar
  79. Siggins, G. R., and Gruol, D. L., 1986, Mechanisms of transmitter action in the vertebrate central nervous system, In: Handbook of Physiology, Section I, The Nervous System, Volume IV ( F. E. Bloom, ed.), American Physiological Society, Bethesda, pp. 1–114.Google Scholar
  80. Spuler, A., Endres, W., and Grafe, P., 1987, Metabolic origin of activity-related pH-changes in mammalian peripheral and central unmyelinated fibre tracts, Pfluegers Arch. 408: R69 (abstract).Google Scholar
  81. Stadler, H., and Tsukita, S., 1984, Synaptic vesicles contain an ATP-dependent proton pump and show `knob-like’ protrusions on their surface, EMBO J. 3: 3333–3337.PubMedGoogle Scholar
  82. Sykovà, E., 1988, Extracellular pH and stimulated neurons, Ciba Found. Symp. 139: 220–235.PubMedGoogle Scholar
  83. Takeuchi, A., and Takeuchi, N., 1965, Localized action of gamma-amino butyric acid on the crayfish muscle, J. Physiol. (London) 177: 225–238.Google Scholar
  84. Takeuchi, A., and Takeuchi, N., 1967, Anion permeability of the inhibitory post-synaptic membrane of the crayfish neuromuscular junction, J. Physiol. (London) 191: 575–590.Google Scholar
  85. Takeuchi, A., and Takeuchi, N., 1969, A study of the action of picrotoxin on the inhibitory neuromuscular junction of the crayfish, J. Physiol. (London) 205: 377–391.Google Scholar
  86. Thomas, R. C., 1976, The effect of carbon dioxide on the intracellular pH and buffering power of snail neurones, J. Physiol. 255: 715–735.PubMedGoogle Scholar
  87. Thomas, R. C., 1984, Experimental displacement of intracellular pH and the mechanism of its subsequent recovery, J. Physiol. (London) 354: 3P - 22 P.Google Scholar
  88. Thomas, R. C., 1988, Changes in the surface pH of voltage-clamped snail neurones apparently caused by H+ fluxes through a channel, J. Physiol. (London) 398: 313–327.Google Scholar
  89. Thomas, R. C., and Meech, R. W., 1982, Hydrogen ion currents and intracellular pH in depolarized voltage-clamped snail neurones, Nature 299: 826–828.PubMedCrossRefGoogle Scholar
  90. Urbanics, R., Leniger-Follert, E., and Lubbers, D. W., 1978, Time course of changes of extracellular H+ and K+ activities during and after direct electrical stimulation of the brain cortex, Pfluegers Arch. 378: 47–53.CrossRefGoogle Scholar
  91. Vanheel, B., De Hemptinne, A., and Leusen, I., 1986, Influence of surface pH on intracellular pH regulation in cardiac and skeletal muscle, Am. J. Physiol. 250: C748 - C760.PubMedGoogle Scholar
  92. Voipio, J., Rydqvist, B., and Kaila, K., 1988, The reversal potential of GABA-activated current (EGABA) may be sensitive to metabolic production of CO2/HCO3, Eur. J. Neurosci. ENA-Suppl. p. 61 (abstract).Google Scholar
  93. Wanke, E., Carbone, E., and Testa, P. L., 1979, K+ conductance modified by a titratable group accessible to protons from the intracellular side of the squid axon membrane, Biophys. J. 26: 319–324.PubMedCrossRefGoogle Scholar
  94. Wanke, E., Carbone, E., and Testa, P. L., 1980, The sodium channel and intracellular H+ blockage in squid axons, Nature 287: 62–63.PubMedCrossRefGoogle Scholar
  95. Wichser, J., and Kazemi, H., 1975, CSF bicarbonate regulation in respiratory acidosis and alkalosis, J. Appl. Physiol. 38: 504–512.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • K. Kaila
    • 1
  • J. Voipio
    • 1
  1. 1.Department of Zoology, Division of PhysiologyUniversity of HelsinkiHelsinkiFinland

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