Neurochemical Research

, Volume 15, Issue 8, pp 797–804 | Cite as

Modification of chloride flux across brain membranes by inhibitory amino acids in developing and adult mice

  • S. S. Oja
  • E. R. Korpi
  • Pirjo Saransaari
Original Articles
Accepted:

Abstract

The influx of36Cl− was studied in membrane vesicles prepared from different brain regions from 3-day-old and adult mice. In both age groups the influx was enhanced about threefold by γ-aminobutyric acid (GABA), which effect was blocked by bicuculline and picrotoxin but not by baclofen, characteristic of a GABAA receptor-mediated event. In samples from the adult brain stem the GABA stimulation was smaller than in samples from the other brain regions. Most of the compounds studied apparently act at the same receptor site with the following order of efficacy: muscimol > GABA > β-alanine > hypotaurine > taurine. A number of anticonvulsant taurine derivatives were not effective and glycine only in the brain stem. The weak modulatory effects of taurine could be of significance in vivo since depolarizing stimuli release massive amounts of taurine in developing brain tissue.

Key Words

Chloride flux GABA taurine β-alanine hypoaurine development 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Krnjevic, K. 1974. Chemical nature of synaptic transmission in vertebrates. Physiol. Rev. 54:418–450.Google Scholar
  2. 2.
    Nistri, A., and Constanti, A. 1979. Pharmacological characterization of different types of GABA and glutamate receptors in vertebrates and invertebrates. Prog. Neurobiol. 13:117–235.PubMedGoogle Scholar
  3. 3.
    Oja, S. S., Kontro, P., and Lähdesmäki, P. 1977. Amino acids as inhibitory neurotransmitters. Prog. Pharmac. 1/3:1–119.Google Scholar
  4. 4.
    Cash, D. J., and Subbarao, K. 1987. γ-Aminobutyric acid (GABA) mediated transmembrane chloride flux with membrane vesicles from rat brain measured by quench flow technique: kinetic homogeneity of ion flux and receptor desensitization. Life Sci. 41:437–445.PubMedGoogle Scholar
  5. 5.
    Kardos, J., and Maderspach, K. 1987. GABAA receptor-controlled36Cl− influx in cultured rat cerebellar granule cells. Life Sci. 41:265–272.PubMedGoogle Scholar
  6. 6.
    Allan, A. M., and Harris, R. A. 1986. γ-Aminobutyric acid agonists and antagonists alter chloride flux across brain membranes. Mol. Pharmac. 29:497–505.Google Scholar
  7. 7.
    Harris, R. A., and Allan, A. M. 1985. Functional coupling of γ-aminobutyric acid receptors to chloride channels in brain membranes. Science 228:1108–1110.PubMedGoogle Scholar
  8. 8.
    Faber, D. S., and Korn, H. 1987. Voltage-dependence of glycine-activated Cl− channels: a potentiometer for inhibition? J. Neurosci. 7:807–811.PubMedGoogle Scholar
  9. 9.
    Finger, W. 1983. Effects of glycine on the grayfish neuromuscular junction. I. Glycine-operated inhibitory postsynaptic channels and a glycine-effected decrease in membrane conductance. Pflügers Arch. 397:121–127.Google Scholar
  10. 10.
    Gold, M. R., and Martin, A. R. 1984. γ-Aminobutyric acid and glycine activate Cl− channels having different characteristics in CNS neurones. Nature 308:639–641.PubMedGoogle Scholar
  11. 11.
    Hamill, O. P., Bormann, J., and Sakmann, B. 1983. Activation of multiple-conductance state chloride channels in spinal neurones by glycine and GABA. Nature 305:805–808.PubMedGoogle Scholar
  12. 12.
    Oja, S. S., and Kontro, P. 1983. Taurine. Pages 501–533, in Lajtha, A. (ed), Handbook of Neurochemistry, Vol. 3, 2nd edition, Plenum Press, New York.Google Scholar
  13. 13.
    Barker, J. L. 1985. GABA and glycine: ion channel mechanisms. Pages 71–100,in Rogawski, M. A., and Barker, J. L. (eds.), Neurotransmitter Actions in the Vertebrate Nervous System, Plenum Press, New York.Google Scholar
  14. 14.
    Choquet, D., and Korn, H. 1986. Évolution des sensibilités a la glycine, au GABA et a la β-alanine de neurones spinaux en culture. C. R. Acad. Sci., Paris 303:127–130.Google Scholar
  15. 15.
    Kontro, P., and Oja, S. S. 1987. Taurine and GABA release from mouse cerebral cortex slices: potassium stimulation releases more taurine than GABA from developing brain. Devl Brain Res. 37:277–291.Google Scholar
  16. 16.
    Kontro, P., and Oja, S. S. 1989. Release of taurine and GABA from cerebellar slices from developing and adult mice. Neuroscience 29:413–423.PubMedGoogle Scholar
  17. 17.
    Andersen, L., Sundman, L.-O., Lindén, I.-B., Kontro, P., and Oja, S. S. 1984. Synthesis and anticonvulsant properties of some 2-aminoethanesulfonic acid (taurine) derivatives. J. Pharm. Sci. 73:106–108.PubMedGoogle Scholar
  18. 18.
    Korpi, E. R., and Uusi-Oukari, M. 1989. GABAA receptor mediated chloride flux in brain homogenates from rat lines with differing innate alcohol sensitivities. Neuroscience 32:387–392.PubMedGoogle Scholar
  19. 19.
    Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–275.PubMedGoogle Scholar
  20. 20.
    Luu, M. D., Morrow, A. L., Paul, S. M., and Schwartz, R. D. 1987. Characterization of GABAA receptor-mediated36chloride uptake in rat brain synaptoneurosomes. Life Sci. 41:1277–1287.PubMedGoogle Scholar
  21. 21.
    Schwartz, R. D., Suzdak, P. D., and Paul, S. M. 1986. γ-Aminobutyric acid (GABA)- and barbiturate-mediated36Cl− uptake in rat brain synaptoneurosomes: evidence for rapid desensitization of the GABA receptor-coupled chloride ion channel. Mol. Pharmac. 30:419–426.Google Scholar
  22. 22.
    Wong, E. H. F., Leeb-Lundberg, L. M. F., Teichberg, V. I., and Olsen, R. W. 1984. γ-Aminobutyric acid activation of36Cl− flux in rat hippocampal slices and its potentiation by barbiturates. Brain Res. 303:267–275.PubMedGoogle Scholar
  23. 23.
    Thampy, K. G., and Barnes, E. M., Jr. 1984. γ-Aminobutyric acid-gated chloride channels in cultured cerebral neurons. J. Biol. Chem. 259:1753–1757.PubMedGoogle Scholar
  24. 24.
    Alger, B. E. 1985. GABA and glycine: postsynaptic actions. Pages 33–69,in Rogawski, M. A., and Barker, J. L. (eds), Neurotransmitter Actions in the Vertebrate Nervous System. Plenum Press, New York.Google Scholar
  25. 25.
    Kontro, P., Marnela, K. M., and Oja, S. S. 1984. GABA, taurine and hypotaurine in developing mouse brain. Acta Physiol. Scand. Suppl. 537:71–74.Google Scholar
  26. 26.
    Martin del Rio, R., Orensanz Munoz, L. M., and DeFeudis, F. V. 1977. Contents of β-alanine and γ-aminobutyric acid in regions of rat CNS. Expl Brain Res. 28:225–227.Google Scholar
  27. 27.
    Oja, S. S., and Kontro, P. 1989. Release of endogenous taurine and γ-aminobutyric acid from brain slices from the adult and developing mouse. J. Neurochem. 52:1018–1024.PubMedGoogle Scholar
  28. 28.
    Celentano, J. J., Gibbs, T. T., and Farb, D. H. 1988. Ethanol potentiates GABA- and glycine-induced chloride currents in chick spinal cord neurons. Brain Res. 455:377–380.PubMedGoogle Scholar
  29. 29.
    Mehta, A. K., and Ticku, M. K. 1988. Ethanol potentiation of GABAergic transmission in cultured spinal cord neurons involves γ-aminobutyric acidA-gated chloride channels. J. Pharmac. Exptl Ther. 246:558–564.Google Scholar
  30. 30.
    Malminen, O., and Kontro, P. 1986. Modulation of the GABA-benzodiazepine receptor complex by taurine in rat brain membranes. Neurochem. Res. 11:85–94.PubMedGoogle Scholar
  31. 31.
    Malminen, O., and Kontro, P. 1987. Actions of taurine on the GABA-benzodiazepine receptor complex solubilized from rat brain. Neurochem. Res. 11:113–117.Google Scholar
  32. 32.
    Namima, M., Okamoto, K., and Sakai, Y. 1983. Modulatory action of taurine on the release of GABA in cerebellar slices of the guinea pig. J. Neurochem. 40:1–9.PubMedGoogle Scholar
  33. 33.
    Malminen, O., and Korpi, E. R. 1988. GABA/benzodiazepine receptor/chloride ionophore complex in brains of rat lines selectively bred fro differences in ethanol-induced motor impairment. Alcohol 5:239–249.PubMedGoogle Scholar
  34. 34.
    Lawrence, L. J., Palmer, C. J., Gree, K. W., Wang, X., Yamamura, H. I., and Casida, J. E. 1985. t-[3H]Butylbicycloorthobenzoate: new radioligand probe for the gamma-aminobutyric acid-regulated chloride ionophore. J. Neurochem. 45:798–804.PubMedGoogle Scholar
  35. 35.
    Allan, A. M., and Harris, R. A. 1986. Anesthetic and convulsant barbiturates alter γ-aminobutyric acid-stimulated chloride flux across brain membranes. J. Pharmac. Expl Ther. 238:763–768.Google Scholar
  36. 36.
    Suzdak, P. D., Schwartz, R. D., Skolnick, P., and Paul, S. M. 1986. Ethanol stimulates γ-aminobutyric acid receptor-mediated chloride transport in rat brain synaptoneurosomes. Proc. Natl Acad. Sci. U.S.A. 83:4071–4075.PubMedGoogle Scholar
  37. 37.
    Malatynska, E., Serra, M., Ikeda, M., Biggio, G., and Yamamura, H. I. 1988. Modulation of GABA-stimulated chloride influx by β-carbolines in rat brain membrane vesicles. Brain Res. 443:395–397.PubMedGoogle Scholar
  38. 38.
    Kontro, P., Lindén, I.-B., Gothóni, G., and Oja, S. S. 1983. Novel anticonvulsant taurine derivatives. Pages 211–220,in Kuriyama, K., Huxtable, R. J., and Iwata, H. (eds.), Sulfur Amino Acids — Biochemical and Clinical Aspects, Alan R. Liss, New York.Google Scholar
  39. 39.
    Oja, S. S., Kontro, P., Lindén, I.-B., and Gothóni, G. 1983. Anticonvulsant activity of some 2-aminoethanesulphonic acid (taurine) derivatives. Eur. J. Pharmacol. 87:191–198.PubMedGoogle Scholar
  40. 40.
    Kontro, P., and Oja, S. S. 1987. Effects of the anticonvulsant taurine derivative, taltrimide, on membrane transport and binding of GABA and taurine in the mouse cerebrum. Neuropharmacology 26:19–23.PubMedGoogle Scholar
  41. 41.
    Kontro, P., and Oja, S. S. 1987. Co-operativity in sodium-independent taurine binding to brain membranes in the mouse. Neuroscience 23:567–570.PubMedGoogle Scholar
  42. 42.
    Aldinio, C., Balzano, M. A., and Toffano, G. 1980. Ontogenic development of GABA recognition sites in different brain areas. Pharmac. Res. Commun. 12:495–500.Google Scholar
  43. 43.
    Coyle, J. T., and Enna, S. J. 1976. Neurochemical aspects of the ontogenesis of GABAnergic neurons in the rat brain. Brain Res. 111:119–133.PubMedGoogle Scholar
  44. 44.
    Massotti, M., Alleva, F. R., Balazs, T., and Guidotti, A. 1980. GABA and benzodiazepine receptors in the offspring of dams receiving diazepam: ontogenetic studies. Neuropharmacology 19:951–956.PubMedGoogle Scholar
  45. 45.
    Skerritt, J. H., and Johnston, G. A. R. 1982. Postnatal developmental of GABA binding sites and their endogenous inhibitors in rat brain. Devl Neurosci. 5:189–197.Google Scholar
  46. 46.
    Kontro, P., and Oja, S. S. 1987. Taurine and GABA binding in mouse brain: effects of freezing, washing and Triton X-100 treatment on membranes. Int. J. Neurosci. 32:881–889.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1990

Authors and Affiliations

  • S. S. Oja
    • 1
  • E. R. Korpi
    • 2
  • Pirjo Saransaari
    • 1
  1. 1.Tampere Brain Research Center, Department of Biomedical SciencesUniversity of TampereTampereFinland
  2. 2.Research LaboratoriesAlko Ltd.HelsinkiFinland

Personalised recommendations