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Glial uptake system of GABA distinct from that of taurine in the bullfrog sympathetic ganglia

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Abstract

The kinetics and specificity of GABA and taurine uptake were studied in the bullfrog sympathetic ganglia. GABA uptake system consisted of simple saturable component and taurine uptake system consisted of two saturable components exclusive of non-saturable influx. Taurine unaffected GABA uptake while GABA inhibited taurine uptake competitively with theK i/Km ratio of 38. GABA (5.14 μM) uptake was inhibited by δ-aminovaleric acid and slightly by 2,4-diaminobutyric acid (5 mM, each) among ten structural analogs. Taurine uptake under high-affinity conditions was most strongly suppressed by hypotaurine and β-alanine competitively with theK i/Km ratio of 1.0 and 1.9, respectively. Autoradiography showed that glial cells were heavily labeled by both [3H]GABA and [3H]taurine. These results suggest that GABA is transported by a highly specific carrier system distinct from the taurine carrier and that taurine, hypotaurine, and β-alanine may share the same high-affinity carrier system in the glial cells of the bullfrog sympathetic ganglia.

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References

  1. Roberts, E. 1979. New directions in GABA research I: Immunocytochemical studies of GABA neurons. Pages 428–445,in Krogsgaard-Lassen, P., Scheel-Kruger, J., and Kofod, H. (eds.), GABA-neurotransmitters: pharmacochemical, biochemical and pharmacological aspects. Munksgaard, Copenhagen.

    Google Scholar 

  2. Martin, D. L. 1976. Carrier-mediated transport and removal of GABA from synaptic regions. Pages 347–386,in Roberts, E., Chase, T. N., and Tower, D. B. (eds.), GABA in nervous system function. Raven Press, New York.

    Google Scholar 

  3. Hösli, E., Hösli, L., and Schousboe, A. 1986. Amino acid uptake. Pages 133–153,in Fedoroff, S., and Vernadakis, A. (eds.), Cellular Neurobiology, vol. 2, Astrocytes, Academic Press, New York.

    Google Scholar 

  4. Shousboe, A. 1981. Transport and metabolism of glutamate and GABA in neurons and glial cells. Int. Rev. Neurobiol. 22:1–45.

    Google Scholar 

  5. Hardy, J. A., Barton, A., and Lofdahl, E., Cheetham, S. C., Johnston, G. A. R., and Dodd, P. R. 1986. Uptake of γ-aminobutyric acid and glycine by synaptosomes from postmortem human brain. J. Neurochem. 47:460–467.

    Google Scholar 

  6. Debler, E. A., and Lajtha, A. 1987. High-affinity transport of γ-aminobutyric acid, glycine, taurine,l-aspartic acid, andl-glutamic acid in synaptosomal (P2) tissue: a kinetic and substrate specificity analysis. J. Neurochem. 48:1851–1856.

    Google Scholar 

  7. Kontro, P., and Oja, S. S. 1981. Hypotaurine transport in brain slices: comparison with taurine and GABA. Neurochem. Res. 6:1179–1191.

    Google Scholar 

  8. Balcar, V. J., Mark, J., Borg, J., and Mandel, P. 1979. High-affinity uptake of γ-aminobutyric acid in cultured glial and neuronal cells. Neurochem. Res. 4:339–354.

    Google Scholar 

  9. Martin, D. L., and Shain, W. 1979. High affinity transport of taurine and β-alanine and low-affinity transport of γ-aminobutyric acid by a single transport system in cultured glioma cells. J. Biol. Chem. 254:7076–7084.

    Google Scholar 

  10. Reynolds, R., and Herschkowitz, N. 1986. Selective uptake of neuroactive amino acids by both oligodendrocytes and astrocytes in primary dissociated culture: a possible role for oligodendrocytes in neurotransmitter metabolism. Brain Res. 371:253–266.

    Google Scholar 

  11. Larsson, O. M., Griffith, R., Allen, I. C., and Schousboe, A. 1986. Mutual inhibition kinetic analysis of γ-aminobutyric acid, taurine, and β-alanine high affinity transport into neurons and astrocytes: evidence for similarity between the taurine and β-alanine carriers in both cell types. J. Neurochem. 47:426–432.

    Google Scholar 

  12. Schon, F., and Kelly, J. S. 1974. The characterization of [3]GABA uptake into the satellite glial cells of rat sensory ganglia. Brain Res. 66:289–300.

    Google Scholar 

  13. Bowery, N. G., and Brown, D. A. 1972. γ-Aminobutyric acid uptake by sympathetic ganglia. Nature 238:89–91.

    Google Scholar 

  14. Bowery, N. G., Brown, D.A., White, R. D., and Yamini, G. 1979. [3H]γ-Aminobutyric acid uptake into neuroglial cells of rat superior cervical ganglia. J. Physiol. (Lond.) 293:51–74.

    Google Scholar 

  15. Okamoto, K., Kimura, H., and Sakai, Y. 1983. Evidence for taurine as an inhibitory neurotransmitter in cerebellar stellate interncurons: selective antagonism by TAG (6-aminomethyl-3-methyl-4H, 1,2,4-benzothiadiazine-1,1-dioxide). Brain Res. 265:163–168.

    Google Scholar 

  16. Bernardi, N., Assumpcao, J. A., Dacke, C. G., and Davidoson, N. 1984. Release of labelled taurine from the rat dorsal medulla and cerebellum. Pflugers Arch. 401:193–197.

    Google Scholar 

  17. Kuriyama, K. 1980. Taurine as a neuromodulator. Fed. Proc. 39:2680–2684.

    Google Scholar 

  18. Hanretta, A. T., and Lombardini, J. B. 1987. Is taurine a hypothalamic neurotransmitter?: a model of the differential uptake and compartmentalization of taurine by neuronal and glial cell particles from the rat hypothalamus. Brain Res. Rev. 12:167–201.

    Google Scholar 

  19. Oja, S. S., and Kontro, P. 1983. Taurine. Pages 501–533,in Lajtha, A. (ed.), Handbook of neurochemistry, vol. 3, 2nd edn., Plenum Press, New York.

    Google Scholar 

  20. Holopainen, I., Kontro, P., Frey, H. J., and Oja, S. S. 1983. Taurine, hypotaurine, and GABA uptake by cultured neuroblastoma cells. J. Neurosci. Res. 10:83–92.

    Google Scholar 

  21. Lowry, O. H., Rosenbrough, N. J., Farr, A. L., and Randall, R. J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–275.

    Google Scholar 

  22. Oja, S. S., and Vahvelainen, M.-L. 1975. Transport of amino acids in brain slices. Pages 67–137,in Marks, N., and Rodnight, R. (eds.), Research Methods in Neurochemistry, vol. 3, Plenum Press, New York.

    Google Scholar 

  23. Spears, G., Sneyed, J. G. T., and Loten, E. G. 1971. A method for deriving kinetic constants for two enzymes acting on the same substrate. Biochem. J. 125:1149–1151.

    Google Scholar 

  24. Beart, P. M., Kelly, J. S., and Schon, F. 1974. γ-Aminobutyric acid in the rat peripheral nervous system, pineal and posterior pituitary. Biochem. Soc. Trans. 2:165–178.

    Google Scholar 

  25. Voaden, M. J., Marshall, J., and Murani, N. 1974. The uptake of [3H]γ-aminobutyric acid and [3H]glycine by the isolated retina of the frog. Brain Res. 67:115–132.

    Google Scholar 

  26. Davidoff, R. A., and Adair, R. 1974. High-affinity uptake of3H-gamma-aminobutyric acid into frog spinal slices. Brain Res. 76:552–556.

    Google Scholar 

  27. Iversen, L. L., and Johnston, G. A. R. 1971. GABA uptake in rat cerebral nervous system: comparison of uptake in slices and homogenates and the effects of some inhibitors J. Neurochem. 18:1939–1950.

    Google Scholar 

  28. Levi, G., Wilkin, G. P., Ciotti, M. T., and Johnstone, S. 1983. Enrichment of differentiated stellate astrocytes in cerebellar interneuron cultures as studied by GFAP immunofluorescence and autoradiographic uptake patterns with [3H]D-aspartate and [3H]GABA. Dev. Brain Res. 10:227–241.

    Google Scholar 

  29. Johnstone, S. R., Levi, G., Wilkin, G. P., Schneider, A., and Ciotti, M. T. 1986. Subpopulations of rat cerebellar astrocytes in primary culture: morphology, cell surface antigens and [3H]GABA transport. Dev. Brain Res. 24:63–75.

    Google Scholar 

  30. Reynolds, R., and Herschkowitz, N. 1984. Uptake of [3H]GABA by oligodendrocytes in dissociated brain cell culture: a combined autoradiographic and immunocytochemical study. Brain Res. 322:17–31.

    Google Scholar 

  31. Holopainen, I., and Kontro, P. 1986. High-affinity uptake of taurine and β-alanine in primary cultures of rat astrocytes. Neurochem. Res. 11:207–215.

    Google Scholar 

  32. Holopainen, I., and Kontro, P. 1985. Taurine and β-alanine uptake in primary cultures of rat astrocytes: competitive inhibition by GABA. Acta Neurol. Scand. 72:238.

    Google Scholar 

  33. Roberts, P. J. 1976. Amino acid transport in spinal and sympathetic ganglia. Pages 165–178,in Levi, G., Battistin, L., and Lajtha, A. (eds.), Transport phenomena in the nervous system: physiological and pathological aspects. Plenum Press, New York.

    Google Scholar 

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Authors and Affiliations

  1. Department of Physiology, Tokyo Medical College, 6-1-1 Shinjuku, 160, Shinjuku-ku, Tokyo, Japan

    Junko Tasaka, Saeko Sakai & Tsuneo Tosaka

  2. Department of Pathology, Tokyo Medical College, Tokyo, Japan

    Isao Yoshihama

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  1. Junko Tasaka
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  2. Saeko Sakai
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Tasaka, J., Sakai, S., Tosaka, T. et al. Glial uptake system of GABA distinct from that of taurine in the bullfrog sympathetic ganglia. Neurochem Res 14, 271–277 (1989). https://doi.org/10.1007/BF00971323

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