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Sodium dependency of GABA uptake into glial cells in bullfrog sympathetic ganglia

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Abstract

The kinetics of sodium dependency of GABA uptake by satellite glial cells was studied in bullfrog sympathetic ganglia. GABA uptake followed simple Michaelis-Menten kinetics at all sodium concentrations tested. Increasing external sodium concentration increased bothK m andV max for GABA uptake, with an increase in theV max/K m ratio. The initial rate of uptake as a function of the sodium concentration exhibited sigmoid shape at 100 μM GABA. Hill number was estimated to be 2.0. Removal of external potassium ion or 10 μM ouabain reduced GABA uptake time-dependently. The effect of ouabain was potentiated by 100 μM veratrine. These results suggest that at least two sodium ions are involved with the transport of one GABA molecule and that sodium concentration gradient across the plasma membrane is the main driving force for the transport of GABA. The essential sodium gradient may be maintained by Na+, K+-ATPase acting as an ion pump.

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References

  1. Jessen, K. R., Mirsky, R., Dennison, M. E., and Burnstock, G. 1979. GABA may a neurotransmitter in the vertebrate peripheral nervous system. Nature 281:71–74.

    PubMed  Google Scholar 

  2. Kerr, D. I. B., and Krantis, A. 1983. Uptake and stimulus-evoked release of3H-gamma-aminobutyric acid by myenteric plexus. Br. J. Pharmacol. 78:271–276.

    PubMed  Google Scholar 

  3. Ong, J., and Kerr, D. I. B. 1984. GABAa and GABAb-receptor mediated modification of intestinal motility. Eur. J. Pharmacol. 86:9–17.

    Google Scholar 

  4. Kusunoki, M., Taniyama, K., and Tanaka, C. 1984. Neuronal GABA release and GABA inhibition of ACh release in guinea pig urinary bladder. Am. J. Physiol. 246:R502-R509.

    PubMed  Google Scholar 

  5. Saito, N., Taniyama, K., and Tanaka, C. 1985. Uptake and release of γ-aminobutyric acid in guinea pig gallbladder. Am. J. Physiol. 247:G192-G196.

    Google Scholar 

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

    Google Scholar 

  7. 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 

  8. Larsson, O. M., Griffiths, 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.

    PubMed  Google Scholar 

  9. Hardy, J. A., Barton, A., Lofdahl, E., Cheeyham, 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.

    PubMed  Google Scholar 

  10. Wood, J. D., and Sidhu, H. S. 1986. Uptake of γ-aminobutyric acid by brain tissue preparations: A reevaluation. J. Neurochem. 46:739–744.

    PubMed  Google Scholar 

  11. Wood, J. D., and Sidhu, H. S. 1987. A comparative study and partial characterization of multi-uptake systems for γ-aminobutyric acid. J. Neurochem. 49:1202–1208.

    PubMed  Google Scholar 

  12. Seidman, B. C., and Verity, N. A. 1987. Selective inhibition of synaptosomal γ-aminobutyric acid uptake by triethyllead: role of energy transduction and chloride ion. J. Neurochem. 48:1142–1149.

    PubMed  Google Scholar 

  13. Debler, E. A., and Lajtha, A. 1987. High-affinity transport of γ-aminobutyric acid, glycine, taurine, L-aspartic acid, and L-glutamic acid in synaptosomal (P2) tissue: a kinetic and substrate specificity analysis. J. Neurochem. 47:460–467.

    Google Scholar 

  14. Fykse, E. M., and Fonnum, F. 1988. Uptake of γ-aminobutyric acid by a synaptic vesicle fraction isolated rat brain. J. Neurochem. 50:1237–1241.

    PubMed  Google Scholar 

  15. Hertz, L., Wu, P. H., and Schousboe, A. 1978. Evidence for net uptake of GABA into mouse astrocytes in primary cultures — its sodium dependence and potassium independence. Neurochem. Res. 3:313–323.

    Google Scholar 

  16. Larsson, O. M., Hertz, L., and Schousboe, A. 1980. GABA uptake in astrocytes in primary cultures: coupling with two sodium ions. J. Neurosci. Res. 5:469–477.

    PubMed  Google Scholar 

  17. Drejer, J., Meier, E., and Schousboe, A. 1983. Novel neuron-related regulatory mechanisms for astrocytic glutamate and GABA high-affinity uptake. Neurosci. Lett. 37:301–306.

    PubMed  Google Scholar 

  18. Wilkin, G. P., Levi, G., Johnstone, S. R., and Riddle, P. N. 1983. Cerebellar astroglial cells in primary culture: expression of different morphological appearances and different ability to take up [3H]d-aspartate and [3H]GABA. Dev. Brain Res. 10:265–277.

    Google Scholar 

  19. Hansson, E., Isacsson, H., and Sellström, Å. 1984. Characteristics of dopamine and GABA transport in primary cultures of astroglial cells. Acta Physiol. Scand. 121:333–341.

    PubMed  Google Scholar 

  20. 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.

    PubMed  Google Scholar 

  21. Reynolds, R., and Herschkowitz, N. 1987. Oligodendroglial and astroglial heterogeneity in mouse primary central nervous system culture as demonstrated by differences in GABA and D-aspartate transport and immuno-cytochemistry. Dev. Brain Res. 36:13–25.

    Google Scholar 

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

    PubMed  Google Scholar 

  23. Gavrilovic, J., Raff, M., and Cohen, J. 1984. GABA uptake by purified rat Schwann cells in culture. Brain Res. 303:183–185.

    PubMed  Google Scholar 

  24. Schon, F., and Kelly, J. S. 1974. The characterization of [3H]GABA uptake into the satellite glial cells of rat sensory ganglia. Brain. Res. 1966:289–300.

    Google Scholar 

  25. Hösli, E., and Hösli, L. 1978. Autoradiographic locarization of the uptake of [3H]GABA and L-[3H]glutamic acid in neurons and glial cells of cultured dorsal root ganglia. Neurosci. Lett. 7:173–176.

    Google Scholar 

  26. 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 

  27. Tasaka, J., Sakai, S., Tosaka, T., and Yoshihama, I. 1989. Glial uptake system of GABA distinct from that of taurine in the bullfrog sympathetic ganglia. Neurochem. Res. 14:271–277.

    PubMed  Google Scholar 

  28. Bowery, N. G., and Hill, D. R. 1986. GABA mechanisms in autonomic ganglia. in Erdö, S. L., and Bowery, N. G. (eds.), GABAergic mechanisms in the mammalian periphery, Raven Press, New York.

    Google Scholar 

  29. Kato, E., Morita, K., Kuba, K., Yamada, S., Kuhara, T., Shinka, T., and Matsumoto, I. 1980. Does γ-aminobutyric acid in blood control transmitter release in bullfrog sympathetic ganglia? Brain Res. 195:208–214.

    PubMed  Google Scholar 

  30. 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 

  31. Henn, F. A. and Hamberger, A. 1971. Glial cell function: uptake of transmitter substances. Proc. Natl. Acad. Sci. U.S.A. 68:2686–2690.

    PubMed  Google Scholar 

  32. Schrier, B. K., and Thompson, E. J. 1974. On the role of glial cells in the mammalian nervous system. J. Biol. Chem. 249:1769–1780.

    PubMed  Google Scholar 

  33. Oja, S. S., and Korpi, E. R. 1983. Amino acid transport. Pages 311–337,in Lajtha, A. (ed.), Handbook of Neurochemistry, vol. 5, 2nd edn., Plenum Press, New York.

    Google Scholar 

  34. 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.

    PubMed  Google Scholar 

  35. Hofstee, B. H. J. 1959. Non-inverted versus inverted plots in enzyme kinetics. Nature 184:1296–1298.

    PubMed  Google Scholar 

  36. Martin, D. L. 1973. Kinetics of the sodium-dependent transport of gamma-aminobutyric acid by synaptosomes. J. Neurochem. 21:345–356.

    PubMed  Google Scholar 

  37. Wheeler, D. D., and Hollingsworth, R. G. 1979. A model of GABA transport by cortical synaptosomes from the Long-Evans rat. J. Neurosci. Res. 4:265–289.

    PubMed  Google Scholar 

  38. Voaden, M. J., Marshall, J., and Murani, M. 1974. The uptake of3H γ-aminobutyric acid and3H glycine by the isolated retina of the frog. Brain Res. 67:115–132.

    PubMed  Google Scholar 

  39. Schubert, D. 1975. The uptake of GABA by clonal nerve and glia. Brain Res. 84:87–98.

    PubMed  Google Scholar 

  40. Sellström, Å., and Hamberger, A. 1975. Neuronal and glial cells system for γ-aminobutyric acid transport. J. Neurochem. 24:847–852.

    PubMed  Google Scholar 

  41. Glusman, S., Pacheco, A., Gonzales, R., and Haber, B. 1979. The filum terminale of the frog spinal cord, a non transformed glial preparation I. morphology and uptake of γ-aminobutyric acid. Brain Res. 172:259–276.

    PubMed  Google Scholar 

  42. Medzihradsky, F., Nandhasri, P. S., Idoyaga-Vargas, V., and Sellinger, O. Z. 1971. A comparison of the ATPase activity of the glial cell fraction and the neuronal pericaryal fraction isolated in bulk from rat cerebral cortex. J. Neurochem. 18:1599–1603.

    PubMed  Google Scholar 

  43. Haljamae, H., Hamberger, A. 1971. Potassium accumulation by bulk preparated neuronal and glial cells. J. Neurochem. 18:1903–1912.

    PubMed  Google Scholar 

  44. Kimelberg, H. K. 1974. Active potassium transport and (Na+−K+)ATPase activity in cultured glioma and neuroblastoma cells. J. Neurochem. 22:971–976.

    PubMed  Google Scholar 

  45. Gray, P. T. A., and Ritchie, J. M. 1985. Ion channels in Schwann and glial cells. Trends Neurosci. 411–415.

  46. Kanner, B. I. 1978. Active transport of γ-aminobutyric acid by membrane vesicles isolated from rat brain. Biochemistry 17:1207–1211.

    PubMed  Google Scholar 

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

    Saeko Sakai, Junko Tasaka & Tsuneo Tosaka

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Sakai, S., Tasaka, J. & Tosaka, T. Sodium dependency of GABA uptake into glial cells in bullfrog sympathetic ganglia. Neurochem Res 15, 843–847 (1990). https://doi.org/10.1007/BF00968563

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