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The glial cell glutamate uptake carrier countertransports pH-changing anions

Abstract

UPTAKE into glial cells helps to terminate glutamate's neurotransmitter action and to keep its extracellular concentration, [Glu]o, below neurotoxic levels. The accumulative power of the uptake carrier stems from its transport of inorganic ions such as sodium (into the cell) and potassium (out of the cell)1–3. There is controversy over whether the carrier also transports a proton (or pH-changing anion)4,5. Here we show that the carrier generates an alkalinization outside and an acidification inside glial cells, and transports anions out of the cells, suggesting that there is a carrier cycle in which two Na+ accompany each glutamate anion into the cell, while one K+ and one OH(or HCO3) are transported out. This stoichiometry predicts a minimum [Glu]o of 0.6 μM normally (tonically activating presynaptic autoreceptors and postsynaptic NMD A receptors), and 370 μM during brain anoxia (high enough to kill neurons). Transport of OH/HCO3 on the uptake carrier generates significant pH changes, and may provide a mechanism for neuron–glial interaction.

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References

  1. Kanner, B. I. & Schuldiner, S. CRC Crit. Rev. Biochem. 22, 1–38 (1987).

    Article  CAS  Google Scholar 

  2. Barbour, B., Brew, H. & Attwell, D. Nature 335, 433–435 (1988).

    Article  ADS  CAS  Google Scholar 

  3. Barbour, B., Brew, H. & Attwell, D. J. Physiol. 436, 169–193 (1991).

    Article  CAS  Google Scholar 

  4. Erecinska, M., Wantorsky, D. & Wilson, D. F. J. biol. Chem. 258, 9069–9077 (1983).

    CAS  Google Scholar 

  5. Schwartz, E. A. & Tachibana, M. J. Physiol. 426, 43–80 (1990).

    Article  CAS  Google Scholar 

  6. Nicholls, D. & Attwell, D. Trends Pharmac. Sci. 11, 462–468 (1990).

    Article  Google Scholar 

  7. Brew, H. & Attwell, D. Nature 327, 707–709 (1987).

    Article  ADS  CAS  Google Scholar 

  8. Sarantis, M. & Attwell, D. Brain res. 516, 322–325 (1990).

    Article  CAS  Google Scholar 

  9. Rink, T. J., Tsien, R. Y. & Pozzan, T. J. Cell Biol. 95, 189–196 (1982).

    Article  CAS  Google Scholar 

  10. Putnam, R. W., Roos, A. & Wilding, T. J. J. Physiol. 381, 205–219 (1986).

    Article  CAS  Google Scholar 

  11. Newman, E. A. & Astion, M. L. Glia 4, 424–428 (1991).

    Article  CAS  Google Scholar 

  12. Kaila, K., Saarikoski, J. & Voipio, J. J. Physiol. 427, 241–260 (1990).

    Article  CAS  Google Scholar 

  13. Chesler, M. Prog. in Neurobiol. 34, 401–427 (1990).

    Article  CAS  Google Scholar 

  14. Berger, S. J., Carter, J. G. & Lowry, O. H. J. Neurochem. 28, 149–158 (1977).

    Article  CAS  Google Scholar 

  15. Schousboe, A., Fosmark, H. & Hertz, L. J. Neurochem. 25, 909–911 (1975).

    Article  CAS  Google Scholar 

  16. Kvamme, E., Schousboe, A., Hertz, L., Torgner, I. A. & Svenneby, G. Neurochem. Res. 10, 993–1008 (1985).

    Article  CAS  Google Scholar 

  17. Forsythe, I. D. & Clements, J. D. J. Physiol. 429, 1–16 (1990).

    Article  CAS  Google Scholar 

  18. Patneau, D. K. & Mayer, M. L. J. Neurosci. 10, 2385–2393 (1990).

    Article  CAS  Google Scholar 

  19. Sather, W., Dieudonné, S., MacDonald, J. F. & Ascher, P. J. Physiol. 450, 643–672 (1992).

    Article  CAS  Google Scholar 

  20. Sah, P., Hestrin, S. & Nicoll, R. Science 246, 815–818 (1989).

    Article  ADS  CAS  Google Scholar 

  21. Choi, D. W., Maulucci-Gedde, M. & Kriegstein, A. R. J. Neurosci. 7, 357–368 (1987).

    Article  CAS  Google Scholar 

  22. Szatkowski, M., Barbour, B. & Attwell, D. Nature 348, 443–446 (1990).

    Article  ADS  CAS  Google Scholar 

  23. Thomas, R. C. Ion Sensitive Intracellular Microelectrodes (Academic, London, 1978).

    Google Scholar 

  24. Eisner, D. A. et al. Pflügers Arch. 413, 553–558 (1989).

    Article  CAS  Google Scholar 

  25. Chaillet, J. R. & Boron, W. F. J. gen. Physiol. 86, 765–794 (1985).

    Article  CAS  Google Scholar 

  26. Mobbs, P., Brew, H. & Attwell, D. Brain Res. 460, 235–245 (1988).

    Article  CAS  Google Scholar 

  27. Edsall, J. T. & Wyman, J. Biophysical Chemistry 585 (Academic, New York, 1958).

    Google Scholar 

  28. Eigen, M. & De Maeyer, L. Proc. R. Soc. Lond. A 247, 505–533 (1958).

    ADS  CAS  Google Scholar 

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Bouvier, M., Szatkowski, M., Amato, A. et al. The glial cell glutamate uptake carrier countertransports pH-changing anions. Nature 360, 471–474 (1992). https://doi.org/10.1038/360471a0

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