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Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake

Nature volume 348, pages 443–446 (1990)Cite this article

Abstract

GLUTAMATE uptake into nerve and glial cells usually functions to keep the extracellular glutamate concentration low in the central nervous system1. But one component of glutamate release from neurons is calcium-independent, suggesting a non-vesicular release that may be due to a reversal of glutamate uptake2,3. The activity of the electrogenic glutamate uptake carrier can be monitored by measuring the membrane current it produces4, and uptake is activated by intracellular potassium ions5. Here we report that raising the potassium concentration around glial cells evokes an outward current component produced by reversed glutamate uptake. This current is activated by intracellular glutamate and sodium, inhibited by extracellular glutamate and sodium, and increased by membrane depolarization. These results demonstrate a non-vesicular mechanism for the release of glutamate from glial cells and neurons. This mechanism may contribute to the neurotoxic rise in extracellular glutamate concentration during brain anoxia.

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References

  1. Hertz, L. Prog. Neurobiol. 13, 277–323 (1979).

    Article  CAS  Google Scholar 

  2. Miller, A. M. & Schwartz, E. A. J. Physiol., Lond. 334, 325–350 (1983).

    Article  CAS  Google Scholar 

  3. Nicholls, D. G., Sihra, T. S. & Sanchez-Prieto, J. J. Neurochem. 49, 50–57 (1987).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  6. Sarantis, M. & Attwell, D. Brain Res. 516, 322–325 (1990).

    Article  CAS  Google Scholar 

  7. Cull-Candy, S. G., Howe, J. R. & Ogden, D. J. Physiol., Lond. 400, 189–222 (1988).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Walz, W. & Hertz, L. J. Neurochem. 39, 70–77 (1982).

    Article  CAS  Google Scholar 

  10. Newman, E. A. Nature 317, 809–811 (1985).

    Article  ADS  CAS  Google Scholar 

  11. Newman, E. A. Nature 309, 155–157 (1984).

    Article  ADS  CAS  Google Scholar 

  12. Brew, H., Gray, P., Mobbs, P. & Attwell, D. Nature 324, 466–468 (1986).

    Article  ADS  CAS  Google Scholar 

  13. Ballanyi, K., Grafe, P. & Ten Bruggencate, G. J. Physiol., Lond. 382, 159–174 (1987).

    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. Rothman, S. M. & Olney, J. W. Trends Neurosci. 10, 299–302 (1987).

    Article  CAS  Google Scholar 

  18. Sanchez-Prieto, J. & Gonzalez, P. J. Neurochem. 50, 1322–1324 (1988).

    Article  CAS  Google Scholar 

  19. Walz, W. & Hertz, L. Prog. Neurobiol. 20, 133–183 (1983).

    Article  CAS  Google Scholar 

  20. Siesjö, B. News physiol. Sci. 5, 120–125 (1990).

    Google Scholar 

  21. Ikeda, M., Nakazawa, T., Abe, K., Kaneko, T. & Yamatsu, K. Neurosci. Lett. 96, 202–206 (1989).

    Article  CAS  Google Scholar 

  22. Sontheimer, H., Kettenmann, H., Backus, K. H. & Schachner, M. Glia 1, 328–336 (1988).

    Article  CAS  Google Scholar 

  23. Sakmann, B. & Trube, G. J. Physiol. Lond. 347, 641–657 (1984).

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Physiology, University College London, Gower Street, London, WC1E 6BT, UK

    Marek Szatkowski, Boris Barbour & David Attwell

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  1. Marek Szatkowski
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  2. Boris Barbour
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  3. David Attwell
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Szatkowski, M., Barbour, B. & Attwell, D. Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348, 443–446 (1990). https://doi.org/10.1038/348443a0

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