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Regulation of glutamate release by presynaptic kainate receptors in the hippocampus

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Abstract

MOST reported actions of kainate are mediated by AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate) receptors1,2. Here we report that, unlike AMPA which stimulates, kainate elicits a dose-dependent decrease in L-glutamate release from rat hippocampal synaptosomes and also depresses glutamatergic synaptic transmission. Brief exposure to kainate inhibited Ca2+ -dependent [3H] L-glutamate release by up to 80%. Inhibition was reversed by kainate antagonists but not by the AMPA-selective non-competitive antagonist l-(4-aminophenyl)-4-methyl-7,8-methyl-enedioxy-5H-2,3-benzodiazepine (GYKI 52466)3–7. A corresponding reversible kainate-evoked depression of NMDA (N-methyl-D-aspartate) receptor-mediated excitatory postsynaptic currents (e.p.s.cs) was observed when AMPA receptors were blocked by GYKI 52466. The synaptic depression was preceded by a brief period of enhanced release and a small inward current was also observed. The effects of kainate were unaffected by metabotropic glutamate (mGlu), GABAA, GABA B, glycine and adenosine receptor antagonists. These results indicate that glutamate release can be modulated directly by kainate autoreceptors.

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References

  1. Patneau, D. K. & Mayer, M. L. Neuron 6, 785–798 (1991).

    Article  CAS  Google Scholar 

  2. Bettler, B. & Mulle, C. Neuropharmacology 34, 123–139 (1995).

    Article  CAS  Google Scholar 

  3. Tarnawa, I., Engeberg, I. & Flatman, J. A. in Amino Acids, Chemistry, Biology and Medicine (eds Lubec, G. & Rosenthal, G. A.) 538–546 (ESCOM, Leiden, Netherlands, 1990).

    Book  Google Scholar 

  4. Palmer, A. J. & Lodge, D. Eur. J. Pharmac. molec. Pharm. Sec. 244, 193–194 (1993).

    Article  CAS  Google Scholar 

  5. Donevan, S. D. & Rogawski, M. A. Neuron 10, 51–59 (1993).

    Article  CAS  Google Scholar 

  6. Zorumski, C. F., Yamada, K. A., Price, M. D. & Olney, J. W. Neuron 10, 61–67 (1993).

    Article  CAS  Google Scholar 

  7. Paternain, A. V., Morales, M. & Lerma, J. Neuron 14, 185–189 (1995).

    Article  CAS  Google Scholar 

  8. Barnes, J. M., Dev, K. K. & Henley, J. M. Br. J. Pharmac. 113, 339–341 (1994).

    Article  CAS  Google Scholar 

  9. Johansen, T. H., Drejer, J., Watjen, F. & Nielsen, E. Ø. Eur. J. Pharmac. molec. Pharm. Sec. 246, 195–204 (1993).

    Article  CAS  Google Scholar 

  10. Verdoorn, T. A., Johansen, T. H., Drejer, J. & Nielsen, E. Ø. Eur. J. Pharmac. molec. Pharm. Sec. 269, 43–49 (1994).

    Article  CAS  Google Scholar 

  11. Honoré, T. et al. Science 241, 701–703 (1988).

    Article  ADS  Google Scholar 

  12. Sheardown, M. J., Nielsen, E. Ø., Hansen, A. J., Jacobsen, P. & Honoré, T. Science 247, 571–574 (1990).

    Article  ADS  CAS  Google Scholar 

  13. Wong, L. A. & Mayer, M. L. Molec. Pharmac. 44, 504–510 (1993).

    CAS  Google Scholar 

  14. Martin, D., Bustos, G. A., Bowe, M. A., Bray, S. D. & Nadler, J. V. J. Neurochem. 56, 1647–1655 (1991).

    Article  CAS  Google Scholar 

  15. Zhou, M., Peterson, C. L., Lu, Y.-B. & Nadler, J. V. J. Neurochem. 64, 1556–1566 (1995).

    Article  CAS  Google Scholar 

  16. Collingridge, G. L. & Watkins, J. C. (eds) The NMDA Receptor (Oxford Univ. Press, 1994).

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

    Article  CAS  Google Scholar 

  18. Collingridge, G. L., Kehl, S. J. & McLennan, H. J. Physiol., Lond. 334, 33–46 (1983).

    Article  CAS  Google Scholar 

  19. Legendre, P., Rosenmund, C. & Westbrook, G. L. J. Neurosci. 13, 674–684 (1993).

    Article  CAS  Google Scholar 

  20. Bahn, S., Volk, B. & Wisden, W. J. Neurosci. 14, 5525–5547 (1994).

    Article  CAS  Google Scholar 

  21. Agrawal, S. G. & Evans, R. H. Br. J. Pharmac. 87, 345–355 (1986).

    Article  CAS  Google Scholar 

  22. Sawada, S., Higashima, M. & Yamamoto, C. Expl Brain Res. 60, 323–329 (1985).

    Article  CAS  Google Scholar 

  23. Nistri, A. & Cherubini, E. J. Physiol., Lond. 435, 465–481 (1991).

    Article  CAS  Google Scholar 

  24. Malva, J. O. et al. Neurosci. Lett. 185, 83–86 (1995).

    Article  CAS  Google Scholar 

  25. Lerma, J., Paternain, A. V., Naranjo, J. R. & Mellström, B. Proc. natn. Acad. Sci. U.S.A. 90, 11688–11692 (1993).

    Article  ADS  CAS  Google Scholar 

  26. Ruano, D., Lambolez, B., Rossier, J., Paternain, A. V. & Lerma, J. Neuron 14, 1009–1017 (1995).

    Article  CAS  Google Scholar 

  27. Zeman, S. & Lodge, D. Br. J. Pharmac. 106, 367–372 (1992).

    Article  CAS  Google Scholar 

  28. Huettner, J. E. Neuron 5, 255–266 (1990).

    Article  CAS  Google Scholar 

  29. Renard, A., Crepel, F. & Audinat, E. Neuropharmacology 34, 335–347 (1995).

    Article  CAS  Google Scholar 

  30. Egebjerg, J., Bettler, B., Hermans-Borgmeyer, I. & Heinemann, S. Nature 351, 745–748 (1991).

    Article  ADS  CAS  Google Scholar 

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Chittajallu, R., Vignes, M., Dev, K. et al. Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 379, 78–81 (1996). https://doi.org/10.1038/379078a0

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