Knocking out the glial glutamate transporter GLT-1 reduces glutamate uptake but does not affect hippocampal glutamate dynamics in early simulated ischaemia

European Journal of Neuroscience

Volumn 15, Issue 2, 2002, Pages 308-314

  Hamann, Martine ^a   Rossi, David J ^a   Marie, Hélène ^a   Attwell, David ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Anoxic depolarization; Dihydrokainate; Hypoxia; Mouse

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; GLUTAMINE; N METHYL DEXTRO ASPARTIC ACID; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL MODEL; ANIMAL TISSUE; ANOXIA; ARTICLE; BRAIN ISCHEMIA; BRAIN SLICE; CELL MEMBRANE DEPOLARIZATION; CELL SECRETION; CONTROLLED STUDY; EVOKED CORTICAL RESPONSE; GLIA; HIPPOCAMPUS; KNOCKOUT MOUSE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; TISSUE LEVEL;

2-AMINO-5-PHOSPHONOVALERATE; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; DIZOCILPINE MALEATE; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMIC ACID; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; KAINIC ACID; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; N-METHYLASPARTATE; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; QUINOXALINES; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 0036460164     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.0953-816x.2001.01861.x     Document Type: Article

References (36)

1. Arriza, J.L., Fairman, W.A., Wadiche, J.I., Murdoch, G.H., Kavanaugh, M.P. & Amara, S.G. (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci., 14, 5559-5569.
2. Attwell, D., Barbour, B. & Szatkowski, M. (1993) Nonvesicular release of neurotransmitter. Neuron, 11, 401-407.
3. Barbour, B., Brew, H. & Attwell, D. (1991) Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander (Ambystome) retina. J. Physiol., 436, 169-193.
4. Chittajallu, R., Vignes, M., Dev, K.K., Barnes, J.M., Collingridge, G.L. & Henley, J.M. (1996) Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature, 379, 78-81.
5. Choi, D.W., Maulucci-Gedde, M. & Kriegstein, A.R. (1987) Glutamate neurotoxicity in cortical cell culture. J. Neurosci., 7, 357-368.
6. Crepel, V., Hammond, C., Chinestra, P., Diabira, D. & Ben-Ari, Y. (1993) A selective LTP of NMDA receptor-mediated currents induced by anoxia in CA1 hippocampal neurons. J. Neurophysiol., 70, 2045-2055.
7. Danbolt, N.C. (2001) Glutamate uptake. Prog. Neurobiol., 65, 1-105.
8. Dawson, L.A., Djali, S., Gonzales, C., Vinegra, M.A. & Zaleska, M.M. (2000) Characterization of transient focal ischemia-induced increases in extracellular glutamate and aspartate in spontaneously hypertensive rats. Brain Res. Bull., 53, 767-776.
9. Furuta, A., Rothstein, J.D. & Martin, L.J. (1997) Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J. Neurosci., 17, 8363-8375.
10. Hansen, A.J. (1985) Effect of anoxia on ion distribution in the brain. Physiol. Rev., 65, 101-148.
11. Haugeto, O., Ullensvang, K., Levy, L.M., Chaudhry, F.A., Honore, T., Nielsen, M., Lehre, K.P. & Danbolt, N.C. (1996) Brain glutamate transporters form homomultimers. J. Biol. Chem., 271, 27715-27722.
12. Hirota, H., Katayama, Y., Kawamata, T., Kano, T. & Tsubokawa, T. (1995) Inhibition of the high-affinity glutamate uptake system facilitates the massive potassium flux during cerebral ischaemia in vivo. Neurol. Res., 17, 94-96.
13. Hori, N., Doi, N., Miyahara, S., Shinoda, Y. & Carpenter, D.O. (1991) Appearance of NMDA receptors triggered by anoxia independent of voltage in vivo and in vitro. Exp. Neurol., 112, 304-311.
14. Kamboj, R.K., Schoepp, D.D., Nutt, S., Shekter, L., Korczak, B., True, R.A., Rampersad, V., Zimmerman, D.M. & Wosnick, M.A. (1994) Molecular cloning, expression, and pharmacological characterization of humEAA1, a human kainate receptor subunit. J. Neurochem., 62, 1-9.
15. Kanai, Y. & Hediger, M.A. (1992) Primary structure and functional characterization of a high-affinity glutamate transporter. Nature, 360, 467-471.
16. Lehre, K.P. & Danbolt, N.C. (1998) The number of glutamate transporter subtype molecules at glutamatergic synapses: Chemical and stereological quantification in young adult rat brain. J. Neurosci., 18, 8751-8757.
17. Lehre, K.P., Levy, L.M., Ottersen, O.P., Storm-Mathisen, J. & Danbolt, N.C. (1995) Differential expression of two glial glutamate transporters in the rat brain: Quantitative and immunocytochemical observations. J. Neurosci., 15, 1835-1853.
18. +-dependent glutamate uptake. J. Neurosci., 18, 9620-9628.
19. Madl, J.E. & Burgesser, K. (1993) Adenosine triphosphate depletion reverses sodium-dependent, neuronal uptake of glutamate in rat hippocampal slices. J. Neurosci., 13, 4429-4444.
20. Maki, R., Robinson, M.B. & Dichter, M.A. (1994) The glutamate uptake inhibitor L-trans-pyrrolidine-2,4-dicarboxylate depresses excitatory synaptic transmission via a presynaptic mechanism in cultured hippocampal neurons. J. Neurosci., 14, 6754-6762.
21. Massieu, L., Morales-Villagran, A. & Tapia, R. (1995) Accumulation of extracellular glutamate by inhibition of its uptake is not sufficient for inducing neuronal damage: An in vivo microdialysis study. J. Neurochem., 64, 2262-2272.
22. Ottersen, O.P. (1989) Postembedding immunogold labelling of fixed glutamate: An electron microscopic analysis of the relationship between gold particle density and antigen concentration. J. Chem. Neuroanat., 2, 57-66.
23. Phillis, J.W., Smith-Barbour, M., Perkins, L.M. & O'Regan, M.H. (1994) Characterization of glutamate, aspartate, and GABA release from ischemic rat cerebral cortex. Brain Res. Bull., 34, 457-466.
24. Rao, V.L., Dogan, A., Todd, K.G., Bowen, K.K., Kim, B.T., Rothstein, J.D. & Dempsey, R.J. (2001) Antisense knockdown of the glial glutamate transporter GLT-1, but not the neuronal glutamate transporter EAAC1, exacerbates transient focal cerebral ischemia-induced neuronal damage in rat brain. J. Neurosci., 21, 1876-1883.
25. Roettger, V. & Lipton, P. (1996) Mechanism of glutamate release from rat hippocampal slices during in vitro ischemia. Neuroscience, 75, 677-685.
26. Rossi, D., Oshima, T. & Attwell, D. (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature, 403, 316-321.
27. Seki, Y., Feustel, P.J., Keller, R.W. Jr, Tranmer, B.I. & Kimelberg, H.K. (1999) Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokainate and an anion channel blocker. Stroke, 30, 433-440.
28. Shimamoto, K., Lebrun, B., Yasuda-Kamatani, Y., Sakaitani, M., Shigeri, Y., Yumoto, N. & Nakajima, T. (1998) DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol. Pharmacol., 53, 195-201.
29. Storm-Mathisen, J., Danbolt, N.C., Rothe, F., Torp, R., Zhang, N., Aas, J.-E., Kanner, B.I., Langmoen, I. & Ottersen, O.P. (1992) Ultrastructural immunocytochemical observations on the localization, metabolism and transport of glutamate in normal and ischemic brain tissue. Prog. Brain Res., 94, 225-241.
30. Szatkowski, M. & Attwell, D. (1994) Triggering and execution of neuronal death in brain ischaemia: Two phases of glutamate release by different mechanisms. Trends Neurosci., 17, 359-365.
31. Szatkowski, M., Barbour, B. & Attwell, D. (1990) Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature, 348, 443-446.
32. Tanaka, K. (1994) Pharmacological characterization of a cloned rat glutamate transporter (Glu-T-1). Mol. Brain Res., 21, 167-170.
33. Tanaka, K., Watase, K., Manabe, T., Yamada, K., Watanabe, M., Takahashi, K., Iwama, H., Nishikawa, T., Ichihara, N., Kikuchi, T., Okuyama, S., Kawashima, N., Hori, S., Takimoto, M. & Wada, K. (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science, 276, 1699-1702.
34. Ullensvang, K., Lehre, K.P., Storm-Mathisen, J. & Danbolt, N.C. (1997) Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur. J. Neurosci., 9, 1646-1655.
35. Wahl, F., Obrenovitch, T.P., Hardy, A.M., Plotkine, M., Boulu, R. & Symon, L. (1994) Extracellular glutamate during focal cerebral ischaemia in rats: Time course and calcium-dependency. J. Neurochem., 63, 1003-1011.
36. Zerangue, N. & Kavanaugh, M.P. (1996) Flux coupling in a neuronal glutamate transporter. Nature, 383, 634-637.