Synaptic activation of glutamate transporters in hippocampal astrocytes

Neuron

Volumn 19, Issue 6, 1997, Pages 1297-1308

  Bergles, Dwight E ^a   Jahr, Craig E ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 3 HYDROXYASPARTIC ACID; 4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CADMIUM CHLORIDE; CARRIER PROTEIN; DIHYDROKAINIC ACID; GLUTAMIC ACID; PICROTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; HIPPOCAMPUS; MEMBRANE CURRENT; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

EID: 0031472475     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80420-1     Document Type: Article

References (65)

1. Aitken, P.G., and Somjen, G.G. (1986). The sources of extracellular potassium accumulation in the CA1 region of hippocampal slices. Brain Res. 369, 163-167.
2. Arriza, J.L., Fairman, W.A., Wadiche, J.I., Murdoch, G.H., Kavanaugh, M.P., and Amara, S.G. (1994). Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci. 14, 5559-5569.
3. Asztely, F., Erdemli, G., and Kullmann, D.M. (1997). Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18, 281-293.
4. Balcar, V.J., Johnston, G.A.R., and Twitchin, B. (1977). Stereo-specificity of the inhibition of L-glutamate and L-aspartate high affinity uptake in rat brain slices by threo-3-hydroxyaspartate. J. Neurochem. 28, 1145-1146.
5. Barbour, B., Brew, H., and Attwell, D. (1991). Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander retina. J. Physiol. 436, 169-193.
6. Barbour, B., Keller, B., Llano, I., and Marty, A. (1994). Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells. Neuron 12, 1331-1343.
7. Baude, A., Nusser, Z., Roberts, J.D.B., Mulvihill, E., McIllhinney, R.A.J., and Somogyi, P. (1993). The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771-787.
8. Brew, H., and Attwell, D. (1987). Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327, 707-709.
9. Bruns, D., Engert, F., and Lux, H.-D. (1993). A fast activating presynaptic reuptakecurrent during serotonergic transmission in identified neurons of Hirudo. Neuron 10, 559-572.
10. Clark, B.A., and Barbour, B. (1997). Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices. J. Physiol. 502, 335-350.
11. Clements, J.D., Lester, R.A., Tong, G., Jahr, C.E., and Westbrook, G.L. (1992). The time course of glutamate in the synaptic cleft. Science 258, 1498-1501.
12. de Barry, J., Langley, O.K., Vincendon, G., and Gombos, G. (1982). L-glutamate and L-glutamine uptake in adult rat cerebellum: an autoradiographic study. Neuroscience 7, 1289-1297.
13. Diamond, J.S., and Jahr, C.E. (1995). Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron 15, 1097-1107.
14. Diamond, J.S., and Jahr, C.E. (1997). Transporters buffer synaptically released glutamate on a millisecond time scale. J. Neurosci. 17, 4672-4687.
15. Eccles, J.C., and Jaeger, J.C. (1958). The relationship between the mode of operation and the dimensions of the junctional regions at synapses and motor end-organs. Proc. R. Soc. Lond. [Biol.] 148, 38-56.
16. Eliasof, S., and Jahr, C.E. (1996). Retinal glial cell glutamate transporter is coupled to an anionic conductance. Proc. Natl. Acad. Sci. USA 93, 4153-4158.
17. Hestrin, S., Sah, P., and Nicoll, R.A. (1990). Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5, 247-253.
18. Isaacson, J.S., and Nicoll, R.A. (1993). The uptake inhibitor L-trans-PDC enhances responses to glutamate but fails to alter the kinetics of excitatory synaptic currents in the hippocampus. J. Neurophysiol. 70, 2187-2191.
19. Isaacson, J.S., and Walmsley, B. (1995). Counting quanta: direct measurements of transmitter release at a central synapse. Neuron 15, 1-20.
20. Johnston, G.A.R., Kennedy, S.M.E., and Twitchin, B. (1979). Action of the neurotoxin kainic acid on high affinity uptake of L-glutamic acid in rat brain slices. J. Neurochem. 32, 121-127.
21. Jonas, P., and Sakmann, B. (1992). Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. J. Physiol. 455, 143-171.
22. Kanai, Y., Nussberger, S., Romero, M.F., Boron, W.F., Hebert, S.C., and Hediger, M.A. (1995). Electrogenic properties of the epithelial and neuronal high affinity glutamate transporter. J. Biol. Chem. 270, 16561-16568.
23. Karpen, J.W., Loney, D.A., and Baylor, D.A. (1992). Cyclic GMP-activated channels of salamander retinal rods: spatial distribution and variation in responsiveness. J. Physiol. 448, 257-274.
24. Kavanaugh, M.P., Bendahan, A., Zerangue, N., Zhang, Y., and Kanner, B.I. (1997). Mutation of an amino acid residue influencing potassium coupling in the glutamate transporter GLT-1 induces obligate exchange. J. Biol. Chem. 272, 1703-1708.
25. Kiskin, N.I., Krishtal, O.A., and Tsyndrenko, A.Y. (1986). Excitatory amino acid receptors in hippocampal neurons: kainate fails to desensitize them. Neurosci. Lett. 63, 225-230.
26. Klockner, U., Storck, T., Conradt, M., and Stoffel, W. (1994). Functional properties and substrate specificity of the cloned L-glutamate/ L-aspartate transporter GLAST-1 from rat brain expressed in Xenopus oocytes. J. Neurosci. 14, 5759-5765.
27. Koneintzko, U., and Muller, C.M. (1994). Astrocyte dye coupling in rat hippocampus: topography, developmental onset and modulation by protein kinase C. Hippocampus 4, 297-306.
28. Kosaka, T., and Hama, K. (1986). Three-dimensional structure of astrocytes in the rat dentate gyrus. J. Comp. Neurol. 249, 242-260.
29. Kullmann, D.M., Erdemli, G., and Asztely, F. (1996). LTP of AMPA and NMDA receptor-mediated signals: evidence for presynaptic expression and extrasynaptic glutamate spill-over. Neuron 17, 461-474.
30. Lehre, K.P., Levy, L.M., Ottersen, O.P., Storm-Mathisen, J., Danbolt, N.C. (1995). Differential expression of two gliai glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J. Neurosci. 15, 1835-1853.
31. Linden, D.J. (1997). Long-term potentiation of glial synaptic currents in cerebellar culture. Neuron 18, 983-994.
32. 3H]glutamate in rat brain tissue. Brain Res. 115, 139-144.
33. Mennerick, S., and Zorumski, C.F. (1994). Glial contribution to excitatory transmission in cultured hippocampal cells. Nature 368, 59-62.
34. Mennerick, S., Benz, A., and Zorumski, C.F. (1996). Components of glial responses to exogenous and synaptic glutamate in rat hippocampal microcultures. J. Neurosci. 16, 55-64.
35. Newman, E.A. (1986). High potassium conductance in astrocyte endfeet. Nature 233, 453-454.
36. Otis, T., Wu, Y.-C., and Trussell, L.O. (1996). Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J. Neurosci. 16, 1634-1644.
37. Palay, S.L., and Chan-Palay, V. (1974). Cerebellar Cortex, Cytology and Organization (New York: Springer-Verlag).
38. Pines, G., Danbolt, N.C., Bjoras, M., Zhang, Y., Bendahan, A., Eide, L., Koepsell, H., Storm-Mathisen, J., Seeberg, E., and Kanner, B.I. (1992). Cloning and expression of a rat brain L-glutamate transporter. Nature 360, 464-467.
39. Rothstein, J.D., Martin, L., Levey, A.I., Dykes-Hoberg, M., Jin, L., Wu, D., Nash, N., and Kuncl, R.W. (1994). Localization of neuronal and glial glutamate transporters. Neuron 13, 713-725.
40. Rothstein, J.D., Dykes-Hoberg, M., Pardo, C.A., Bristol, L.A., Jin, L., Kunci, R.W., Kanai, Y., Hediger, M.A., Wang, Y., Schielke, J.P., and Welty, D.F. (1996). Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16, 675-686.
41. Sakmann, B., and Stuart, G. (1995). Patch pipette recordings from the soma, dendrites, and axon of neurons in brain slices. In Single Channel Recording, B. Sakmann and E. Neher, eds. (New York, New York: Plenum Press), pp. 199-211.
42. Sarantis, M., Ballerini, L., Miller, B., Silver, R.A., Edwards, M., and Attwell, D. (1993). Glutamate uptake from the synaptic cleft does not shape the decay of the non-NMDA component of the synaptic current. Neuron 11, 541-549.
43. Scanziani, M., Salin, P.A., Vogt, K.E., Malenka, R.C., and Nicoll, R.A. (1997). Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385, 630-634.
44. 3H]aspartate during postnatal development of the hippocampal formation: a quantitative autoradiographic study. Expl. Brain Res. 70, 50-54.
45. Schwartz, E.A., and Tachibana, M. (1990). Electrophysiology of glutamate and sodium co-transport in a glial cell of the salamander retina. J. Physiol. 426, 43-80.
46. Schwartzkroin, P.A., and Prince, D.A. (1979). Recordings from presumed glial cells in the hippocampal slice. Brain Res. 161, 533-538.
47. Shibata, T., Watanabe, M., Tanaka, K., Wada, K., and Inoue, Y. (1996). Dynamic changes in expression of glutamate transporter mRNAs in developing brain. Neuroreport 7, 705-709.
48. Silver, R.A., Cull-Candy, S.G., and Takahashi, T. (1996). Non-NMDA glutamate receptor occupancy and open probability at a rat cerebellar synapse with single and multiple release sites. J. Physiol. 494, 231-250.
49. Sorra, K.E., and Harris, K.M. (1993). Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J. Neurosci. 13, 3736-3748.
50. Spacek, J. (1971). Three-dimensional reconstructions of astroglia and oligodendroglia cells. Z. Zellforsch. 112, 430-442.
51. Spacek, J. (1985). Three-dimensional analysis of dendritic spines III. Glial sheath. Anat. Embryol. 171, 245-252.
52. Spruston, N., Jaffe, D.B., Williams, S.H., and Johnston, D. (1993). Voltage-and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J. Neurophysiol. 70, 781-802.
53. Steinhauser, C., Jabs, R., and Kettenmann, H. (1994). Properties of GABA and glutamate responses in identified glial cells of the mouse hippocampal slice. Hippocampus 4, 19-36.
54. Szatkowski, M., Barbour, B., and Attwell, D. (1990). Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348, 443-446.
55. Takahashi, M., Sarantis, M., and Attwell, D. (1996). Postsynaptic glutamate uptake in rat cerebellar Purkinje cells. J. Physiol. 497, 523-530.
56. Tanaka, K., Watase, K., Manabe, T., Yamada, K., Watanabe, M., Takahashi, K., Iwama, H., Nishikawa, T., Ichihara, N., Kikuchi, T., et al. (1997). Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276, 1699-1702.
57. Tong, G., and Jahr, C.E. (1994). Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13, 1195-1203.
58. Trussell, L.O., and Fischbach, G.D. (1989). Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3, 209-218.
59. Wadiche, J.I., Arriza, J.L., Amara, S.G., and Kavanaugh, M.P. (1995a). Kinetics of a human glutamate transporter. Neuron 14, 1019-1027.
60. Wadiche, J.I., Amara, S.G., and Kavanaugh, M.P. (1995b). Ion fluxes associated with excitatory amino acid transport. Neuron 15, 721-728.
61. Wilkin, G.P., Garthwaite, J., and Balazs, R. (1982). Putative acidic amino acid transmitters in the cerebellum. II. Electron microscopic localization of transport sites. Brain Res. 244, 69-80.
62. Wyllie, D.J.A., Mathie, A., Symonds, C.J., and Cull-Candy, S.G. (1991). Activation of glutamate receptors and glutamate uptake in identified macroglial cells in rat cerebellar cultures. J. Physiol. 432, 235-258.
63. Yamamoto, T., Vukelic, J., Hertzberg, E.L., and Nagy, J.I. (1992). Differential anatomical and cellular patterns of connexin43 expression during postnatal development of rat brain. Dev. Brain Res. 66, 165-180.
64. Zerangue, N., and Kavanaugh, M.P. (1996). Flux coupling in a neuronal glutamate transporter. Nature 383, 634-637.
65. Zhang, S., and Trussell, L.O. (1994). A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J. Neurophysiol. 72, 705-718.