Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signaling

Nature Neuroscience

Volumn 9, Issue 11, 2006, Pages 1388-1396

  Veruki, Margaret Lin ^a   Mørkve, Svein Harald ^a   Hartveit, Espen ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE TRANSPORTER;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; KINETICS; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; SYNAPTIC TRANSMISSION;

AMACRINE CELLS; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; AXONS; DATA INTERPRETATION, STATISTICAL; ELECTROPHYSIOLOGY; HISTOCYTOCHEMISTRY; KINETICS; PRESYNAPTIC TERMINALS; RATS; RETINAL BIPOLAR CELLS; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33750470835     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1793     Document Type: Article

References (49)

1. Danbolt, N.C. Glutamate uptake. Prog. Neurobiol. 65, 1-105 (2001).
2. Chaudhry, F.A. et al. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15, 711-720 (1995).
3. Rothstein, J.D. et al. Localization of neuronal and glial glutamate transporters. Neuron 13, 713-725 (1994).
4. Chen, W. et al. The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons. J. Neurosci. 24, 1136-1148 (2004).
5. Eliasof, S. & Werblin, F. Characterization of the glutamate transporter in retinal cones of the tiger salamander. J. Neurosci. 13, 402-411 (1993).
6. Gundersen, V., Danbolt, N.C., Ottersen, O.P. & Storm-Mathisen, J. Demonstration of glutamate/aspartate uptake activity in nerve endings by use of antibodies recognizing exogenous D-aspartate. Neuroscience 57, 97-111 (1993).
7. Hasegawa, J., Obara, T., Tanaka, K. & Tachibana, M. High-density presynaptic transporters are required for glutamate removal from the first visual synapse. Neuron 50, 63-74 (2006).
8. He, Y., Janssen, W.G., Rothstein, J.D. & Morrison, J.H. Differential synaptic localization of the glutamate transporter EAAC1 and glutamate receptor subunit GluR2 in the rat hippocampus. J. Comp. Neurol. 418, 255-269 (2000).
9. Palmer, M.J., Taschenberger, H., Hull, C., Tremere, L. & von Gersdorff, H. Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. J. Neurosci. 23, 4831-4841 (2003).
10. Picaud, S., Larsson, H.P., Wellis, D.P., Lecar, H. & Werblin, F. Cone photoreceptors respond to their own glutamate release in the tiger salamander. Proc. Natl. Acad. Sci. USA 92, 9417-9421 (1995).
11. Sarantis, M., Everett, K. & Attwell, D. A presynaptic action of glutamate at the cone output synapse. Nature 332, 451-453 (1988).
12. Tachibana, M. & Kaneko, A. L-glutamate-induced depolarization in solitary photoreceptors: a process that might contribute to the interaction between photoreceptors in situ. Proc. Natl. Acad. Sci. USA 85, 5315-5319 (1988).
13. Zerangue, N. & Kavanaugh, M.P. Flux coupling in a neuronal glutamate transporter. Nature 383, 634-637 (1996).
14. Fairman, W.A., Vandenberg, R.J., Arriza, J.L., Kavanaugh, M.P. & Amara, S.G. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375, 599-603 (1995).
15. Wadiche, J.I., Amara, S.G. & Kavanaugh, M.P. Ion fluxes associated with excitatory amino acid transport. Neuron 15, 721-728 (1995).
16. Arriza, J.L., Eliasof, S., Kavanaugh, M.P. & Amara, S.G. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc. Natl. Acad. Sci. USA 94, 4155-4160 (1997).
17. Protti, D.A. & Llano, I. Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices. J. Neurosci. 18, 3715-3724 (1998).
18. Shimamoto, K. et al. DL-threo-β-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol. Pharmacol. 53, 195-201 (1998).
19. Eliasof, S. & Jahr, C.E. Retinal glial cell glutamate transporter is coupled to an anionic conductance. Proc. Natl. Acad. Sci. USA 93, 4153-4158 (1996).
20. Veruki, M.L., Mørkve, S.H. & Hartveit, E. Functional properties of spontaneous EPSCs and non-NMDA receptors in rod amacrine (AII) cells in the rat retina. J. Physiol. (Lond.) 549, 759-774 (2003).
21. Cavelier, P., Hamann, M., Rossi, D., Mobbs, P. & Attwell, D. Tonic excitation and inhibition of neurons: ambient transmitter sources and computational consequences. Prog. Biophys. Mol. Biol. 87, 3-16 (2005).
22. von Gersdorff, H. & Matthews, G. Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J. Neurosci. 17, 1919-1927 (1997).
23. von Gersdorff, H., Sakaba, T., Berglund, K. & Tachibana, M. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21, 1177-1188 (1998).
24. Singer, J.H. & Diamond, J.S. Vesicle depletion and synaptic depression at a mammalian ribbon synapse. J. Neurophysiol. 95, 3191-3198 (2006).
25. 2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J. Neurosci. 23, 10923-10933 (2003).
26. Singer, J.H., Lassova, L., Vardi, N. & Diamond, J.S. Coordinated multivesicular release at a mammalian ribbon synapse. Nat. Neurosci. 7, 826-833 (2004).
27. Bergles, D.E. & Jahr, C.E. Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19, 1297-1308 (1997).
28. Otis, T.S. & Jahr, C.E. Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J. Neurosci. 18, 7099-7110 (1998).
29. Hartveit, E. Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J. Neurophysiol. 81, 2923-2936 (1999).
30. Rauen, T., Taylor, W.R., Kuhlbrodt, K. & Wiessner, M. High-affinity glutamate transporters in the rat retina: a major role of the glial glutamate transporter GLAST-1 in neurotransmitter clearance. Cell Tissue Res. 291, 19-31 (1998).
31. Wadiche, J.I., Arriza, J.L., Amara, S.G. & Kavanaugh, M.P. Kinetics of a human glutamate transporter. Neuron 14, 1019-1027 (1995).
32. Asztely, F., Erdemli, G. & Kullmann, D.M. Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18, 281-293 (1997).
33. Billups, D. & Attwell, D. Control of intracellular chloride concentration and GABA response polarity in rat retinal ON bipolar cells. J. Physiol. (Lond.) 545, 183-198 (2002).
34. Duebel, J. et al. Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor clomeleon. Neuron 49, 81-94 (2006).
35. Yamashita, M. & Wässle, H. Reversal potential of GABA-induced currents in rod bipolar cells of the rat retina. Vis. Neurosci. 6, 399-401 (1991).
36. Euler, T. & Masland, R.H. Light-evoked responses of bipolar cells in a mammalian retina. J. Neurophysiol. 83, 1817-1829 (2000).
37. Bergles, D.E., Dzubay, J.A. & Jahr, C.E. Glutamate transporter currents in Bergmann glial cells follow the time course of extrasynaptic glutamate. Proc. Natl. Acad. Sci. USA 94, 14821-14825 (1997).
38. Bergles, D.E., Tzingounis, A.V. & Jahr, C.E. Comparison of coupled and uncoupled currents during glutamate uptake by GLT-1 transporters. J. Neurosci. 22, 10153-10162 (2002).
39. Barbour, B. & Häusser, M. Intersynaptic diffusion of neurotransmitter. Trends Neurosci. 20, 377-384 (1997).
40. Huang, Y.H. & Bergles, D.E. Glutamate transporters bring competition to the synapse. Curr. Opin. Neurobiol. 14, 346-352 (2004).
41. Mørkve, S.H., Veruki, M.L. & Hartveit, E. Functional characteristics of non-NMDA-type ionotropic glutamate receptor channels in AII amacrine cells in rat retina. J. Physiol. (Lond.) 542, 147-165 (2002).
42. Derouiche, A. & Rauen, T. Coincidence of L-glutamate/L-aspartate transporter (GLAST) and glutamine synthetase (GS) immunoreactions in retinal glia: evidence for coupling of GLAST and GS in transmitter clearance. J. Neurosci. Res. 42, 131-143 (1995).
43. Pow, D.V. & Barnett, N.L. Developmental expression of excitatory amino acid transporter 5: a photoreceptor and bipolar cell glutamate transporter in rat retina. Neurosci. Lett. 280, 21-24 (2000).
44. Rauen, T. & Kanner, B.I. Localization of the glutamate transporter GLT-1 in rat and macaque monkey retinae. Neurosci. Lett. 169, 137-140 (1994).
45. Rauen, T., Rothstein, J.D. & Wässle, H. Differential expression of three glutamate transporter subtypes in the rat retina. Cell Tissue Res. 286, 325-336 (1996).
46. Ward, M.M., Jobling, A.I., Puthussery, T., Foster, L.E. & Fletcher, E.L. Localization and expression of the glutamate transporter, excitatory amino acid transporter 4, within astrocytes of the rat retina. Cell Tissue Res. 315, 305-310 (2004).
47. Tachibana, M. & Kaneko, A. γ-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells. Proc. Natl. Acad. Sci. USA 84, 3501-3505 (1987).
48. Palmer, M.J., Hull, C., Vigh, J. & von Gersdorff, H. Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J. Neurosci. 23, 11332-11341 (2003).
49. Arnth-Jensen, N., Jabaudon, D. & Scanziani, M. Cooperation between independent hippocampal synapses is controlled by glutamate uptake. Nat. Neurosci. 5, 325-331 (2002).