Glutamate transporters contribute to the time course of synaptic transmission in cerebellar granule cells

Journal of Neuroscience

Volumn 19, Issue 21, 1999, Pages 9663-9673

  Overstreet, Linda S ^a,b   Kinney, Gregory A ^a,c   Liu, Ying Bing ^a,d   Billups, Daniela ^a   Slater, N Traverse ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d SICHUAN UNIVERSITY   (China)

Author keywords

Cerebellum; Glutamate transport; Reuptake; Synaptic transmission; Time course; Transporters

Indexed keywords

AMPA RECEPTOR; GLUTAMATE TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN SLICE; CONTROLLED STUDY; EVOKED RESPONSE; GRANULE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 0033232782     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-21-09663.1999     Document Type: Article

References (67)

1. Arriza JL, Fairman WA, Wadiche JL, Murdoch GH, Kavanaugh MP, Amara SG (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. Neuron 14:5559-5569.
2. Asztely F, Erdemli G, Kullmann DM (1997) Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18:281-293.
3. Barbour B, Häusser M (1997) Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20:377-384.
4. Barbour B, Brew H, Attwell D (1991) Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander (Ambystoma) retina. J Physiol (Lond) 436:169-193.
5. Barbour B, Keller BU, Llano I, Marty A (1994) Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells. Neuron 12:1331-1343.
6. Barmack NH, Baughman RW, Eckenstein FP (1992) Cholinergic innervation of the cerebellum of rat, rabbit, cat, and monkey as revealed by choline acetyltransferase activity and immunohistochemistry. J Comp Neurol 317:233-249.
7. Bergles DE, Jahr CE (1997) Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19:1297-1308.
8. Bridges RJ, Stanley MS, Anderson MW, Cotman CW, Chamberlin AR (1991) Conformationally defined neurotransmitter analogues. Selective inhibition of glutamate uptake by one pyrrolidine-2:4-dicarboxylate diastereomer. J Med Chem 34:717-725.
9. Castagna M, Shayakul C, Trotti D, Sacchi VF, Harvey WR, Hediger MA (1997) Molecular characteristics of mammalian and insect amino acid transporters: implications for amino acid homeostasis. J Exp Biol 200:269-286.
10. Chaudhry FA, Lehre KP, van Lookeren Campagne M, Ottersen OP, Danbolt NC, Storm-Mathisen J (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711-720.
11. Clark BA, Barbour B (1997) Currents evoked in Bermann glial cells by parallel fibre stimulation in rat cerebellar slices. J Physiol (Lond) 502:335-350.
12. Clements JD (1996) Transmitter time course in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19:163-171.
13. Clements JD, Lester RAJ, Tong G, Jahr CE, Westbrook GL (1992) The time course of glutamate in the synaptic cleft. Science 258:1498-1501.
14. D'Angelo E, Rossi P, Taglietti V (1993) Different proportions of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptor currents at the mossy fibre-granule cell synapse of developing rat cerebellum. Neuroscience 53:121-130.
15. D'Angelo E, De Filippi G, Rossi P, Taglietti V (1995) Synaptic excitation of individual rat cerebellar granule cells in situ: evidence for the role of NMDA receptors. J Physiol (Lond) 484:397-413.
16. Diamond JS, Jahr CE (1995) Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron 15:1097-1107.
17. Diamond JS, Jahr CE (1997) Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci 17:4672-4687.
18. Ebralidze AK, Rossi DJ, Tonegawa S, Slater NT (1996) Modification of NMDA receptor-channels and synaptic transmission by targeted disruption of the NR2C gene. J Neurosci 16:5014-1525.
19. Edmonds B, Colquhoun D (1992) Rapid decay of averaged single-channel NMDA receptor activations recorded at low agonist concentration. Proc R Soc Lond B Biol Sci 250:279-86.
20. Edwards FA, Konnerth A, Sakmann B, Takahashi T (1989) A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflügers Arch 414:600-612.
21. Eliasof S, Jahr CE (1996) Retinal glial cell glutamate transporter is coupled to an anionic conductance. Proc Natl Acad Sci USA 93:4153-4158.
22. Fairman WA, Vandenberg RA, Arriza JL, Kavanaugh MP, Amara SG (1995) An excitatory amino acid transporter with properties of a ligand-gated chloride conductance. Nature 375:599-603.
23. Furuta A, Martin LJ, Lin C-LG, Dykes-Hoberg M, Rothstein JD (1997) Cellular and synaptic localization of the neuronal glutamate transporters excitatory amino acid transporter 3 and 4. Neuroscience 81:1031-1042.
24. Gerrits NM, Epema AH, van Linge A, Dalm E (1989) The primary vestibulocerebellar projection in the rabbit: absence of primary afferents in the flocculus. Neurosci Lett 105:27-33.
25. Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34:635-660.
26. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100.
27. Hestrin S, Sah P, Nicoll RA (1990) Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5:247-253.
28. Isaacson JS, Nicoll RA (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.
29. Jakab RL (1989) Three-dimensional reconstruction and synaptic architecture of cerebellar glomeruli in the rat. Acta Morphol Hung 37:11-20.
30. Jakab RL, Hámori J (1988) Quantitative morphology and synaptology of cerebellar glomeruli in the rat. Anat Embryol 179:81-88.
31. Kinney GA, Overstreet LS, Slater NT (1997) Prolonged physiological entrapment of glutamate in the synaptic cleft of cerebellar unipolar brush cells. J Neurophysiol 78:1320-1333.
32. Korte G, Mugnaini E (1979) The cerebellar projection of the vestibular nerve in the cat. J Comp Neurol 184:265-278.
33. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC (1995) Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci 15:1835-1853.
34. Lester RAJ, Clements JD, Westbrook GL, Jahr CE (1990) Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346:565-567.
35. Maki R, Robinson MB, Dichter MA (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.
36. Matsui K, Hosoi N, Tachibana M (1999) Active role of glutamate uptake in the synaptic transmission from retinal nonspiking neurons. J Neurosci 19:6755-6766.
37. Mennerick S, Zorumski CF (1994) Glial contributions to excitatory neurotransmission in cultured hippocampal cells. Nature 368:59-62.
38. Mennerick S, Zorumski CF (1995) Presynaptic influence on the time course of fast excitatory synaptic currents in cultured hippocampal cells. J Neurosci 15:3178-3192.
39. Mennerick S, Benz A, Zorumski CF (1996) Components of glial responses to exogenous and synaptic glutamate in rat hippocampal microcultures. J Neurosci 16:55-64.
40. Min MY, Rusakov DA, Kullmann DM (1998) Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fiber synapses: role of glutamate diffusion. Neuron 21:561-570.
41. O'Brien RJ, Fischbach, GD (1986) Modulation of embryonic motorneuron glutamate sensitivity by interneurons and age. J Neurosci 6:3290-3296.
42. Olverman HJ, Jones AW, Watkins JC (1984) L-glutamate has higher affinity than other amino acids for [3H]-D-AP-5 binding sites in rat brain membranes. Nature 307:460-462.
43. Overstreet LS, Liu Y-B, Slater NT (1997) Glutamate transporters sculpt the timecourse of synaptic transmission in cerebellar granule cells. Soc Neurosci Abstr 23:2006.
44. Otis TS, Wu Y-C, Trussell LO (1996) Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J Neurosci 16:634-1644.
45. Otis TS, Kavanaugh MP, Jahr CE (1997) Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277:1515-1518.
46. Patneau DK, Mayer ML (1990) Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10:2385-2399.
47. Rossi DJ, Hamann M (1998) Spillover-mediated transmission at inhibitory synapses promoted by high-affinity α6 subunit GABAA receptors and glomerular geometry. Neuron 20:783-795.
48. Rossi DJ, Slater NT (1993) The developmental onset of NMDA receptor-channel activity during neuronal migration. Neuropharmacology 32:1239-1248.
49. Rothstein JD, Martin L, Levey AI, Dykes-Doberg M, Jin L, Wu D, Nash N, Kuncl RW (1994) Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
50. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveal a major role for astroglial transport in excitoxicity and clearance of glutamate. Neuron 16:675-686.
51. Sarantis M, Ballerini L, Miller B, Silver RA, Edwards M, 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.
52. Silver RA, Traynelis SF, Cull-Candy SG (1992) Rapid-time-course miniature and evoked excitatory currents at cerebellar synapses in situ. Nature 355:163-166.
53. Silver RA, Colquhoun D, Cull-Candy SG, Edmonds B (1996) Deactivation and desensitization of non-NMDA receptors in patches and the time course of EPSCs in rat cerebellar granule cells. J Physiol (Lond) 493:167-173.
54. Slater NT, Kinney GA (1996) Reuptake contributes to the removal of glutamate from the synaptic cleft of rat cerebellar granule and unipolar brush cells. Soc Neurosci Abstr 22:796.
55. Szatkowski M, Barbour B, Attwell D (1990) Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348:443-446.
56. Takahashi M, Kovalchuk Y, Attwell D (1995) Pre- and post-synaptic determinants of EPSC waveform at cerebellar climbing fibre and parallel fibre to Purkinje cell synapses. J Neurosci 15:5693-5707.
57. Takahashi M, Sarantis M, Attwell D (1996a) Postsynaptic glutamate uptake in rat cerebellar Purkinje cells. J Physiol (Lond) 497:523-530.
58. Takahashi T, Feldmeyer D, Suzuki N, Onodera K, Cull-Candy SG, Sakimura K, Mishina M (1996b) Functional correlation of NMDA receptor ∈ subunits expression with the properties of single-channel and synaptic currents in the developing cerebellum. J Neurosci 16:4376-4382.
59. Takahashi M, Billups B, Rossi D, Sarantis M, Hamann M, Attwell D (1997) The role of glutamate transporters in glutamate homeostasis in the brain. J Exp Biol 200:401-409.
60. 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.
61. Tong G, Jahr CE (1994) Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13:1195-1203.
62. Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC (1997) Differential developmental expression of the two rat brain glutamate transport proteins GLAST and GLT. Eur J Neurosci 9:1646-1655.
63. Wadiche JI, Amara SG, Kavanaugh MP (1995a) Ion fluxes associated with excitatory amino acid transport. Neuron 15:721-728.
64. Wadiche JI, Arriza JL, Amara SG, Kavanaugh MP (1995b) Kinetics of a human glutamate transporter. Neuron 14:1019-1027.
65. Wall MJ, Usowicz M (1997) Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9:533-548.
66. Wang GJ, Chung HJ, Schnuer J, Lea E, Robinson MB, Potthoff WK, Aizenman E, Rosenberg PA (1998) Dihydrokainate-sensitive neuronal glutamate transport is required for protection of rat cortical neurons in culture against synaptically released glutamate. Eur J Neurosci 10:2523-2531.
67. Yamada K, Watanabe M, Shibata T, Tanaka K, Wada K, Inoue Y (1996) EAAT4 is a post-synaptic glutamate transporter at Purkinje cell synapses. NeuroReport 7:2013-2017.