Glial glutamate transporters limit spillover activation of presynaptic NMDA receptors and influence synaptic inhibition of Purkinje neurons

Journal of Neuroscience

Volumn 24, Issue 25, 2004, Pages 5659-5669

  Huang, Hao ^a   Bordey, Angélique ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocyte; Cerebellum; Glial cells; Glutamate uptake; Patch clamp; Slice

Indexed keywords

3 BENZYLOXYASPARTIC ACID; ANTIPORTER; ASPARTIC ACID DERIVATIVE; CYSTINE; CYSTINE GLUTAMATE ANTIPORTER; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RYANODINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BERGMANN GLIA LAYER; BRAIN SLICE; CEREBELLUM; CONTROLLED STUDY; EVOKED INHIBITORY POSTSYNAPTIC CURRENT; EVOKED RESPONSE; GABAERGIC TRANSMISSION; GLIA; INHIBITORY POSTSYNAPTIC POTENTIAL; MEASUREMENT; MINIATURE INHIBITORY POSTSYNAPTIC CURRENT; MOUSE; NEUROTRANSMITTER UPTAKE; NEWBORN; NONHUMAN; PAIRED PULSE RATIO; PATCH CLAMP; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PURKINJE CELL;

ACTION POTENTIALS; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ANTIPORTERS; CALCIUM; CEREBELLUM; CYSTINE; EVOKED POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MICE; NERVE FIBERS; NEURAL INHIBITION; NEUROGLIA; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, PRESYNAPTIC; RYANODINE; SYNAPTIC TRANSMISSION;

EID: 3042780934     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1338-04.2004     Document Type: Article

References (67)

1. Akazawa C, Shigemoto R, Bessho Y, Nakanishi S, Mizuno N (1994) Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in the cerebellum of developing and adult rats. J Comp Neurol 347:150-160.
2. Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1-14.
3. 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.
4. Auger C, Attwell D (2000) Fast removal of synaptic glutamate by postsynaptic transporters. Neuron 28:547-558.
5. Baker DA, Xi ZX, Shen H, Swanson CJ, Kalivas PW (2002) The origin and neuronal function of in vivo nonsynaptic glutamate. J Neurosci 22:9134-9141.
6. 2+ stores contribute to inhibitory neurotransmitter release onto mouse cerebellar Purkinje cells. Br J Pharmacol 137:529-537.
7. Bender AS, Reichelt W, Norenberg MD (2000) Characterization of cystine uptake in cultured astrocytes. Neurochem Int 37:269-276.
8. Bergles DE, Dzubay JA, Jahr CE (1997) Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate. Proc Natl Acad Sci USA 94:14821-14825.
9. Bordey A, Sontheimer H (2000) Ion channel expression by astrocytes in situ: comparison of different CNS regions. Glia 30:27-38.
10. Bordey A, Sontheimer H (2003) Modulation of glutamatergic transmission by bergmann glial cells in rat cerebellum in situ. J Neurophysiol 89:979-988.
11. Brasnjo G, Otis TS (2001) Neuronal glutamate transporters control activation of postsynaptic metabotropic glutamate receptors and influence cerebellar long-term depression. Neuron 31:607-616.
12. Caillard O, Ben Ari Y, Gaiarsa JL (2000) Activation of presynaptic and postsynaptic ryanodine-sensitive calcium stores is required for the induction of long-term depression at GABAergic synapses in the neonatal rat hippocampus amphetamine. J Neurosci 20:RC94(1-5).
13. 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.
14. Clark BA, Barbour B (1997) Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices. J Physiol (Lond) 502:335-350.
15. Cossart R, Tyzio R, Dinocourt C, Esclapez M, Hirsch JC, Ben Ari Y, Bernard C (2001) Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 29:497-508.
16. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.
17. de Blas AL (1984) Monoclonal antibodies to specific astroglial and neuronal antigens reveal the cytoarchitecture of the Bergmann glia fibers in the cerebellum. J Neurosci 4:265-273.
18. Dehnes Y, Chaudhry FA, Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC (1998) The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J Neurosci 18:3606-3619.
19. Diana MA, Levenes C, Mackie K, Marty A (2002) Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22:200-208.
20. Duan S, Anderson CM, Stein BA, Swanson RA (1999) Glutamate induces rapid upregulation of astrocyte glutamate transport and cell-surface expression of GLAST. J Neurosci 19:10193-10200.
21. Duguid IC, Smart TG (2004) Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nat Neurosci 7:525-533.
22. 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.
23. Emptage N, Bliss TV, Fine A (1999) Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22:115-124.
24. Fairman WA, Vandenberg RJ, Arriza JL, Kavanaugh MP, Amara SG (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375:599-603.
25. Farrant M, Cull-Candy SG (1991) Excitatory amino acid receptor-channels in Purkinje cells in thin cerebellar slices. Proc R Soc Lond B Biol Sci 244:179-184.
26. Furuta A, Rothstein JD, Martin LJ (1997) Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17:8363-8375.
27. Galante M, Marty A (2003) Presynaptic ryanodine-sensitive calcium stores contribute to evoked neurotransmitter release at the basket cell-Purkinje cell synapse. J Neurosci 23:11229-11234.
28. Gegelashvili G, Robinson MB, Trotti D, Rauen T (2001) Regulation of glutamate transporters in health and disease. Prog Brain Res 132:267-286.
29. Glitsch M, Marty A (1999) Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J Neurosci 19:511-519.
30. He Y, Janssen WG, Rothstein JD, Morrison JH (2000) Differential synaptic localization of the glutamate transporter EAAC1 and glutamate receptor subunit GluR2 in the rat hippocampus. J Comp Neurol 418:255-269.
31. Jiang L, Xu J, Nedergaard M, Kang J (2001) A kainate receptor increases the efficacy of GABAergic synapses. Neuron 30:503-513.
32. Kataoka Y, Morii H, Watanabe Y, Ohmori H (1997) A postsynaptic excitatory amino acid transporter with chloride conductance functionally regulated by neuronal activity in cerebellar Purkinje cells. J Neurosci 17:7017-7024.
33. Khakh BS, Henderson G (2000) Modulation of fast synaptic transmission by presynaptic ligand-gated cation channels. J Auton Nerv Syst 81:110-121.
34. King JS, Chen YF, Bishop GA (1993) An analysis of HRP-filled basket cell axons in the cat's cerebellum. II. Axonal distribution. Anat Embryol (Berl) 188:299-305.
35. Kreitzer AC, Regehr WG (2001a) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
36. Kreitzer AC, Regehr WG (2001b) Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21:RC174(1-5).
37. Kullmann DM (2001) Presynaptic kainate receptors in the hippocampus: slowly emerging from obscurity. Neuron 32:561-564.
38. Lehre KP, Danbolt NC (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.
39. Llano I, Gonzalez J, Caputo C, Lai FA, Blayney LM, Tan YP, Marty A (2000) Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci 3:1256-1265.
40. Marcaggi P, Billups D, Attwell D (2003) The role of glial glutamate transporters in maintaining the independent operation of juvenile mouse cerebellar parallel fibre synapses. J Physiol (Lond) 552:89-107.
41. Min MY, Melyan Z, Kullmann DM (1999) Synaptically released glutamate reduces gamma-aminobutyric acid (GABA)ergic inhibition in the hippocampus via kainate receptors. Proc Natl Acad Sci USA 96:9932-9937.
42. Minelli A, Barbaresi P, Reimer RJ, Edwards RH, Conti F (2001) The glial glutamate transporter GLT-1 is localized both in the vicinity of and at distance from axon terminals in the rat cerebral cortex. Neuroscience 108:51-59.
43. Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923-926.
44. Otis TS, Kavanaugh MP, Jahr CE (1997) Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277:1515-1518.
45. Palacin M, Estevez R, Bertran J, Zorzano A (1998) Molecular biology of mammalian plasma membrane amino acid transporters. Physiol Rev 78:969-1054.
46. Palay SL, Chan-Palay V (1974a) The basket cell. In: Cerebellar cortex, cytology and organization (Palay SL, Chan-Palay V, eds), pp 180-215. New York: Springer.
47. Palay SL, Chan-Palay V (1974b) The climbing fiber. In: Cerebellar cortex, cytology and organization (Palay SL, Chan-Palay V, eds), pp 236. New York: Springer.
48. Petralia RS, Wang YX, Wenthold RJ (1994) The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14:6102-6120.
49. Rall W (1977) Core conductor theory and cable properties of neurons. In: Handbook of physiology, Sec I, The nervous system (Kandel ER, ed), pp 39-97. Bethesda, MD: American Physiological Society.
50. 2+ from separate presynaptic and postsynaptic intracellular stores. J Neurosci 16:5951-5960.
51. Rosenmund C, Legendre P, Westbrook GL (1992) Expression of NMDA channels on cerebellar Purkinje cells acutely dissociated from newborn rats. J Neurophysiol 68:1901-1905.
52. Satake S, Saitow F, Yamada J, Konishi S (2000) Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons. Nat Neurosci 3:551-558.
53. Schwartz EA, Tachibana M (1990) Electrophysiology of glutamate and sodium co-transport in a glial cell of the salamander retina. J Physiol (Lond) 426:43-80.
54. Shigeri Y, Shimamoto K, Yasuda-Kamatani Y, Seal RP, Yumoto N, Nakajima T, Amara SG (2001) Effects of threo-beta-hydroxyaspartate derivatives on excitatory amino acid transporters (EAAT4 and EAAT5). J Neurochem 79:297-302.
55. 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.
56. 2+ stores: activation and function. Trends Neurosci 18:299-306.
57. Soltesz I, Smetters DK, Mody I (1995) Tonic inhibition originates from synapses close to the soma. Neuron 14:1273-1283.
58. Spruston N, Jaffe DB, Williams SH, Johnston D (1993) Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J Neurophysiol 70:781-802.
59. Stuart G, Hausser M (1994) Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13:703-712.
60. Swanson LW, Duan S (1999) Regulation of glutamate transporter function. The Neuroscientist 5:280-282.
61. TTakahashi KA, Linden DJ (2000) Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. J Neurophysiol 83:1167-1180.
62. Takahashi M, Sarantis M, Attwell D (1996) Postsynaptic glutamate uptake in rat cerebellar purkinje cells. J Physiol (Lond) 497.2:523-530.
63. Thompson CL, Drewery DL, Atkins HD, Stephenson FA, Chazot PL (2000) Immunohistochemical localization of N-methyl-D-aspartate receptor NR1, NR2A, NR2B and NR2C/D subunits in the adult mammalian cerebellum. Neurosci Lett 283:85-88.
64. Tsai MJ, Chang YF, Schwarcz R, Brookes N (1996) Characterization of L-alpha-aminoadipic acid transport in cultured rat astrocytes. Brain Res 741:166-173.
65. Wadiche JI, Arriza JL, Amara SG, Kavanaugh MP (1995) Kinetics of a human glutamate transporter. Neuron 14:1019-1027.
66. Warr O, Takahashi M, Attwell D (1999) Modulation of extracellular glutamate concentration in rat brain slices by cystine-glutamate exchange. J Physiol (Lond) 514:783-793.
67. Yamada K, Fukaya M, Shibata T, Kurihara H, Tanaka K, Inoue Y, Watanabe M (2000) Dynamic transformation of Bergmann glial fibers proceeds in correlation with dendritic outgrowth and synapse formation of cerebellar Purkinje cells. J Comp Neurol 418:106-120.