Glial glutamate transporters maintain one-to-one relationship at the climbing fiber-Purkinje cell synapse by preventing glutamate spillover

Journal of Neuroscience

Volumn 26, Issue 24, 2006, Pages 6563-6572

  Takayasu, Yukihiro ^a   Iino, Masae ^a   Shimamoto, Keiko ^b   Tanaka, Kohichi ^c   Ozawa, Seiji ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SUNTORY INSTITUTE FOR BIOORGANIC RESEARCH   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Climbing fiber; EPSC; GLAST; Glutamate transporter; Multiple innervation; Purkinje cell

Indexed keywords

3 [3 (4 METHOXYBENZOYLAMINO)BENZYLOXY]ASPARTATE; GAMMA DEXTRO GLUTAMYLGLYCINE; GLIAL GLUTAMATE TRANSPORTER; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR STIMULATING AGENT; ASPARTIC ACID; BENZOTHIADIAZINE DERIVATIVE; BENZYLOXYASPARTATE; CYCLOTHIAZIDE; DRUG DERIVATIVE; EXCITATORY AMINO ACID TRANSPORTER 1; METHACRYLIC ACID DERIVATIVE; PHOSPHORYLCHOLINE; POLY(2 METHACRYLOYLOXYETHYL PHOSPHORYLCHOLINE CO N BUTYL METHACRYLATE); POLY(2-METHACRYLOYLOXYETHYL PHOSPHORYLCHOLINE-CO-N-BUTYL METHACRYLATE);

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CLIMBING FIBER; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GLIA CELL; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RAT; SYNAPTIC MEMBRANE; ANIMAL; C57BL MOUSE; CEREBELLUM; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; ELECTROSTIMULATION; IN VITRO STUDY; METABOLISM; METHODOLOGY; MOUSE MUTANT; NERVE CELL INHIBITION; NERVE FIBER; NEWBORN; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION RESPONSE; SYNAPSE;

ANIMALS; ANIMALS, NEWBORN; ASPARTIC ACID; BENZOTHIADIAZINES; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; METHACRYLATES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE FIBERS; NEURAL INHIBITION; PHOSPHORYLCHOLINE; PURKINJE CELLS; SYNAPSES;

EID: 33745798873     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5342-05.2006     Document Type: Article

References (62)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
2. Arriza JL, Eliasof S, Kavanaugh MP, Amara SG (1997) Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci USA 94:4155-4160.
3. Batchelor AM, Garthwaite J (1997) Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature 385:74-77.
4. Carter AG, Regehr WG (2000) Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse. J Neurosci 20:4423-4434.
5. 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.
6. Chen C, Kano M, Abeliovich A, Chen L, Bao S, Kim JJ, Hashimoto K, Thompson RF, Tonegawa S (1995) Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKC gamma mutant mice. Cell 83:1233-1242.
7. Clark BA, Cull-Candy SG (2002) Activity-dependent recruitment of extra-synaptic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 22:4428-4436.
8. Clements JD, Lester RA, Tong G, Jahr CE, Westbrook GL (1992) The time course of glutamate in the synaptic cleft. Science 258:1498-1501.
9. Crépel F (1982) Regression of functional synapses in the immature mammalian cerebellum. Trends Neurosci 5:266-269.
10. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.
11. 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.
12. Diamond JS (2001) Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells. J Neurosci 21:8328-8338.
13. DiGregorio DA, Nusser Z, Silver RA (2002) Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse. Neuron 35:521-533.
14. Dzubay JA, Jahr CE (1999) The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J Neurosci 19:5265-5274.
15. Dzubay JA, Otis TS (2002) Climbing fiber activation of metabotropic glutamate receptors on cerebellar Purkinje neurons. Neuron 36:1159-1167.
16. Eccles JC, Ito M, Szentagothai J (1967) The cerebellum as a neuronal machine. New York: Springer.
17. Eliasof S, Arriza JL, Leighton BH, Kavanaugh MP, Amara SG (1998) Excitatory amino acid transporters of the salamander retina: identification, localization, and function. J Neurosci 18:698-712.
18. 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.
19. Furuta A, Martin LJ, Lin CL, 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.
20. Harrison J, Jahr CE (2003) Receptor occupancy limits synaptic depression at climbing fiber synapses. J Neurosci 23:377-383.
21. Hashimoto K, Kano M (2005) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38:785-796.
22. Hashimoto K, Ichikawa R, Takechi H, Inoue Y, Aiba A, Sakimura K, Mishina M, Hashikawa T, Konnerth A, Watanabe M, Kano M (2001) Roles of glutamate receptor δ2 subunit (GluRδ2) and metabotropic glutamate receptor subtype 1 (mGluR1) in climbing fiber synapse elimination during postnatal cerebellar development. J Neurosci 21:9701-9712.
23. Huang YH, Dykes-Hoberg M, Tanaka K, Rothstein JD, Bergles DE (2004) Climbing fiber activation of EAAT4 transporters and kainate receptors in cerebellar Purkinje cells. J Neurosci 24:103-111.
24. Ichikawa R, Miyazaki T, Kano M, Hashikawa T, Tatsumi H, Sakimura K, Mishina M, Inoue Y, Watanabe M (2002) Distal extension of climbing fiber territory and multiple innervation caused by aberrant wiring to adjacent spiny branchlets in cerebellar Purkinje cells lacking glutamate receptor δ2. J Neurosci 22:8487-8503.
25. 2+-permeable AMPA receptors in Bergmann glia. Science 292:926-929.
26. Johnston D, Brown TH (1983) Interpretation of voltage-clamp measurements in hippocampal neurons. J Neurophysiol 50:464-486.
27. Kanai Y, Hediger MA (1992) Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360:467-471.
28. Kano M, Hashimoto K, Chen C, Abeliovich A, Aiba A, Kurihara H, Watanabe M, Inoue Y, Tonegawa S (1995) Impaired synapse elimination during cerebellar development in PKCγ mutant mice. Cell 83:1223-1231.
29. Kano M, Hashimoto K, Kurihara H, Watanabe M, Inoue Y, Aiba A, Tonegawa S (1997) Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron 18:71-79.
30. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y, Aizawa S, Mishina M (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluRδ2 mutant mice. Cell 81:245-252.
31. Konnerth A, Llano I, Armstrong CM (1990) Synaptic currents in cerebellar Purkinje cells. Proc Natl Acad Sci USA 87:2662-2665.
32. 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.
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. Li P, Wilding TJ, Kim SJ, Calejesan AA, Huettner JE, Zhuo M (1999) Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature 397:161-164.
35. Liu G, Choi S, Tsien RW (1999) Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22:395-409.
36. Llano I, Marty A, Armstrong CM, Konnerth A (1991) Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J Physiol (Lond) 434:183-213.
37. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349:760-765.
38. Matsui K, Jahr CE (2003) Ectopic release of synaptic vesicles. Neuron 40:1173-1183.
39. Matsui K, Jahr CE (2004) Differential control of synaptic and ectopic vesicular release of glutamate. J Neurosci 24:8932-8939.
40. Offermanns S, Hashimoto K, Watanabe M, Sun W, Kurihara H, Thompson RF, Inoue Y, Kano M, Simon MI (1997) Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Gαq. Proc Natl Acad Sci USA 94:14089-14094.
41. Otis TS, Kavanaugh MP, Jahr CE (1997) Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277:1515-1518.
42. Partin KM, Patneau DK, Mayer ML (1994) Cyclothiazide differentially modulates desensitization of α-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid receptor splice variants. Mol Pharmacol 46:129-138.
43. Patneau DK, Vyklicky Jr L, Mayer ML (1993) Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. J Neurosci 13:3496-3509.
44. Pelletier JC, Hesson DP, Jones KA, Costa AM (1996) Substituted 1,2-dihydrophthalazines: potent, selective, and noncompetitive inhibitors of the AMPA receptor. J Med Chem 39:343-346.
45. Pines G, Danbolt NC, Bjoras M, Zhang Y, Bendahan A, Eide L, Koepsell H, Storm-Mathisen J, Seeberg E, Kanner BI (1992) Cloning and expression of a rat brain L-glutamate transporter. Nature 360:464-467.
46. A receptors and glomerular geometry. Neuron 20:783-795.
47. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW (1994) Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
48. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N, Nakajima T (1998) DL-threo-β-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53:195-201.
49. Shimamoto K, Sakai R, Takaoka K, Yumoto N, Nakajima T, Amara SG, Shigeri Y (2004) Charactarization of novel L-threo-β-benzyloxyaspartate derivatives, potent blockers of the glutamate transporters. Mol Pharmacol 65:1008-1015.
50. 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.
51. +-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci USA 89:10955-10959.
52. Takatsuru Y, Takayasu Y, Iino M, Nikkuni O, Ueda Y, Tanaka K, Ozawa S (2006) Roles of glial glutamate transporters in shaping EPSCs at the climbing fiber-Purkinje cell synapses. Neurosci Res 54:140-148.
53. Takayasu Y, Iino M, Ozawa S (2004) Roles of glutamate transporters in shaping excitatory synaptic currents in cerebellar Purkinje cells. Eur J Neurosci 19:1285-1295.
54. Takayasu Y, Iino M, Kakegawa W, Maeno H, Watase K, Wada K, Yanagihara D, Miyazaki T, Komine O, Watanabe M, Tanaka K, Ozawa S (2005) Differential roles of glial and neuronal glutamate transporters in Purkinje cell synapses. J Neurosci 25:8788-8793.
55. Tanaka J, Ichikawa R, Watanabe M, Tanaka K, Inoue Y (1997) Extra-junctional localization of glutamate transporter EAAT4 at excitatory Purkinje cell synapses. NeuroReport 8:2461-2464.
56. Tanaka K (1994) Pharmacological characterization of a cloned rat glutamate transporter (GluT-1). Brain Res Mol Brain Res 21:167-170.
57. Thompson CL, Drewery DL, Atkins HD, Stephenson FA, aChazot 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.
58. Yamada KA, Tang CM (1993) Benzothiadiazides inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents. J Neurosci 13:3904-3915.
59. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32:301-313.
60. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M, Inoue Y, Okuyama S, Sakagawa T, Ogawa S, Kawashima N, Hori S, Takimoto M, Wada K, Tanaka K (1998) Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 10:976-988.
61. Watkins JC (1991) Some chemical highlights in the development of excitatory amino acid pharmacology. Can J Physiol Pharmacol 69:1064-1075.
62. Wisden W, Seeburg PH (1993) A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13:3582-3598.