Climbing Fiber Activation of EAAT4 Transporters and Kainate Receptors in Cerebellar Purkinje Cells

Journal of Neuroscience

Volumn 24, Issue 1, 2004, Pages 103-111

  Huang, Yanhua H ^a   Dykes Hoberg, Margaret ^a   Tanaka, Kohichi ^b   Rothstein, Jeffrey D ^a   Bergles, Dwight E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Cerebellum; EAAC1; EAAT4; EPSC; GluR5; Glutamate transporter; Kainate receptor; Purkinje neuron

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMIC ACID; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR; PROTEIN EAAC1; PROTEIN EAAT4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CLIMBING FIBER; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; KNOCKOUT MOUSE; MEMBRANE CURRENT; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RECEPTOR INTRINSIC ACTIVITY; RECEPTOR OCCUPANCY; SYNAPSE; WILD TYPE;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; CELLS, CULTURED; CEREBELLUM; ELECTRIC CONDUCTIVITY; EXCITATORY AMINO ACID TRANSPORTER 3; EXCITATORY AMINO ACID TRANSPORTER 4; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; KINETICS; MICE; MICE, KNOCKOUT; NERVE FIBERS; PURKINJE CELLS; RATS; RECEPTORS, GLUTAMATE; RECEPTORS, KAINIC ACID; SYMPORTERS; SYNAPSES;

EID: 0842301342     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4473-03.2004     Document Type: Article

References (51)

1. Arnth-Jensen N, Jabaudon D, Scanziani M (2002) Cooperation between independent hippocampal synapses is controlled by glutamate uptake. Nat Neurosci 5:325-331.
2. Auger C, Attwell D (2000) Fast removal of synaptic glutamate by postsynaptic transporters. Neuron 28:547-558.
3. 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.
4. 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.
5. Bergles DE, Tzingounis AV, Jahr CE (2002) Comparison of coupled and uncoupled currents during glutamate uptake by GLT-1 transporters. J Neurosci 22:10153-10162.
6. Bortolotto ZA, Clarke VR, Delany CM, Parry MC, Smolders I, Vignes M, Ho KH, Miu P, Brinton BT, Fantaske R, Ogden A, Gates M, Ornstein PL, Lodge D, Bleakman D, Collingridge GL (1999) Kainate receptors are involved in synaptic plasticity. Nature 402:297-301.
7. 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.
8. Brickley S, Swanson G, Contractor A, Farrant M, Sailer A, Cull-Candy S, Heinemann S (1999) Functional GluR5-containing kainate receptors are restricted to extrasynaptic sties in Purkinje cells of the mouse cerebellum. J Physiol (Lond) 521:90P.
9. Bureau I, Dieudonne S, Coussen F, Mulle C (2000) Kainate receptor-mediated synaptic currents in cerebellar Golgi cells are not shaped by diffusion of glutamate. Proc Natl Acad Sci USA 97:6838-6843.
10. Contractor A, Swanson GT, Sailer A, O'Gorman S, Heinemann SF (2000) Identification of the kainate receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. J Neurosci 20:8269-8278.
11. Cossart R, Epsztein J, Tyzio R, Becq H, Hirsch J, Ben-Ari Y, Crepel V (2002) Quantal release of glutamate generates pure kainate and mixed AMPA/kainate EPSCs in hippocampal neurons. Neuron 35:147-159.
12. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.
13. 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.
14. Diamond JS (2001) Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells. J Neurosci 21:8328-8338.
15. Diamond JS, Jahr CE (1997) Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci 17:4672-4687.
16. Dzubay JA, Otis TS (2002) Climbing fiber activation of metabotropic glutamate receptors on cerebellar purkinje neurons. Neuron 36:1159-1167.
17. 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.
18. Frerking M, Ohliger-Frerking P (2002) AMPA receptors and kainate receptors encode different features of afferent activity. J Neurosci 22:7434-7443.
19. Harrison J, Jahr CE (2003) Receptor occupancy limits synaptic depression at climbing fiber synapses. J Neurosci 23:377-383.
20. Hausser M, Roth A (1997) Dendritic and somatic glutamate receptor channels in rat cerebellar Purkinje cells. J Physiol (Lond) 501:77-95.
21. 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.
22. Jabaudon D, Shimamoto K, Yasuda-Kamatani Y, Scanziani M, Gahwiler BH, Gerber U (1999) Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc Natl Acad Sci USA 96:8733-8738.
23. Kidd FL, Isaac JT (2001) Kinetics and activation of postsynaptic kainate receptors at thalamocortical synapses: role of glutamate clearance. J Neurophysiol 86:1139-1148.
24. Lehre KP, Danbolt NC (1998) The number of glutamate transporter sub-type molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18:8751-8757.
25. 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.
26. Lerma J (2003) Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4:481-495.
27. Lerma J, Paternain AV, Rodriguez-Moreno A, Lopez-Garcia JC (2001) Molecular physiology of kainate receptors. Physiol Rev 81:971-998.
28. Otis TS, Wu YC, Trussell LO (1996) Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J Neurosci 16:1634-1644.
29. Otis TS, Kavanaugh MP, Jahr CE (1997) Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277:1515-1518.
30. Paternain AV, Morales M, Lerma J (1995) Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14:185-189.
31. Peghini P, Janzen J, Stoffel W (1997) Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J 16:3822-3832.
32. Perkel DJ, Hestrin S, Sah P, Nicoll RA (1990) Excitatory synaptic currents in Purkinje cells. Proc R Soc Lond B Biol Sci 241:116-121.
33. Rammes G, Swandulla D, Spielmanns P, Parsons CG (1998) Interactions of GYKI 52466 and NBQX with cyclothiazide at AMPA receptors: experiments with outside-out patches and EPSCs in hippocampal neurones. Neuropharmacology 37:1299-1320.
34. 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.
35. 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 reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686.
36. Rozas JL, Paternain AV, Lerma J (2003) Noncanonical signaling by ionotropic kainate receptors. Neuron 39:543-553.
37. Sepkuty JP, Cohen AS, Eccles C, Rafiq A, Behar K, Ganel R, Coulter DA, Rothstein JD (2002) A neuronal glutamate transporter contributes to neurotransmitter GABA synthesis and epilepsy 22:6372-6379.
38. 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.
39. 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.
40. Shimamoto K, Shigeri Y, Yasuda-Kamatani Y, Lebrun B, Yumoto N, Nakajima T (2000) Syntheses of optically pure beta-hydroxyaspartate derivatives as glutamate transporter blockers. Bioorg Med Chem Lett 10:2407-2410.
41. Silver RA, Momiyama A, Cull-Candy SG (1998) Locus of frequency-dependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses. J Physiol (Lond) 510:881-902.
42. Spacek J (1985) Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat Embryol (Berl) 171:245-252.
43. Swanson GT, Heinemann SF (1998) Heterogeneity of homomeric GluR5 kainate receptor desensitization expressed in HEK293 cells. J Physiol (Lond) 513:639-646.
44. Tamaru Y, Nomura S, Mizuno N, Shigemoto R (2001) Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106:481-503.
45. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Hori S, Takimoto M, Wada K (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1 276:1699-1702.
46. Tong G, Jahr CE (1994) Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13:1195-1203.
47. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19:6897-6906.
48. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32:301-313.
49. Wadiche JI, Amara SG, Kavanaugh MP (1995) Ion fluxes associated with excitatory amino acid transport. Neuron 15:721-728.
50. Wisden W, Seeburg PH (1993) A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13:3582-3598.
51. Yuzaki M, Forrest D, Curran T, Connor JA (1996) Selective activation of calcium permeability by aspartate in Purkinje cells. Science 273:1112-1114.