The glutamate-aspartate transporter GLAST mediates glutamate uptake at inner hair cell afferent synapses in the mammalian cochlea

Journal of Neuroscience

Volumn 26, Issue 29, 2006, Pages 7659-7664

  Glowatzki, Elisabeth ^a   Cheng, Ning ^b   Hiel, Hakim ^a   Yi, Eunyoung ^a   Tanaka, Kohichi ^c   Ellis Davies, Graham C R ^d   Rothstein, Jeffrey D ^b   Bergles, Dwight E ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

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

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

AMPA receptor; BAC transgenic; EAAT1; GLAST; Glutamate transporter; Hair cell; Organ of Corti; Ribbon synapse

Indexed keywords

ASPARTATE AMINOTRANSFERASE; DEXTRO ASPARTIC ACID; DIHYDROKAINIC ACID; EXCITATORY AMINO ACID TRANSPORTER; GLUTAMIC ACID; GLUTAMATE TRANSPORTER;

ANIMAL TISSUE; ARTICLE; COCHLEA; CONTROLLED STUDY; CORTI ORGAN; DENDRITE; GLIA CELL; HAIR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPSE; TRANSGENIC MOUSE; ANIMAL; COCHLEAR NERVE; CYTOLOGY; ELECTRIC CONDUCTIVITY; GENETICS; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; PROMOTER REGION; SENSORY NERVE CELL; ULTRASTRUCTURE;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; COCHLEA; COCHLEAR NERVE; DENDRITES; ELECTRIC CONDUCTIVITY; GLUTAMIC ACID; HAIR CELLS, INNER; MICE; MICE, TRANSGENIC; NEURONS, AFFERENT; ORGAN OF CORTI; PROMOTER REGIONS (GENETICS); RATS; SYNAPSES;

EID: 33747080821     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1545-06.2006     Document Type: Article

References (37)

1. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, Amara SG (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 14:5559-5569.
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. Basile AS, Huang JM, Xie C, Webster D, Berlin C, Skolnick P (1996) N-methyl-D-aspartate antagonists limit aminoglycoside antibiotic-induced hearing loss. Nat Med 2:1338-1343.
4. Bergles DE, Jahr CE (1997) Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19:1297-1308.
5. Bergles DE, Jahr CE (1998) Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J Neurosci 18:7709-7716.
6. 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.
7. Bergles DE, Diamond JS, Jahr CE (1999) Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol 9:293-298.
8. 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.
9. Brasnjo G, Otis TS (2004) Isolation of glutamate transport-coupled charge flux and estimation of glutamate uptake at the climbing fiber-Purkinje cell synapse. Proc Natl Acad Sci USA 101:6273-6278.
10. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192.
11. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.
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. Fuchs PA, Glowatzki E, Moser T (2003) The afferent synapse of cochlear hair cells. Curr Opin Neurobiol 13:452-458.
14. Furness DN, Lawton DM (2003) Comparative distribution of glutamate transporters and receptors in relation to afferent innervation density in the mammalian cochlea. J Neurosci 23:11296-11304.
15. Furness DN, Lehre KP (1997) Immunocytochemical localization of a high-affinity glutamate-aspartate transporter, GLAST, in the rat and guinea-pig cochlea. Eur J Neurosci 9:1961-1969.
16. Furness DN, Hulme JA, Lawton DM, Hackney CM (2002) Distribution of the glutamate/aspartate transporter GLAST in relation to the afferent synapses of outer hair cells in the guinea pig cochlea. J Assoc Res Otolaryngol 3:234-247.
17. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5:147-154.
18. Hakuba N, Koga K, Gyo K, Usami S-I, Tanaka K (2000) Exacerbation of noise-induced hearing loss in mice lacking the glutamate transporter GLAST. J Neurosci 20:8750-8753.
19. Hakuba N, Matsubara A, Hyodo J, Taniguchi M, Maetani T, Shimizu Y, Tsujiuchi Y, Shudou M, Gyo K (2003) AMPA/kainate-type glutamate receptor antagonist reduces progressive inner hair cell loss after transient cochlear ischemia. Brain Res 979:194-202.
20. Huang YH, Dykes-Hoberg M, Tanaka K, Rothstein JD, Bergles DE (2004a) Climbing fiber activation of EAAT4 transporters and kainate receptors in cerebellar Purkinje cells. J Neurosci 24:103-111.
21. Huang YH, Sinha SR, Tanaka K, Rothstein JD, Bergles DE (2004b) Astrocyte glutamate transporters regulate metabotropic glutamate receptor-mediated excitation of hippocampal interneurons. J Neurosci 24:4551-4559.
22. Huang YH, Sinha SR, Fedoryak OD, Ellis-Davies GC, Bergles DE (2005) Synthesis and characterization of 4-methoxy-7-nitroindolinyl-D-aspartate, a caged compound for selective activation of glutamate transporters and N-methyl-D-aspartate receptors in brain tissue. Biochemistry 44:3316-3326.
23. Jin ZH, Kikuchi T, Tanaka K, Kobayashi T (2003) Expression of glutamate transporter GLAST in the developing mouse cochlea. Tohoku J Exp Med 200:137-144.
24. 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.
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. Li HS, Niedzielski AS, Beisel KW, Hiel H, Wenthold RJ, Morley BJ (1994) Identification of a glutamate/aspartate transporter in the rat cochlea. Hear Res 78:235-242.
27. Otis TS, Kavanaugh MP, Jahr CE (1997) Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277:1515-1518.
28. Ottersen OP, Takumi Y, Matsubara A, Landsend AS, Laake JH, Usami S (1998) Molecular organization of a type of peripheral glutamate synapse: the afferent synapses of hair cells in the inner ear. Prog Neurobiol 54:127-148.
29. Palmer MJ, Taschenberger H, Hull C, Tremere L, von Gersdorff H (2003) Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. J Neurosci 23:4831-4841.
30. Rebillard G, Ruel J, Nouvian R, Saleh H, Pujol R, Dehnes Y, Raymond J, Puel JL, Devau G (2003) Glutamate transporters in the guinea-pig cochlea: partial mRNA sequences, cellular expression and functional implications. Eur J Neurosci 17:83-92.
31. Robertson D (1983) Functional significance of dendritic swelling after loud sounds in the guinea pig cochlea. Hear Res 9:263-278.
32. 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.
33. 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.
34. Trussell LO (1999) Synaptic mechanisms for coding timing in auditory neurons. Annu Rev Physiol 61:477-496.
35. Wadiche JI, Kavanaugh MP (1998) Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J Neurosci 18:7650-7661.
36. Wadiche JI, Amara SG, Kavanaugh MP (1995) Ion fluxes associated with excitatory amino acid transport. Neuron 15:721-728.
37. Yang XW, Model P, Heintz N (1997) Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat Biotechnol 15:859-865.