High-affinity Na+/K+-dependent glutamate transporter EAAT4 is expressed throughout the rat fore- and midbrain

Journal of Comparative Neurology

Volumn 511, Issue 2, 2008, Pages 155-172

  Massie, Ann ^a   Cnops, Lieselotte ^b   Smolders, Ilse ^a   McCullumsmith, Robert ^c   Kooijman, Ron ^a   Kwak, Shin ^d   Arckens, Lutgarde ^b   Michotte, Yvette ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

Distribution; EAAT4; Fore and midbrain; Immunohistochemistry; in situ hybridization; Real time PCR

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER 4; MESSENGER RNA; SLC1A6 PROTEIN, RAT; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN REGION; CELLULAR DISTRIBUTION; CEREBELLUM; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FOREBRAIN; HIPPOCAMPUS; IN SITU HYBRIDIZATION; INTERPEDUNCULAR NUCLEUS; MALE; MESENCEPHALON; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBICULUM; SUBSTANTIA NIGRA; SUPERIOR COLLICULUS; SUPRAOPTIC NUCLEUS; THALAMUS POSTERIOR NUCLEUS; TISSUE DISTRIBUTION; VENTRAL TEGMENTUM; ANIMAL; CYTOLOGY; GENETICS; HISTOLOGY; HUMAN; METABOLISM; MOUSE MUTANT; NERVE CELL; WISTAR RAT;

ANIMALS; EXCITATORY AMINO ACID TRANSPORTER 4; HUMANS; IN SITU HYBRIDIZATION; MALE; MESENCEPHALON; MICE; MICE, KNOCKOUT; NEURONS; PROSENCEPHALON; RATS; RATS, WISTAR;

EID: 58149240677     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21823     Document Type: Article

References (112)

1. Albin RL, Marcowiec RL, Hollingsworth ZR, Dure LS, Penney JB, Young AB. 1992. Excitatory amino acid binding sites in the basal ganglia of the rat: a quantitative autoradiographic study. Neuroscience 46:35-48.
2. Amaral DG. 1978. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182:851-914.
3. Ampe B, Massie A, D'Haens J, Ebinger G, Michotte Y, Sarre S. 2007. NMDA-mediated release of glutamate and GABA in the subthalamic nucleus is mediated by dopamine: an in vivo microdialysis study in rats. J Neurochem 103:1063-1074.
4. 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 U S A 94:4155-4160.
5. Attwell D. 2000. Brain uptake of glutamate: food for thought. J Nutr 130:1023S-1025S.
6. Bar-Peled O, Ben-Hur H, Biegon A, Groner Y, Dewhurst S, Furuta A, Rothstein JD. 1997. Distribution of glutamate transporter subtypes during human brain development. J Neurochem 69:2571-2580.
7. Berger UV, Hediger MA. 1998. Comparative analysis of glutamate transporter expression in rat brain using differential double in situ hybridization. Anat Embryol (Berl) 198:13-30.
8. Berger UV, Hediger MA. 2000. Distribution of the glutamate transporters GLAST and GLT-1 in rat circumventricular organs, meninges, and dorsal root ganglia. J Comp Neurol 421:385-399.
9. Berger UV, Hediger MA. 2001. Differential distribution of the glutamate transporters GLT-1 and GLAST in tanycytes of the third ventricle. J Comp Neurol 433:101-114.
10. Berger UV, DeSilva TM, Chen W, Rosenberg PA. 2005. Cellular and subcellular mRNA localization of glutamate transporter isoforms GLT1a and GLT1b in rat brain by in situ hybridization. J Comp Neurol 492:78-89.
11. Bergles DE, Diamond JS, Jahr CE. 1999. Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol 9:293-298.
12. 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.
13. Brown DA, Docherty RJ, Halliwell JV. 1983. Chemical transmission in the rat interpeduncular nucleus in vitro. J Physiol (Lond) 341:655-670.
14. Canteras NS, Shammah-Lagnado SJ, Silva AB, Ricardo JA. 1990. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxydase study in the rat. Brain Res 513: 43-59.
15. Carlson J, Armstrong B, Switzer III RC, Ellison G. 2000. Selective neurotoxic effects of nicotine on axons in fasciculus retroflexus further support evidence that this is a weak link in brain across multiple drugs of abuse. Neuropharmacology 39:2792-2798.
16. Carr DB, Sesack SR. 2000. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20:3864-3873.
17. Charara A, Smith Y, Parent A. 1996. Glutamatergic inputs from the pedunculopontine nucleus to midbrain dopaminergic neurons in primates: Phaseolus vulgaris-leucoagglutinin anterograde labeling combined with postembedding glutamate and GABA immunohistochemistry. J Comp Neurol 364:254-266.
18. Chaudhry FA, Lehre KP, Campagne MV, 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.
19. Chen W, Aoki C, Mahadomrongkul V, Gruber CE, Wang GJ, Blitzblau R, Irwin N, Rosenberg PA. 2002. Expression of a variant form of the glutamate transporter GLT1 in neuronal cultures and in neurons and astrocytes in the rat brain. J Neurosci 22:2142-2152.
20. Chen W, Mahadomrongkul V, Berger UV, Bassan, M, DeSilva T, Tanaka K, Irwin N, Aoki C, Rosenberg PA. 2004. The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons. J Neurosci 24:1136-1148.
21. Chevalier G, Deniau JM. 1990. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci 13:277-280.
22. Contestabile A, Villani L, Fasolo A, Franzoni MF, Gribaudo L, Oktedalen O, Fonnum F. 1987. Topography of cholinergic and substance P pathways in the habenulo-interpeduncular system of the rat. An immunocytochemical and microchemical approach. Neuroscience 21:253-270.
23. Conti F, DeBiasi S, Minelli A, Rothstein JD, Melone M. 1998. EAAC1, a high-affinity glutamate transporter, is localized to astrocytes and GABAergic neurons besides pyramidal cells in the rat cerebral cortex. Cereb Cortex 8:108-116.
24. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
25. Danbolt NC, Pines G, Kanner BI. 1990. Purification and reconstitution of the sodium- and potassium-coupled glutamate transport glycoprotein from rat brain. Biochemistry 29:6734-6740.
26. Davis KE, Straff DJ, Weinstein EA, Bannerman PG, Correale DM, Rothstein JD, Robinson MB. 1998. Multiple signaling pathways regulate cell surface expression and activity of the excitatory amino acid carrier 1 subtype of Glu transporter in C6 glioma. J Neurosci 18:2475-2485.
27. 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.
28. Deniau JM, Hammon C, Riszk A, Feger J. 1978. Electrophysiological properties of identified output neurons of the rat substantia nigra (pars compacta and pars reticulata): evidence for the existence of branched neurons. Exp Brain Res 32:409-422.
29. 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.
30. 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.
31. Fallon JH, Loughlin SE. 1995. Substantia nigra. In: Paxinos G, editor. The rat nervous system. San Diego: Academic Press. p 215-237.
32. Furuta A, Rothstein JD, Martin LJ. 1997. Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17:8363-8375.
33. Georges F, Aston-Jones G. 2001. Potent regulation of midbrain dopamine neurons by the bed nucleus of the stria terminalis. J Neurosci 21: RC160.
34. Georges F, Aston-Jones G. 2002. Activation of ventral tegmental area cells by the bed nucleus of the stria terminalis: a novel excitatory amino acid input to midbrain dopamine neurons. J Neurosci 22:5173-5187.
35. Gerfen CR. 1992. The neostriatal mosaic: multiple levels of compartimental organization. Trends Neurosci 15:133-139.
36. Hammond C, Deniau JM, Rizk A, Feger J. 1978. Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res 151:235-244.
37. Harris KM, Stevens JK. 1989. Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9:2982-2997.
38. Haugeto O, Ullensvang K, Levy LM, Chaudhry FA, Honoré T, Nielsen M, Lehre KP, Danbolt NC. 1996. Brain glutamate transporter proteins form homomultimers. J Biol Chem 271:27715-27722.
39. Herkenham M, Nauta WJH. 1979. Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187:19-48.
40. Hiroi N. 1995. Compartmental organization of calretinin in the rat striatum. Neurosci Lett 197:223-226.
41. Hu W-H, Walters WM, Xia X-M, Karmally SA, Bethea JR. 2003. Neuronal glutamate transporter EAAT4 is expressed in astrocytes. Glia 44:13-25.
42. 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.
43. Huerta I, McCullumsmith RE, Haroutunian V, Giménez-Amaya JM, Meador-Woodruff JH. 2006. Expression of excitatory amino acid transporter interacting protein transcripts in the thalamus in schizophrenia. Synapse 59:394-402.
44. Inage YW, Itoh M, Wada K, Takashima S. 1998. Expression of two glutamate transporters, GLAST and EAAT4, in the human cerebellum: their correlation in development and neonatal hypoxic-ischemic damage. J Neuropathol Exp Neurol 57:554-562.
45. Itoh M, Watanabe Y, Watanabe M, Tanaka K, Wada K, Takashima S. 1997. Expression of a glutamate transporter subtype, EAAT4, in the developing human cerebellum. Brain Res 767:265-271.
46. Kalivas PW. 1993. Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Rev 18:75-113.
47. Kanai Y, Hediger MA. 1992. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360:467-471.
48. Kelland MD, Freeman AS, Rubin J, Chiodo LA. 1993. Ascending afferent regulation of rat midbrain dopamine neurons. Brain Res Bull 31:539-546.
49. Kinoshita A, Shigemoto R, Ohishi H, Van der Putten H, Mizuno N. 1998. Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study. J Comp Neurol 393:332-352.
50. Kita H, Kitai ST. 1987. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260:435-452.
51. Kita, H, Kitai ST. 1988. Glutamate decarboxylase immunoreactive neurons in rat neostriatum: their morphological types and populations. Brain Res 44, 7:346-352.
52. Kitai ST, Kita H. 1987. Apatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia. New York. Plenum Press.
53. Kugler P, Schmitt A. 1999. Glutamate transporter EAAG1 Is expiessed in neurons and glial cells in.the rat nervous system. Glia 27:129-142.
54. Lehre KP, Dahbolt 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.
55. 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 immunucytochemical observations. J Neurosci 15:1835-1853.
56. Liang,J, Takeuchi H, Doi Y, Kawanokuchi J, Sonobe Y, Jin S, Yawata I, Li H, Yasuoka S, Mizuno T, Suzumura A. 2008. Excitatory amino acid transporter expression by astrocytes is neuroprotective against microglial-excitotoxicity. Braiii Res 1210:11-19.
57. Lin CL, Tzingounis AV, Jin L, Furuta A, Kavanaugh MD, Rothstein JD. 1998. Molecular cloning and expression of the rat EAAT4 glutamate transporter subtype., Brain Res Mol Brain Res 63:174-179.
58. 3H]nicotine binding sites in the rat brain. Neurosci Lett 53:179-184.
59. Massie A, Cnops L, Jacobs S, Van Damme K., Vaudenbussche E, Eysel UT, Vandesande F, Arckens L. 2003. Glutamate levels and transport in cat ( Felis catus) area 17 during cortical reorganization following binocular retinal lesions. J Neurochem 84:1387-1397.
60. Massie A, Vandesande F, Arckens L. 2001. Expression of the high-affinity glutamate transporter EAAT4 in mammalian cerebral cortex. Neuro-report 12:393-397.
61. McCullumsmith RE, Meador-Woodruff JH. 2002. Striatal excitatory amino acid transporter transcript expression in schizophrenia, bipolar disorder and major depressive disorder. Neuropsychopharmacology 26: 368-375.
62. McGehee D, Heath M, Gelber S, Devay P, Role LW. 1995. Nicotine enhancement of fast excitatory synaptic transimission in CNS by presynaptic receptors. Science 269:1692-1697.
63. Mennerick, S, Dhond RP,, Benz A, Xu W, Rothstein JD, Daubolt NC, Isenberg KE, Zorumski CF. 1998. Neuronal expression of the glutamate transporter GLT-1 in hippocampal microcultures. J Neurosci 18:4490-4499.
64. Monaghan DT, Bridges RJ, Cotman CW. 1989. The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu Rev Pharmacol Toxicol 29:365-402.
65. Nagao S, Kwak S, Kanazawa I. 1997. EAAT4, a glutamate transporter with properties of a chloride channel, is predominantly localized in Purkinje cell dendrites, and forms parasagittal compartments in rat cerebellum. Neuroscience 78:929-933.
66. Nakanishi H, Kita H, Kitai ST. 1987. Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res 437:45-55.
67. Otis TS, Brasnjo G, Dzubay JA, Pratap M. 2004. Interactions between glutamate transporters and metabotropic glutamate receptors at excitatory synapses in the cerebellar cortex. Neurochem. Int 45:537-544.
68. Ottersen OP, Storm-Mathisen J. 1984. Neurons containing or accumulating transmitter amino acids. In: Björklund A, Hökfelt T, Kuhar MJ, editors. Handbook of chemical neuroanatomy. Vol. 3. Classical transmitters and transmitter receptors in the CNS, Part II. New York: Elsevier Science Publishers. p 141-216.
69. Parent A. 1986. Comparative neurobiology of the basal ganglia. New York: John Wiley & Sons.
70. 3H]Epibatidine labels nicotinic receptors in rat brain: an autoradiographic study. J Pharmacol Exp Ther 275:1030-1034.
71. Petralia RS, Wenthold RJ. 1992. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 318:329-354.
72. Pignataro L, Sitaramayya A, Finnemann SC, Sarthy VP. 2005. Nonsynaptic localization of the excitatory amin acid transporter 4 in photoreceptors. Mol Cell Neurosci 28:440-51.
73. 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.
74. Qu Y, Moons L, Vandesande F. 1997. Determination of serotonin, catecholamines and their metabolites by direct injection of supernatants from chicken brain tissue homogenate using liquid chromatography with electrochemical detection. J Chromatogr B 704:351-358.
75. Raiteri L, Raiteri M, Bonanno G. 2002. Coexistence and function of different neurotransmitter transporters in the plasma membrane of CNS neurons. Prog Neurobiol 68:287-309.
76. Rakhade SN, Loeb JA. 2008. Focal reduction of neuronal glutamate transporters in human neocortical epilepay. Epilepsia 49:226-236.
77. Rauen T, Kanner BI. 1994. Localization of the glutamate transporter GLT-1 in tat and macaque monkey retinae. Neurosci Lett 169:137-140.
78. Ribak CE, Vaughn JE, Roberts E. 1979. The GABA neurons and their axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry. J Comp Neurol 187, 261-284.
79. Richardson RD, Jarret L, Finke EH. 1960. Embedding in epoxy resins for ultrathin selectioning in electron microscopy. Stain Technol 35:313-323.
80. 2+ permeability and kinetics of glutamate receptors in rat medial habenula neurones: implications for purinergic transmission in this nucleus. J Physiol 518: 539-549
81. 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.
82. 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 transports reveals a major role for astroglial transport in excitotoxicty and clearance of glutamate. Neuron 16:675-686.
83. Saier MH. 1999. Eukaryotic transmembrane solute transport systems. Int Rev. Cytol 190:61-136.
84. Sarre S, Yuan H, Jonkers N, Van Hemelrijck, A. Ebiger G, Michotte Y. 2004. In vivo characterization of somatodendritic dopamine release in the substantia nigra of 6-hydroxydopamine-lesioned rats. J Neurochem 90:29-39.
85. Schmitt A, Asan E, Püschel B, Jöns T, Kugler P. 1996. Expression of the glutamate transporter GLT-1 in neural cells of the rat central nervous system: nonradioactive in situ hybridization and comparative immunocytochemistry. Neuroscience 71:989-1004.
86. Seal RP, Amara SG.1999. Excitatory amino acid transporters: a family in flux. Annu Rev Pharmacol Toxicol 39:431-456.
87. Sesack SR, Pickel VM. 1992. Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320:145-160.
88. Shu S, Ju G, Fan L. 1988. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 84: 169-171.
89. Slotboom DJ, Konings WN, Lolkema JS. 1999. Structural features of the glutamate transporter family. Microbiol Mol Biol Rev 63;293-307.
90. Sonders MS, Amara SG. 1996. Channels in transporters. Curr Opin Neurobiol 6:294-302.
91. Soriano E, Frotscher M. 1994. Mossy cells of the rat fascia dentate are glutamate-immunoreactive. Hippocampus 4:65-69.
92. Sorra KE, Harris KM. 1993. Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J Neurosci 13:3736-3748.
93. +-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci U S A 89:10955-10959.
94. Takayasu Y, Iiono 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.
95. Tanaka K. 1993. Expression cloning of a rat glutamate transporter. Neurosci Res 16:149-153.
96. Tanaka J, Ichikawa R, Watanabe M, Tanaka K, Inoue Y. 1997. Extrajunctional localization of glutamate transporter EAAT4 at excitatory Purkinje cell synapses. Neuroreport 8, 2461-2464.
97. Thierry AM, Chevalier G, Ferron A, Glowinski J. 1983. Diencephalic and mesencephalic efferents of the medial prefrontal cortex in the rat: electrophysiological evidence for the existence of branched axons. Exp Brain Res 50:275-282.
98. Torp R, Danbolt NC, Babaie E, Bjoras M, Seeberg E, Storm-Mathisen J, Ottersen OP. 1994. Differential expression of two glial glutamate transporters in the rat brain: an in situ hybridization study. Eur J Neurosci 6:936-942.
99. Torp R, Danbolt NC, Storm-Mathisen J, Ottersen OP. 1996. Differential cellular and regional distribution of the glutamate transporters GLT-1 and rEAAC1: an in situ hybridization analysis in the rat brain. Soc Neurosci Abstr 22:356.
100. Torres-Salazar D, Fahlke C. 2007. Neuronal glutamate transporters vary in substrate transport rate but not in unitary anion channel conductance. J Biol Chem 282:34719-34726.
101. Vandenberg RJ, Arriza JL, Amara SG, Kavanaugh MP. 1995. Constitutive ion fluxes and substrate binding domains of human glutamate transporters. J Biol Chem 270:17668-17671.
102. Wadiche JI, Amara SG, Kavanaugh MP. 1995a. Ion fluxes associated with excitatory amino acid transport. Neuron 15:721-728.
103. Wadiche JI, Arriza JL, Amara SG, Kavanaugh MP. 1995b. Kinetics of a human glutamate transporter. Neuron 14:1019-1027.
104. Wang GJ, Chung HJ, Schnuer J, Pratt K, Zable AC, Kavanaugh MP, Rosenberg PA. 1998. High affinity glutamate transport in rat cortical neurons in culture. Mol Pharmacol 53:88-96.
105. Ward MM, Jobling AI, Puthussery T, Foster LE, Fletcher EL. 2004. Localization and expression of the glutamate transporter, excitatory amino acid transporter 4, within astrocytes of the rat retina. Cell Tissue Res 315:305-310.
106. Wenzel HJ, Buckmaster PS, Anderson NL, Wenzel ME, Schwartzkroin PA. 1997. Ultrastructural localization of neurotransmitter immunoreactivity in mossy cell axons and their synaptic targets in the rat dentate gyrus. Hippocampus 7:559-570.
107. Woolf N, Butcher L. 1989. Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum. Brain Res Bull 23:519-540.
108. Wüllner U, Testa CM, Catania MV, Young AB, Penney JB. 1994. Glutamate receptors in striatum and substantia nigra: effects of medial forebrain bundle lesions. Brain Res 645:98-102.
109. 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.
110. Yamashita A, Makita K, Kuroiwa T, Tanaka K. 2006. Glutamate transporters GLAST and EAAT4 regulate postischemic Purkinje cell death: an in vivo study using a cardiac arrest model in mice lacking GLAST or EAAT4. Neurosci Res 55:264-270.
111. Yelnik J. 2002. Functional anatomy of the basal ganglia. Move Disord 17:S15-S21.
112. Yi JH, Herrero R, Chen G, Hazell AS. 2007. Glutamate transporter EAAT4 is increased in hippocampal astrocytes following lateral fluid-percussion injury in the rat. Brain Res 1154:200-205.