Glutamate transport by retinal Müller cells in glutamate/aspartate transporter-knockout mice

GLIA

Volumn 49, Issue 2, 2005, Pages 184-196

  Sarthy, Vijay P ^a   Pignataro, Leonardo ^a   Pannicke, Thomas ^b   Weick, Michael ^b   Reichenbach, Andreas ^b   Harada, Takayuki ^c   Tanaka, Kohichi ^c   Marc, Robert ^d  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Autoradiography, EAAT; Cystine glutamate exchanger; D aspartate; Glia; Immunocytochemistry

Indexed keywords

ANTIPORTER; ASPARTIC ACID; CARRIER PROTEIN; CYSTEINE GLUTAMATE EXCHANGER PROTEIN; EXCITATORY AMINO ACID TRANSPORTER; GLUTAMATE ASPARTATE TRANSPORTER; GLUTAMATE TRANSPORTER; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; CONTROLLED STUDY; EXCITOTOXICITY; HOMEOSTASIS; IMMUNOCYTOCHEMISTRY; MOUSE; MUELLER CELL; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RETINA; RETINA CELL; SIGNAL NOISE RATIO;

AMINO ACID TRANSPORT SYSTEM ASC; AMINO ACID TRANSPORT SYSTEM X-AG; AMINO ACID TRANSPORT SYSTEMS; ANIMALS; ASPARTIC ACID; BIOLOGICAL TRANSPORT; CELLS, CULTURED; EXCITATORY AMINO ACID TRANSPORTER 1; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; GLUTAMIC ACID; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NEUROGLIA; PATCH-CLAMP TECHNIQUES; RETINA; SODIUM; SODIUM CHANNELS; SYMPORTERS; UP-REGULATION;

EID: 13244253756     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/glia.20097     Document Type: Article

References (71)

1. Allan AM, Harris RA. 1987. Acute and chronic ethanol treatments alter GABA receptor-operated chloride channels. Pharmacol Biochem Behav 27:665-670.
2. Arriza JL, Kavanaugh MP, Fairman WA, Wu YN, Murdoch GH, North RA, Amara SG. 1993. Cloning and expression of a human neutral amino acid transporter with structural similarity to the glutamate transporter gene family. J Biol Chem 268:15329-15332.
3. 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.
4. Attwell D, Barbour B, Szatkowski M. 1993. Nonvesicular release of neurotransmitter. Neuron 11:401-407.
5. Bannai S, Tateishi N. 1986. Role of membrane transport in metabolism and function of glutathione in mammals. J Membr Biol 89:1-8.
6. Barnett NL, Pow DV. 2000. Antisense knockout of GLAST, a glial glutamate transporter, compromises retinal function. Invest Ophthalmol Vis Sci 38:82834-2834.
7. Bergles DE, Diamond JS, Jahr CE. 1999. Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol 9:293-298.
8. Biedermann B, Bringmann A, Reichenbach, A. 2002. High-affinity GABA uptake in retinal glial (Müller) cells of the guinea pig: electrophysiological characterization, immunocytochemical localization, and modeling efficiency. Glia 39:217-228.
9. Billups B, Rossi D, Attwell D. 1996. Anion conductance behavior of the glutamate uptake carrier in salamander retinal glial cells. J Neurosci 16:6722-6731.
10. Bonanno G, Pittaluga A, Fedele E, Fontana G, Raiteri M. 1993. Glutamic acid and gamma-aminobutyric acid modulate each other's release through heterocarriers sited on the axon terminals of rat brain. J Neurochem 61:222-462.
11. Bonanno G, Vallebuona F, Donadini F, Fontana G, Fedele E, Raiteri M. 1994. Heterocarrier-mediated reciprocal modulation of glutamate and glycine release in rat cerebral cortex and spinal cord synaptosomes. Eur J Pharmacol 252:61-67.
12. Bringmann A, Biedermann B, Reichenbach A. 1999. Expression of potassium channels during postnatal differentiation of rabbit Müller glial cells. Eur J Neurosci 11:2883-2896.
13. Christensen HN. 1990. Role of amino acid transport and counter-transport in nutrition and metabolism. Physiol Rev 70:43-77.
14. Crook DK, Pow DV. 1997. Analysis of the distribution of glycine and GABA in amacrine cells of the developing rabbit retina: a comparison with the ontogeny of a functional GABA transport system in retinal neurons. Vis Neurosci 14:751-763.
15. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
16. Eliasof S, Jahr CE. 1996. Retinal glial cell glutamate transporter is coupled to an anionic conductance. Proc Natl Acad Sci USA 93:4153-4158.
17. Eliasof S, Arriza, JL, Leighton, BH, Kavanaugh MP, Amara SG. 1998a. Excitatory amino acid transporters of the salamander retina: identification, localization and function. J Neurosci 18:698-712.
18. Eliasof S, Arizza JL, Leighton BH, Amara SG, Kavanaugh MP. 1998b. Localization and function of five glutamate transporters cloned from the salamander retina. Vis Res 38:1443-1454.
19. 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.
20. Harada T., Harada C, Watanabe M, Inoue Y, Sakagawa T, Nakayama N, Sasaki S, Okuyama S, Watase K, Wada K, Tanaka K. 1998. Functions of two glutamate transporters GLAST and GLT-1 in the retina. Proc Natl Acad Sci USA 95:4663-4666.
21. Izumi Y, Shimamoto K, Benz AM, Hammerman SB, Olney JW, Zorumski CF. 2002. Glutamate transporters and retinal excitotoxicity. Glia 39:58-688.
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. Jones BW, Watt CB, Frederick JM, Baehr W, Chen CK, Levine EM, Milam AH, Lavail MM, Marc RE. 2003. Retinal remodeling triggered by photoreceptor degenerations. J Comp Neurol 464:1-16.
24. Kalloniatis M, Marc RE, Murray RF. 1996. Amino acid signatures in the primate retina. J Neurosci 16:6807-6829.
25. Kato S, Ishita S, Sugawara K, Mawatari K. 1993. Cytine/glutamate antiporter expression in retinal Müller glial cells: implications for DL-alpha-amino adipate toxicity. Neuroscience 57:473-482.
26. Kuzmanovic M, Dudley VJ, Sarthy VP. 2003. GFAP promoter drives Müller cell-specific expression in transgenic mice. Invest Ophthalmol Vis Sci 44:3606-3613.
27. Lehre KP, Davanger S, Danbolt NC. 1997. Localization of the glutamate transporter protein GLAST in rat retina. Brain Res 744:129-137.
28. Levi G, Poce U, Raiteri, M. 1976. Uptake and exchange of GABA and glutamate in isolated nerve endings. Adv Exp Med Biol 69:273-289.
29. +-dependent glutamate transport. J Neurosci 19:1-9.
30. Marc RE. 1999. Mapping glutamatergic drive in the vertebrate retina with a channel permeant organic cation. J Comp Neurol 407:47-64.
31. Marc RE, Cameron DA. 2002. A molecular phenotype atlas of the zebrafish retina. J Neurocytol 30:593-654.
32. Marc RE, Jones BW. 2002. Molecular phenotyping of retinal ganglion cells. J Neurosci 22:413-427.
33. 3)glycine-accumulating neurons of the human retina. J Comp Neurol 232:241-260.
34. Marc RE, Stell WK, Bok D, Lam DMK. 1978. GABA-ergic pathways in goldfish retina. J Comp Neurol 182:221-245.
35. Marc RE, Murray RF, Basinger SF. 1995. Pattern-recognition of amino acid signatures in retinal neurons. J Neurosci 15:5106-5129.
36. +-independent acidic amino acid transporter with structural similarity to the member of heterodimeric amino acid transporter family associated with unknown heavy chains. J Biol Chem 277:21017-21026.
37. Mitani A, Tanaka K. 2003. Functional changes of glial glutamate transporter GLT-1 during ischemia: an in vivo study in the hippocampal CA1 of normal mice and mutant mice lacking GLT-1. J Neurosci 23:7176-7182.
38. Müller JF, Marc RE. 1990. GABA-ergic and glycinergic pathways in the inner plexiform layer of the goldfish retina. J Comp Neurol 291:281-283.
39. Ottersen OP, Zhang N, Walberg F. 1992. Metabolic compartmentation of glutamate and glutamine-morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience 46:519-534.
40. Palacin M, Estevez R, Bertran J, Zorzano A. 1998. Molecular biology of mammalian plasma membrane amino acid transporters. Physiol Rev 78:969-1054.
41. Pannicke T, Bringmann A, Reichenbach, A. 2002. Electrophysiological characterization of retinal Müller glial cells from mouse during postnatal development: comparison with rabbit cells. Glia 38:268-272.
42. 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.
43. Penn JS, Thum LA, Rhem MN, Dell SJ. 1988. Effects of oxygen rearing on the electroretinogram and GFA-protein in the rat. Invest Ophthalmol Vis Sci 29:1623-1630.
44. Pow DV. 2001a. Amino acids and their transporters in the retina. Neurochem Int 38:463-484.
45. Pow DV. 2001b. Visualising the activity of the cystine-glutamate antiporter in glial cells using antibodies to aminoadipic acid, a selectively transported substrate. Glia 34:27-38.
46. Pow DV, Barnett NL. 1999. Changing patterns of spatial buffering of glutamate in developing rat retinae are mediated by the Müller cell glutamate transporter GLAST. Cell Tissue Res 297:57-66.
47. Pow DV, Barnett NL. 2000. Developmental expression of excitatory amino acid transporter 5:a photoreceptor and bipolar cell glutamate transporter in rat retina. Neurosci Lett 280:21-24.
48. Rao VLR, Dogan A, Todd KG, Bowen KK, Kim B-T, Rothstein JD, Dempsey RJ. 2002. Antisense knockdown of the glial glutamate transporter GLT-1, but not the neuronal glutamate transporter EAAC1, exacerbates transient focal cerebral ischemia-induced neuronal damage in rat brain. J Neurosci 21:1876-1883.
49. Rauen T, Kanner BI. 1994. Localization of the glutamate transporter GLT-1 in rat and macaque monkey retinae. Neurosci Lett 169:137-140.
50. Rauen T, Rothstein JD, Wassle H. 1996. Differential expression of three glutamate transporter subtypes in the rat retina. Cell Tissue Res 286:325-336.
51. Rauen T, Taylor WR, Kuhlbrodt K, Wiessner M. 1998. High-affinity glutamate transporters in the rat retina: a major role of the glial glutamate transporter GLAST-1 in transmitter clearance. Cell Tissue Res 291:19-31.
52. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kania 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.
53. 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.
54. Sakai K, Shimizu H, Koike T, Furuya S, Watanabe M. 2003. Neutral amino acid transporter ASCT1 is preferentially expressed in L-Ser-synthetic/storing glial cells in the mouse brain with transient expression in developing capillaries. J Neurosci. 23:550-560.
55. Sarthy VP, Ripps H. 2001. The retinal Müller cell. Structure and function. New York: Kluwer.
56. Sarthy VP, Hendrickson AE, Wu J-Y. 1986. L-Glutamate: a neurotransmitter candidate for cone photoreceptors in the monkey retina. J Neurosci 6:637-643.
57. Schultz K, Stell WK. 1996. Immunocytochemical localization of the high affinity glutamate transporter, EAAC1, in the retina of representative vertebrate species. Neurosci Lett 211:191-194.
58. Seal RP, Amara SG. 1999. Excitatory amino acid transporters: a family in flux. Annu Rev Pharmacol Toxicol 39:431-456.
59. +/glutamate cotransporters. J Biol Chem 268:15351-15355.
60. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K. 1997. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276:1699-1702.
61. Tetsuka K, Takanaga H, Ohtsuki S, Hosoya K-I, Terasaki, Y. 2003. The L-isomer-selective transport of aspartic acid is mediated by ASCT2 at the blood-brain barrier. J Neurochem 87:891-901.
62. Tomi M, Hosoya K, Takanaga H, Ohtsuki S, Terasaki T. 2002. Induction of xCT gene expression and L-cysteine transport activity by diethyl maleate at the inner blood-retinal barrier. Invest Ophthalmol Vis Sci 43:774-779.
63. -, in the newly developed rat retinal Müller cell line (TR-MUL). GLIA 43:208-217.
64. + dependent neutral amino acid transporter. J Biol Chem 271:14883-14890.
65. Voutsinos-Porsche B, Bonvento G, Tanaka K, Steiner P, Welker E, Chatton J.-Y, Magistretti PJ, Pellerin L. 2003. Glial glutamate transporters mediate a functional metabolic cross talk between neurons and astrocytes in the mouse developing cortex. Neuron 39:275-286.
66. Ward MM, Jobling AI, Puthuserry 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.
67. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M. 1998. Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 10:976-988.
68. White RD, Neal MJ. 1976. The uptake of L-glutamate by the retina. Brain Res 111:79-93.
69. Wood JD, Sidhu HS. 1986. Uptake of gamma-aminobutyric acid by brain tissue preparations: a reevaluation. J Neurochem 46:739-744.
70. Ye ZC, Rothstein JD, Sontheimer H. 1999. Compromised glutamate transport in human glioma cells: reduction-mislocalization of sodium-dependent glutamate transporters and enhanced activity of cystine-glutamate exchange. J Neurosci 19:10767-10777.
71. Zerangue N, Kavanaugh MP. 1996. ASCT-1 is a neutral amino acid exchanger with chloride channel activity. J Biol Chem 27:27991-27994.