Advertisement

Excitatory Amino Acid Transporters in the Retina

  • Vijay Sarthy
  • David Pow
Part of the Ophthalmology Research book series (OPHRES)

Introduction

Plasma membrane neurotransmitter transporters contribute to the clearance and recycling of neurotransmitters, and can have a profound impact on the extent of receptor activation during neuronal signaling. Studies of neurotransmitter transporters have been crucial in the development of treatments for major neuropsychiatric conditions. The dopamine, norepinephrine and serotonin transporters (DAT, NET and SERT, respectively) are well-established targets for addictive drugs including cocaine and amphetamines, and for therapeutic antidepressants (1). Recently, glutamate transporters have been suggested as potential targets for stroke therapy (2). Therefore, a sound knowledge of the roles of glutamate transporters in the retina is of great relevance in developing treatments for human ocular diseases such as diabetic retinopathy. An understanding of the mechanisms that regulate these transporters has the potential to impact on both the physiology and pathology of glutamate in...

Keywords

Outer Segment Bipolar Cell Glutamate Transporter Amacrine Cell Glutamate Uptake 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We wish to thank V. Joseph Dudley for help with manuscript preparation. We apologize to authors whose work could not be included because of limitations on the length of the article. Supported by NIH and NHMC (Australia).

References

  1. 1.
    1. Amara SG and Kuhar MJ. Neurotransmitter transporters: recent progress. Ann Rev Neurosci 1993;16:73–93.PubMedCrossRefGoogle Scholar
  2. 2.
    2. Lee J-M, Zipfel GJ, Choi DW. The changing landscape of ischaemic brain injury mechanisms. Nature 1999;399:A7–A14.PubMedGoogle Scholar
  3. 3.
    3. Massey SC. Cell types using glutamate as a neurotransmitter in the vertebrate retina. Prog Ret Res 1990;9:399–425.CrossRefGoogle Scholar
  4. 4.
    4. Lucas DR and Newhouse JP. The toxic effect of sodium L-glutamate on the inner layers of the retina. Arch Ophthalmol 1957;58:193–201.Google Scholar
  5. 5.
    5. Romano C, Chen Q, Olney JW. The intact isolated (ex vivo) retina as a model system for the study of excitotoxicity. Prog Retin Eye Res 1998;17:465–483.PubMedCrossRefGoogle Scholar
  6. 6.
    6. Ambati J, Chalam KV, Chawla DK, D'Angio CT, Guillet EG, Rose SJ, Vanderlinde RE, Ambati BK. Elevated gamma-aminobutyric acid, glutamate and vascular growth factor levels in the vitreous of patients with proliferative diabetic retinopathy. Arch Ophthalmol 1997;115:1161–1166.PubMedGoogle Scholar
  7. 7.
    7. Seal RP and Amara SG. Excitatory amino acid transporters: a family in flux. Ann Rev Pharmacol Toxicol 1999;39:431–456.CrossRefGoogle Scholar
  8. 8.
    8. Pow DV. Amino acids and their transporters in the retina. Neurochem Int 2001;38:463–484.PubMedCrossRefGoogle Scholar
  9. 9.
    9. Rauen T and Kanner BI. Localization of the glutamate transporter GLT-1 in rat and macaque monkey retinae. Neurosci Lett 1994;169:137–140.PubMedCrossRefGoogle Scholar
  10. 10.
    10. Rauen T, Rothstein JD, Wassle H. Differential expression of three glutamate transporter subtypes in the rat retina. Cell Tissue Res 1996;286:325–336.PubMedCrossRefGoogle Scholar
  11. 11.
    11. Lehre KP, Davanger S, Danbolt NC. Localization of the glutamate transporter protein GLAST in rat retina. Brain Res 1997;744:129–137.PubMedCrossRefGoogle Scholar
  12. 12.
    12. Derouiche A and Rauen T. Coincidence of L-glutamate/aspartate transporter (GLAST) and glutamine synthetase (GS) immunoreactions in retinal glia: evidence for coupling of GLAST and GS in transmitter clearance. J Neurosci Res 1995;42:131–143.PubMedCrossRefGoogle Scholar
  13. 13.
    13. Harada T, Harada C, Watanabe M, Inoue Y, Sakagawa T, Nakayama N, Sasaki S, Okuyama S, Watase K, Wada K, Tanaka K. Functions of two glutamate transporters GLAST and GLT-1 in the retina. Proc Natl Acad Sci USA 1998;95:4663–4666.PubMedCrossRefGoogle Scholar
  14. 14.
    14. Barnett NL and Pow DV. Antisense knockdown of GLAST, a glial glutamate transporter, compromises retinal function. Invest Ophthalmol Vis Sci 2000;41:585–591.PubMedGoogle Scholar
  15. 15.
    15. Kang TC, Park SK, Jo SM, et al. Comparative studies on the distribution of glutamate transporters in the retinae of the Mongolian gerbil and the rat. Anat Histol Embryol 2000;29:381–383.PubMedCrossRefGoogle Scholar
  16. 16.
    16. Vandenbranden CA, Yazulla S, Studholme KM, et al. Immunocytochemical localization of the glutamate transporter GLT-1 in goldfish (carassius auratus) retina. J Comp Neurol 2000;423:440–451.PubMedCrossRefGoogle Scholar
  17. 17.
    17. Reye O, Sullivan R, Pow DV. Distribution of two splice variants of the glutamate transporter GLT-1 in the developing rat retina. J Comp Neurol 2002;447:323–330.PubMedCrossRefGoogle Scholar
  18. 18.
    18. Rauen T, Wiessner M, Sullivan R, Lee A, Pow DV. A new GLT1 splice variant; Cloning and immunolocalization of GLT1c in the mammalian retina and brain. Neurochem Int 2004;45:1095–1106.PubMedCrossRefGoogle Scholar
  19. 19.
    19. Schultz K and Stell WK. Immunocytochemical localization of the high affinity glutamate transporter, EAAC1, in the retina of representative vertebrate species. Neurosci Lett 1996;211:191–194.PubMedCrossRefGoogle Scholar
  20. 20.
    20. Fyk-Kolodziej B, Qin P, Dzhagaryan A, Pourcho RG. Differential cellular and subcellular distribution of glutamate transporters in the cat retina. Vis Neurosci 2004;21:551–565.PubMedCrossRefGoogle Scholar
  21. 21.
    21. Ward MM, Jobling AI, Puthuserry T, Foster LE, Fletcher EL. Localization and expression of the glutamate transporter, excitatory amino acid transporter 4, within astrocytes of the rat retina. Cell Tissue Res 2004;315:305–310.PubMedCrossRefGoogle Scholar
  22. 22.
    22. Pignataro L, Sitaramayya A, Finnemann SC, Sarthy VP. Non-synaptic localization of EAAT4 in the outer segments of photoreceptors. MolCell Neurosci 2005;28:440–451.CrossRefGoogle Scholar
  23. 23.
    23. Arriza JL, Eliasof S, Kavanaugh MP, Amara SG. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci USA 1997;94:4155–4160.PubMedCrossRefGoogle Scholar
  24. 24.
    24. Eliasof S, Arriza JL, Leighton BH, Kavanaugh MP, Amara SG. Excitatory amino acid transporters of the salamander retina: identification, localization and function. J Neurosci 1998;18:698–712.PubMedGoogle Scholar
  25. 25.
    25. Pow DV and Barnett NL. Changing patterns of spatial buffering of glutamate in developing rat retinae are mediated by the Müller cell glutamate transporter GLAST. Cell Tissue Res 1999;297:57–66.PubMedCrossRefGoogle Scholar
  26. 26.
    26. Georges P, Cornish EE, Provis JM, Madigan MC. Müller cell expression of glutamate cycle related proteins and anti-apoptotic proteins in early human retinal development. Br J Ophthalmol 2006;90;223–228.PubMedCrossRefGoogle Scholar
  27. 27.
    27. Danbolt NC. Glutamate uptake. Prog Neurobiol 2001;65:1–105.PubMedCrossRefGoogle Scholar
  28. 28.
    28. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L et al. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996;16:675–686.PubMedCrossRefGoogle Scholar
  29. 29.
    29. Jabaudon D, Shimamoto K, Yasuda-Kamatani Y, Scanziani M, Gahwiler BH, Gerber U. Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc Natl Acad Sci USA 1999;96:8733–8738.PubMedCrossRefGoogle Scholar
  30. 30.
    30. Szatkowski M and Attwell D. Triggering and execution of neuronal death in brain ischaemia: two phases of glutamate release by different mechanisms. Trends Neurosci 1994;17:359–365.PubMedCrossRefGoogle Scholar
  31. 31.
    31. Li S, Mealing GAR, Morley P, Stys PK. Novel injury mechanism in anoxia and trauma of spinal cord white matter: Glutamate release via reverse Na+-dependent glutamate transport. J Neurosci 1999;19(16):1–9.Google Scholar
  32. 32.
    32. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, et al. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 1997;276: 1699–1702.PubMedCrossRefGoogle Scholar
  33. 33.
    33. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M. Motor discordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 1998;10:976–988.PubMedCrossRefGoogle Scholar
  34. 34.
    34. Peghini P, Janzen J, Stoffel W. Glutamate transporter EAAC1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. EMBO J 1997;16:3822–3832.PubMedCrossRefGoogle Scholar
  35. 35.
    35. Sarthy VP, Pignataro L, Pannicke T, Weick M, Reichenbach A, Harada T, Tanaka K and Marc R. Glutamate transport by retinal Müller cells in glutamate/aspartate transporter knockout mice. Glia 2004;49:184–196.CrossRefGoogle Scholar
  36. 36.
    36. Hasegawa J, Obara T, Tanaka K, Tachibana M. High-density presynaptic transporters are required for glutamate removal from the first visual synapse. Neuron 2006;50:63–74.PubMedCrossRefGoogle Scholar
  37. 37.
    37. Bergles DE, Diamond JS, Jahr CE. Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol 1999;9:293–298.PubMedCrossRefGoogle Scholar
  38. 38.
    38. Diamond JS and Jahr CE. Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci 1997;17:4672–4687.PubMedGoogle Scholar
  39. 39.
    39. Lehre KP and Danblot NC. The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young and adult rat brain. J Neurosci 1998;18:8751–8757.PubMedGoogle Scholar
  40. 40.
    40. Rabl K, Bryson EJ, Thoreson WB. Activation of glutamate transporters in rods inhibits presynaptic calcium currents. Vis Neurosci 2003;20:557–566.PubMedCrossRefGoogle Scholar
  41. 41.
    41. Grewer C and Rauen T. Electrogenic glutamate transporters in the CNS: Molecular mechanisms, pre-steady-state kinetics, and their impact on synaptic signaling. J Membrane Biol 2005;203:1–20.CrossRefGoogle Scholar
  42. 42.
    42. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M et al. Localization of neuronal and glial glutamate transporters. Neuron 1994;13:713–725.PubMedCrossRefGoogle Scholar
  43. 43.
    43. Conti F, DeBiasi S, Minelli A, Rothstein JD, Melone M. EAAC1, a high-affinity glutamate transporter, is localized to astrocytes and gabaergic neurons besides pyramidal cells in the rat cerebral cortex. Cereb Cortex 1998;8:108–116.PubMedCrossRefGoogle Scholar
  44. 44.
    44. He Y, Janssen WG, Rothstein JD, Morrison JH. Differential synaptic localization of the glutamate transporter EAAC1 and glutamate receptor subunit GluR2 in the rat hippocampus. J Comp Neurol 2000;418:255–269.PubMedCrossRefGoogle Scholar
  45. 45.
    45. Seputsky JP, Cohen AS, Eccles C, Rafiq A, et al. A neuronal glutamate transporter contributes to neurotransmittter GABA synthesis and epilepsy. J Neurosci 2002;22:6372–6379.Google Scholar
  46. 46.
    46. Matthews GC and Diamond JS. Neuronal glutamate uptake contributes to GABA synthesis and inhibitory synaptic strength. J Neurosci 2003;23:2040–2048.Google Scholar
  47. 47.
    47. Sarthy VP, Marc RE, Pignataro L, Tanaka K. Contribution of a glial glutamate transporter to GABA synthesis in the retina. Neuroreport 2004;15:1895–898.PubMedCrossRefGoogle Scholar
  48. 48.
    48. Casado M, Bendahan A, Zafra F, Danbolt NC. Phosphorylation and modulation of brain glutamate transporter by protein kinase C J Biol Chem 1993;268:27313–27317.Google Scholar
  49. 49.
    49. Dowd LA and Robinson MB. Rapid stimulation of EAAC1 mediated Na+-dependent L-glutamate transport activity in C6 glioma cells by phorbol ester. J Neurochem 1996;18:3603–3619.Google Scholar
  50. 50.
    50. Davis KE, Straff DJ, Weinstein EA, Bannerman PG, et al. Multiple signaling pathways regulate cell surface expression and activity of the excitatory amino acid carrier 1 subtype of glutamate transporter in C6 glioma. J Neurosci 1998;18;3603–3619.Google Scholar
  51. 51.
    51. Vandenberg RJ, Mitrovic AD, Johston GAR. Molecular basis for differential inhibition of glutamate transporter sub-types by zinc ions. Mol Pharmacol 1998;54:189–196.PubMedGoogle Scholar
  52. 52.
    52. Zerangue N, Arriza JL, Amara SG, Kavanaugh MP. Differential modulation of human transporter subtypes by arachidonic acid. J Biol Chem 1995;270:6433–6435.PubMedCrossRefGoogle Scholar
  53. 53.
    53. Fairman WA, Sonders MS, Murdoch GH, Amara SG. Arachidonic acid elicits a substrate-gated proton current associated with the glutamate transpoorter EAAT4. Nature Neurosci 1998;1:105–113.PubMedCrossRefGoogle Scholar
  54. 54.
    54. Eskandari S, Kreman M, Kavanaugh MP, Wright EM, Zamphigi GA. Pentameric assembly of a neuronal glutamate transporter. Proc Natl Acad Sci 2000;97:8641–8646.PubMedCrossRefGoogle Scholar
  55. 55.
    55. Trotti D, Danbolt NC, Volterra A. Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol Sci 1998;19: 328–334.PubMedCrossRefGoogle Scholar
  56. 56.
    56. Jackson M, Song W, Liu M, Jin L, Dyles-Hoberg M, et al. Modulation of the neuronal glutamate transporter EAAT4 by two interacting proteins. Nature 2001;410:89–93.PubMedCrossRefGoogle Scholar
  57. 57.
    57. Lin CG, Orlov I, Ruggiero AM, Dykes-Hoberg M, et al. Modulation of the neuronal glutamate transporter EAAC1 by the interacting protein GTRAPS-18. Nature 2001;410:84–88.PubMedCrossRefGoogle Scholar
  58. 58.
    58. Butchbach MER, Lai L, Lin C-I G. Molecular cloning, gene structure, expression profile and functional characterization of the mouse glutamate transporter (EAAT3) interacting protein GTRAP3-18. Gene 2002;292:81–90.PubMedCrossRefGoogle Scholar
  59. 59.
    59. Marie H and Attwell D. C-terminal interactions modulate the affinity of GLAST glutamate transporters in salamander retinal glial cells. J Physiol 1999;520:393–397.PubMedCrossRefGoogle Scholar
  60. 60.
    60. Moron JA, Zakharova I, Ferrer JV, Merrill GA, et al. Mitogen-activated protein kinase regulates dopamine transporter surface expression and dopamine transport capacity. J Neurosci 2003;23:8480–8488.PubMedGoogle Scholar
  61. 61.
    61. Gonzalez MI, Loez-Clome AM, Ortega A. Sodium-dependent glutamate transport in Müller cells: Regulation by phorbol esters. Brain Res 1999;831:140–145.PubMedCrossRefGoogle Scholar
  62. 62.
    62. Ganel R and Crosson CE. Modulation of human glutamate transporter activity by phorbol ester. J Neurochem 1998;70:993–1000.PubMedCrossRefGoogle Scholar
  63. 63.
    63. Bull ND and Barnett NL. Antagonists of protein kinase C inhibit rat retinal glutamate transporter activity in situ. J Neurochem 2002;81:472–480.PubMedCrossRefGoogle Scholar
  64. 64.
    64. Schniepp R, Kohler K, Ladewig T, et al. Retinal localization and in vitro interaction of the glutamate transporter EAAT3 and the serum- and glucocorticoid-inducible kinase SGK1. Invest Ophthalmol Vis Sci 2004;45:1442–1449.PubMedCrossRefGoogle Scholar
  65. 65.
    65. Cheng C, Grover G, Banker G, Amara SG. A novel sorting motif in the glutamate transporter excitatory amino acid transporter 3 directs its targeting in Madin–Darby canine kidney cells and hippocampal neurons. J Neurosci 2002;22:10643–10652.PubMedGoogle Scholar
  66. 66.
    66. Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog Ret Eye Res 2000;19:385–419.CrossRefGoogle Scholar
  67. 67.
    67. Moritz OL, Tam BM, Papermaster DS, Nakayama T. A functional rhodopsin-green fluorescent protein fusion protein localizes correctly in transgenic Xenopus laevis retinal rods and is expressed in a time-dependent manner. J Biol Chem 2001;276:28242–28251.PubMedCrossRefGoogle Scholar
  68. 68.
    68. Tam BM, Moritz OL, Hurd LB, Papermaster DS. Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis J Cell Biol 2000;151:1369–1380.PubMedCrossRefGoogle Scholar
  69. 69.
    69. Luo W, Marsh-Armstrong N, Rattner A, Nathans J. An outer segment localization signal at the C terminus of the photoreceptor–specific retinol dehydrogenase. J Neurosci 2004;24: 2623–2632.PubMedCrossRefGoogle Scholar
  70. 70.
    70. Concepcion F, Mendez A, Chen J. The carboxy-terminal domain is essential for rhodopsin transport in rod photoreceptors. Vis Res 2002;42:417–426.PubMedCrossRefGoogle Scholar
  71. 71.
    71. Sung CH, Makino C, Baylor D, Nathans J. A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment. J Neurosci 1994;14:5818–5833.PubMedGoogle Scholar
  72. 72.
    72. Hertz L and Zielke HR. Astrocytic control of glutamatergic acivity: astrocytes as stars of the show. Trends Neurosci 2005;27:735–742.CrossRefGoogle Scholar
  73. 73.
    73. Chaudhry FA, Reimer RJ, Edwards RH. The glutamine commute: take the N line and transfer to the A. J Cell Biol 2002;157:349–355.PubMedCrossRefGoogle Scholar
  74. 74.
    74. Deitmer JW, Broer A, Broer S. Glutamine efflux from astrocytes is mediated by multiple pathways. J Neurochem 2003;87:127–35.PubMedCrossRefGoogle Scholar
  75. 75.
    75. Broer S and Brookes N. Transfer of glutamine between astrocytes and neurons. J Neurochem 2001;77:705–719.PubMedCrossRefGoogle Scholar
  76. 76.
    76. Melone M, Quagliano F, Barbaresi P, Varoqui H, et al. Localization of the glutamine transporter SNAT1 in rat cerebral cortex and neighboring structures, with a note on its localization in human cortex. Cereb Cortex 2004;14:562–574.PubMedCrossRefGoogle Scholar
  77. 77.
    77. Melone M, Varoqui H, Erickson JD, Conti F. Localization of the Na(+)-coupled neutral amino acid transporter 2 in the cerebral cortex. Neuroscience 2006;140:281–292.PubMedCrossRefGoogle Scholar
  78. 78.
    78. Boulland JL, Olsen KK, Levy LM, Danbolt NC, et al. Cell-specific expression of the glutamine transporter SN1 suggests differences in dependence on the glutamine cycle. Eur J Neurosci 2002;15:1615–1631.PubMedCrossRefGoogle Scholar
  79. 79.
    79. Umapathy NS, Li W, Mysona BA, Smith SB, Ganapathy V. Expression and function of glutamine transporters SN1 (SNAT3) and SN2 (SNAT5) in retinal Müller cells. Invest Ophthalmol Vis Sci 2005;46:3980–3987.PubMedCrossRefGoogle Scholar
  80. 80.
    80. Tamarappoo BK, Raizada MK, Kilberg MS. Identification of a system N-like Na(+)-dependent glutamine transport activity in rat brain neurons. J Neurochem 1997;68:954–960.PubMedCrossRefGoogle Scholar
  81. 81.
    81. Boehmer C, Okur F, Setiawan I, Broer S, Lang F. Properties and regulation of glutamine transporter SN1 by protein kinases SGK and PKB. Biochem Biophys Res Commun 2003;306:156–62.PubMedCrossRefGoogle Scholar
  82. 82.
    82. Mackenzie B and Erickson JD. Sodium-coupled neutral amino acid (System N/A) transporters of the SLC38 gene family. Pflugers Arch 2004;447:784–795.PubMedCrossRefGoogle Scholar
  83. 83.
    83. Segawa H, Fukasawa Y, Miyamoto K, Takeda E, et al. Identification and functional characterization of a Na+-independent neutral amino acid transporter with broad substrate selectivity. J Biol Chem 1999;274:19745–19751.PubMedCrossRefGoogle Scholar
  84. 84.
    84. Broer S and Wagner CA. Structure-function relationships of heterodimeric amino acid transporters. Cell Biochem Biophys 2002;36:155–168.PubMedCrossRefGoogle Scholar
  85. 85.
    85. Nakauchi T, Ando A, Ueda-Yamada M, et al. Prevention of ornithine cytotoxicity by nonpolar side chain amino acids in retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 2003;44:5023–28.PubMedCrossRefGoogle Scholar
  86. 86.
    86. Bodoy S, Martin L, Zorzano A, Palacin M, et al. Identification of LAT4, a novel amino acid transporter with system L activity. J Biol Chem 2005;280:12002–12011.PubMedCrossRefGoogle Scholar
  87. 87.
    87. Dolinska M, Zablocka B, Sonnewald U, Albrecht J. Glutamine uptake and expression of mRNA's of glutamine transporting proteins in mouse cerebellar and cerebral cortical astrocytes and neurons. Neurochem Int 2004;44:75–81.PubMedCrossRefGoogle Scholar
  88. 88.
    88. Utsunomiya-Tate N, Endou H, Kanai Y. Cloning and functional characterization of a system ASC-like Na+-dependent neutral amino acid transporter. J Biol Chem 1996;271:14883–4890.PubMedCrossRefGoogle Scholar
  89. 89.
    89. O'Brien KB, Miller RF, Bowser MT. D-Serine uptake by isolated retinas is consistent with ASCT-mediated transport. Neurosci Lett 2005;385:58–63.PubMedCrossRefGoogle Scholar
  90. 90.
    90. Ward MM, Jobling AI, Kalloniatis M, Fletcher EL. Glutamate uptake in retinal glial cells during diabetes. Diabetologia 2005;48:351–60.PubMedCrossRefGoogle Scholar
  91. 91.
    91. Barnett NL, Pow DV, Bull ND. Differential perturbation of neuronal and glial glutamate transport systems in retinal ischemia. Neurochem Int 2001;39:291–19.PubMedCrossRefGoogle Scholar
  92. 92.
    92. Mawrin C, Pap T, Pallas M, et al. Changes of retinal glutamate transporter GLT-1 mRNA levels following optic nerve damage. Mol Vis 2003;13:10–13.Google Scholar
  93. 93.
    93 . Delfyer MN, Simonutti M, Neveux, et al. Does GDNF exert its neuroprotective effects on photoreceptors in the rd1 retina through the glial glutamate GLAST? Mol Vis 2005;11:677–687.Google Scholar
  94. 94.
    94. Sullivan RKP, Woldemussie E, Macnab L, Ruiz G, Pow DV. Evoked expression of the glutamate transporter GLT-1c in retinal ganglion cells in human glaucoma and in a rat model. Invest Ophthalmol Vis Sci 2006;47:3853–3859.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press, a part of Springer Science + Business Media, LLC 2008

Authors and Affiliations

  • Vijay Sarthy
    • 1
  • David Pow
    • 1
  1. 1.Department of OphthalmologyNorthwestern University Feinberg School of MedicineChicagoUSA

Personalised recommendations