Expression of the γ-aminobutyric acid (GABA) plasma membrane transporter-1 in monkey and human retina

Investigative Ophthalmology and Visual Science

Volumn 47, Issue 4, 2006, Pages 1682-1690

  Casini, Giovanni ^a   Rickman, Dennis W ^b,c   Brecha, Nicholas C ^d,e,f  

^a UNIVERSITY OF TUSCIA   (Italy)

^b DUKE UNIVERSITY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e JULES STEIN EYE INSTITUTE   (United States)

^f VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID CARRIER 1; CARRIER PROTEINS AND BINDING PROTEINS; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; BIOLOGICAL MARKER; SLC6A1 PROTEIN, HUMAN;

ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MONKEY; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA BIPOLAR GANGLION CELL; RETINA FOVEA; ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; MACACA; METABOLISM; RETINA; RETINA AMACRINE CELL; RETINA GANGLION CELL;

AMACRINE CELLS; ANIMALS; BIOLOGICAL MARKERS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; HUMANS; MACACA MULATTA; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; RETINA; RETINAL GANGLION CELLS;

EID: 33645965606     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.05-1117     Document Type: Article

References (88)

1. Borden LA. GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem Int. 1996;29:335-356.
2. Palacín M, Estèvez R, Bertran J, Zorzano A. Molecular biology of mammalian plasma membrane amino acid transporters. Phys Rev. 1998;78:969-1054.
3. Cherubini E, Conti F. Generating diversity at GABAergic synapses. Trends Neurosci. 2001;24:155-162.
4. O'Malley DM, Sandell JH, Masland RH. Co-release of acetylcholine and GABA by the starburst amacrine cells. J Neurosci. 1992;12:1394-1408.
5. Schwartz EA. Transport-mediated synapses in the retina. Phys Rev. 2002;82:875-891.
6. Yu D, Eldred WD. Nitric oxide stimulates γ-aminobutyric acid release and inhibits glycine release in retina. J Comp Neurol. 2005;483:278-291.
7. Pin JP, Bockaert J. Two distinct mechanisms differentially affected by excitatory amino acids trigger GABA release from fetal mouse striatal neurons in primary culture. J Neurosci. 1989;9:648-656.
8. Gaspary HL, Wang W, Richerson GB. Carrier-mediated GABA release activates GABA receptors on hippocampal neurons. J Neurophysiol. 1998;80:270-281.
9. Barakat L, Bordey A. GAT-1 and reversible GABA transport in Bergmann glia in slices. J Neurophysiol. 2002;88:1407-1419.
10. Guastella J, Nelson N, Nelson H, et al. Cloning and expression of a rat brain GABA transporter. Science. 1990;249:1303-1306.
11. Nelson H, Mandiyan S, Nelson N. Cloning of the human brain GABA transporter. FEBS Lett. 1990;269:181-184.
12. Borden LA, Smith KE, Hartig PR, Branchek TA, Weinshank RL. Molecular heterogeneity of the γ-aminobutyric acid GABA transport system: cloning of two novel high affinity GABA transporters from rat brain. J Biol Chem. 1992;267:21098-21104.
13. Borden LA, Dhar TG, Smith KE, Branchek TA, Gluchowski C, Weinshank RL. Cloning of the human homologue of the GABA transporter GAT-3 and identification of a novel inhibitor with selectivity for this site. Recept Channels. 1994;2:207-213.
14. Borden LA, Smith KE, Gustafson EL, Branchek TA, Weinshank RL. Cloning and expression of a betaine/GABA transporter from human brain. J Neurochem. 1995;64:977-984.
15. Clark JA, Deutch AY, Gallipoli PZ, Amara SG. Functional expression and CNS distribution of a β-alanine-sensitive neuronal GABA transporter. Neuron. 1992;9:337-348.
16. López-Corcuera B, Liu QR, Mandiyan S, Nelson H, Nelson N. Expression of a mouse brain cDNA encoding novel γ-aminobutyric acid transporter. J Biol Chem. 1992;267:17491-17493.
17. - dependent betaine transporter that is regulated by hypertonicity. J Biol Chem. 1992;267:649-652.
18. Liu Q-R, Lopez-Corcuera B, Mandiyan S, Nelson H, Nelson N. Molecular characterization of four pharmacologically distinct γ-aminobutyric acid transporters in mouse brain. J Biol Chem. 1993;268:2106-2112.
19. Minelli A, Brecha NC, Karschin C, De Biasi S, Conti F. GAT-1 a high-affinity GABA plasma membrane transporter is localized to neurons and astroglia in cerebral cortex. J Neurosci. 1995;15:7734-7746.
20. Minelli A, De Biasi S, Brecha NC, Conti F. GAT-3 a high-affinity GABA plasma membrane transporter is localized to astrocytic processes and it is not confined to the vicinity of GABAergic synapses in the cerebral cortex. J Neurosci. 1996;16:6255-6264.
21. Ribak CE, Tong WMY, Brecha NC. GABA plasma membrane transporters GAT-1 and GAT-3 display different distributions in the rat hippocampus. J Comp Neurol. 1996;367:595-606.
22. Conti F, Melone M, De Biasi S, Minelli A, Brecha NC, Ducati A. Neuronal and glial localization of GAT-1 a high-affinity gamma-aminobutyric acid plasma membrane transporter in human cerebral cortex with a note on its distribution in monkey cortex. J Comp Neurol. 1998;396:51-63.
23. Augood SJ, Waldvogel HJ, Munkle MC, Faull RL, Emson PC. Localization of calcium-binding proteins and GABA transporter GAT-1 messenger RNA in the human subthalamic nucleus. Neuroscience. 1999;88:521-534.
24. Ikegaki N, Saito N, Hashima M, Tanaka C. Production of specific antibodies against GABA transporter subtypes GAT1, GAT2, GAT3 and their application to immunocytochemistry. Mol Brain Res. 1994;26:47-54.
25. Durkin MM, Smith KE, Borden LA, Weinshank RL, Branchek TE, Gustafson EL. Localization of messenger RNAs encoding three GABA transporters in rat brain: an in situ hybridization study. Mol Brain Res. 1995;33:7-21.
26. Conti F, Zuccarello LV, Barbaresi P, Minelli A, Brecha NC, Melone M. Neuronal glial and epithelial localization of gamma-aminobutyric acid transporter 2, a high-affinity gamma-aminobutyric acid plasma membrane transporter in the cerebral cortex and neighboring structures. J Comp Neurol. 1999;409:482-494.
27. Conti F, Minelli A, Melone M. GABA transporters in the mammalian cerebral cortex: localization development and pathological implications. Brain Res Rev. 2004;45:196-212.
28. Dingledine R, Korn SJ. Gamma-aminobutyric acid uptake and the termination of inhibitory synaptic potentials in the rat hippocampal slice. J Physiol. 1985;366:387-409.
29. Solis JM, Nicoll RA. Postsynaptic action of endogenous GABA released by nipecotic acid in the hippocampus. Neurosci Lett. 1992;147:16-20.
30. Thompson SM, Gahwiler BH. Effects of the GABA uptake inhibitor tiagabine on inhibitory synaptic potentials in rat hippocampal slice cultures. J Neurophysiol. 1992;67:1698-1701.
31. Isaacson JS, Solis JM, Nicoll RA. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron. 1993;10:165-175.
32. Engel D, Schmitz D, Gloveli T, Frahm C, Heinemann U, Draguhn A. Laminar difference in GABA uptake and GAT-1 expression in rat CA1. J Physiol. 1998;512:643-649.
33. Ichinose T, Lukasiewicz PD. GABA transporters regulate inhibition in the retina by limiting GABA(C) receptor activation. J Neurosci. 2002;22:3285-3292.
34. A receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci. 2003;23:10650-10661.
35. Vivar C, Gutierrez R. Blockade of the membranal GABA transporter potentiates GABAergic responses evoked in pyramidal cells by mossy fiber activation after seizures. Hippocampus. 2005;15:281-284.
36. Frahm C, Enge D, Draguhn A. Efficacy of background GABA uptake in rat hippocampal slices. Neuroreport. 2001;12:1593-1596.
37. Mitchell SJ, Silver RA. GABA spillover from single inhibitory axons suppresses low-frequency excitatory transmission at the cerebellar glomerulus. J Neurosci. 2000;20:8651-8658.
38. Brecha NC, Weigmann C. Expression of GAT-1, a high affinity gamma-aminobutyric acid plasma membrane transporter, in the rat retina. J Comp Neurol. 1994;354:602-611.
39. Howd AG, Rattray M, Butt AM. Expression of GABA transporter mRNAs in the developing and adult rat optic nerve. Neurosci Lett. 1997;235:98-100.
40. Ruiz M, Egal H, Sarthy V, Qian X, Sarkar HK. Cloning expression and localization of a mouse retinal γ-aminobutyric acid transporter. Invest Ophthalmol Vis Sci. 1994;35:4039-4048.
41. Honda S, Yamamoto M, Saito N. Immunocytochemical localization of three subtypes of GABA transporter in rat retina. Mol Brain Res. 1995;33:319-325.
42. Johnson J, Chen TK, Rickman DW, Evans C, Brecha NC. Multiple γ-aminobutyric acid plasma membrane transporters GAT-1, GAT-2, GAT-3 in the rat retina. J Comp Neurol. 1996;375:212-224.
43. Hu M, Bruun A, Ehinger B. Expression of GABA transporter subtypes GAT-1, GAT-3 in the adult rabbit retina. Acta Ophthalmol Scand. 1999;77:255-260.
44. Trasarti L, Casini G, Sabatini A, Bosco L, Brecha NC. GABA plasma membrane transporter-1 GAT-1 expression in the rabbit retina. Soc Neurosci Abs. 1999;25:166.
45. Dmitrieva NA, Lindstrom JM, Keyser KT. The relationship between GABA-containing cells and the cholinergic circuitry in the rabbit retina. Vis Neurosci. 2001;18:93-100.
46. Biedermann B, Bringmann A, Reichenbach A. High-affinity GABA uptake in retinal glial Müller cells of the guinea pig: electrophysiological characterization immunohistochemical localization and modeling of efficiency. Glia. 2002;39:217-228.
47. Sivakami S, Ganapathy V, Leibach FH, Miyamoto Y. The gamma-aminobutyric acid transporter and its interaction with taurine in the apical membrane of the bovine retinal pigment epithelium. Biochem J. 1992;283:391-397.
48. Ehinger B. Glial and neuronal uptake of GABA glutamic acid glutamine and glutathione in the rabbit retina. Exp Eye Res. 1977;25:221-234.
49. Agardh E, Ehinger B. 3H-muscimol 3H-nipecotic acid and 3H-isoguvacine as autoradiographic markers for GABA neurotransmission. J Neural Transm. 1982;54:1-18.
50. Hendrickson A, Ryan M, Noble B, Wu JY. Colocalization of [3H]muscimol and antisera to GABA and glutamic acid decarboxylase within the same neurons in monkey retina. Brain Res. 1985;348:391-396.
51. Mosinger JL, Yazulla S. Colocalization of GAD-like immunoreactivity and 3H-GABA uptake in amacrine cells of rabbit retina. J Comp Neurol. 1985;240:396-406.
52. Pow DW, Baldridge W, Crook DK. Activity-dependent transport of GABA analogues into specific cell types demonstrated at high resolution using a novel immunocytochemical strategy. Neuroscience. 73;1996:1129-1143.
53. Pow DV, Sullivan RK, Williams SM, Scott HL, Dodd PR, Finkelstein D. Differential expression of the GABA transporters GAT-1 and GAT-3 in brains of rats cats monkeys and humans. Cell Tissue Res. 2005;320:379-392.
54. Erdo SL, Wolff JR. Gamma-aminobutyric acid outside the mammalian brain. J Neurochem. 1990;54:363-372.
55. Wong HC, Sternini C, Lloyd K, De Giorgio R, Walsh JH. Monoclonal antibody to VIP: production characterization immunoneutralizing activity and usefulness in cytochemical staining. Hybridoma. 1996;15:133-139.
56. Rohrer H, Acheson AL, Thibault J, Thoenen H. Developmental potential of quail dorsal root ganglion cells analyzed in vitro and in vivo. J Neurosci. 1986;6:2616-2624.
57. Onoda N, Fujita SC. A monoclonal antibody specific for a subpopulation of retinal bipolar cells in the frog and other vertebrates. Brain Res. 1987;416:359-363.
58. Greferath U, Grünert U, Wässle H. Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. J Comp Neurol. 1990;301:433-442.
59. Woo T-U, Whitehead RE, Melchitzky DS, Lewis DA. A subclass of prefrontal γ-aminobutyric acid axon terminals are selectively altered in schizophrenia. Proc Natl Acad Sci USA. 1998;95:5341-5346.
60. De Biasi S, Vitellaro-Zuccarello L, Brecha NC. Immunoreactivity for the GABA transporter-1 and GABA transporter-3 is restricted to astrocytes in the rat thalamus: a light and electron-microscopic immunolocalization. Neuroscience. 1998;83:815-828.
61. Cajal SR. La rétine des vertèbres. Cellule. 1893;9:119-255.
62. Casini G, Brecha NC. Colocalization of vasoactive intestinal polypeptide and GABA immunoreactivities in a population of wide-field amacrine cells in the rabbit retina. Vis Neurosci. 1992;8:373-378.
63. Nguyen-Legros J, Versaux-Botteri C, Savy C. Aminergic and GABAergic retinal cell populations in mammals. Microsc Res Tech. 1997;36:26-42.
64. Agardh E, Ehinger B, Wu JY. GABA and GAD-like immunoreactivity in the primate retina. Histochem. 1987;86:485-490.
65. Grünert U, Wässle H. GABA-like immunoreactivity in the macaque monkey retina: a light and electron microscopic study. J Comp Neurol. 1990;297:509-524.
66. Martin PR, Grünert U. Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. J Comp Neurol. 1992;323:269-287.
67. Van Haesendonck E, Missotten L. A subgroup of bipolar cells in human retina is GABA-immunoreactive. Neurosci Lett. 1993;161:187-190.
68. Kalloniatis M, Marc RE, Murry RF. Amino acid signatures in the primate retina. J Neurosci. 1996;16:6807-6829.
69. da Costa BL, Hokoç JN, Pinaud RR, Gattass R. GABAergic retinocollicular projection in the New World monkey Cebus apella. Neuroreport. 1997;8:1797-1802.
70. --dependent neurotransmitter transporters in bovine retina: identification and localization by in situ hybridization histochemistry. Vis Neurosci. 1995;12:1135-1142.
71. Agardh E, Ehinger B. Retinal GABA neuron labelling with [3H]isoguvacine in different species. Exp Eye Res. 1983;36:215-229.
72. Ryan MK, Hendrickson AE. Interplexiform cells in macaque monkey retina. Exp Eye Res. 1987;45:57-66.
73. Sarthy PV, Fu M. Localization of L-glutamic acid decarboxylase mRNA in monkey and human retina by in situ hybridization. J Comp Neurol. 1989;288:691-697.
74. Crooks J, Kolb H. Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. J Comp Neurol. 1992;315:287-302.
75. Koontz MA, Hendrickson LE, Brace ST, Hendrickson AE. Immunocytochemical localization of GABA and glycine in amacrine and displaced amacrine cells of macaque monkey retina. Vis Res. 1993;33:2617-2628.
76. Nag TC, Wadhwa S. Expression of GABA in the fetal postnatal and adult human retinas: an immunohistochemical study. Vis Neurosci. 1997;14:425-432.
77. Andrade da Costa BL, de Mello FG, Hokoç JN. Transporter-mediated GABA release induced by excitatory amino acid agonist is associated with GAD67 but not GAD65 immunoreactive cells of the primate retina. Brain Res. 2000;863:132-142.
78. Vardi N, Kaufman DL, Sterling P. Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase. Vis Neurosci. 1994;11:135-142.
79. Sarthy PV, Fu M. Localization of L-glutamic acid decarboxylase mRNA in cat retinal horizontal cells by in situ hybridization. J Comp Neurol. 1989;288:593-600.
80. Hökfelt T, Ljungdahl A. Autoradiographic identification of cerebral and cerebellar cortical neurons accumulating labeled gamma-aminobutyric acid 3H-GABA. Exp Brain Res. 1972;14:354-362.
81. Sotelo C, Privat A, Drian MJ. Localization of [3H]GABA in tissue culture of rat cerebellum using electron microscope radioautography. Brain Res. 1972;45:302-308.
82. Rattray M, Priestley JV. Differential expression of GABA transporter-1 messenger RNA in subpopulations of GABA neurones. Neurosci Lett. 1993;156:163-166.
83. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci. 1994;14:1834-1855.
84. Ribak CE, Tong WMY, Brecha NC. Astrocytic processes compensate for the apparent lack of GABA transporters in the axon terminals of cerebellar Purkinje cells. Anat Embryol. 1996;194:379-390.
85. Bruun A, Ehinger B. Uptake of certain possible neurotransmitters into retinal neurons of some mammals. Exp Eye Res. 1974;19:435-447.
86. Koontz MA, Hendrickson AE, Ryan MK. GABA-immunoreactive synaptic plexus in the nerve fiber layer of primate retina. Vis Neurosci. 1989;2:19-25.
87. Davanger S, Ottersen OP, Storm-Mathisen J. Glutamate GABA and glycine in the human retina: an immunocytochemical investigation. J Comp Neurol. 1991;311:483-494.
88. Wilson JR, Cowey A, Somogy P. GABA immunopositive axons in the optic nerve and optic tract of macaque monkeys. Vis Res. 1996;10:1357-1363.