Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-22T13:26:16.258Z Has data issue: false hasContentIssue false

Differential cellular and subcellular distribution of glutamate transporters in the cat retina

Published online by Cambridge University Press:  01 July 2004

BOZENA FYK-KOLODZIEJ
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit
PU QIN
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit
ARTURIK DZHAGARYAN
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit
ROBERTA G. POURCHO
Affiliation:
Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit

Abstract

Retrieval of glutamate from extracellular sites in the retina involves at least five excitatory amino acid transporters. Immunocytochemical analysis of the cat retina indicates that each of these transporters exhibits a selective distribution which may reflect its specific function. The uptake of glutamate into Müller cells or astrocytes appears to depend upon GLAST and EAAT4, respectively. Staining for EAAT4 was also seen in the pigment epithelium. The remaining transporters are neuronal with GLT-1α localized to a number of cone bipolar, amacrine, and ganglion cells and GLT-1v in cone photoreceptors and several populations of bipolar cells. The EAAC1 transporter was found in horizontal, amacrine, and ganglion cells. Staining for EAAT5 was seen in the axon terminals of both rod and cone photoreceptors as well as in numerous amacrine and ganglion cells. Although some of the glutamate transporter molecules are positioned for presynaptic or postsynaptic uptake at glutamatergic synapses, others with localizations more distant from such contacts may serve in modulatory roles or provide protection against excitoxic or oxidative damage.

Type
Research Article
Copyright
2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arriza, J.L., Fairman, W.A., Wadiche, J.L., Murdoch, G.H., Kavanaugh, M.P., & Amara, S.G. (1994). Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. Journal of Neuroscience 14, 55595569.Google Scholar
Arriza, J.L., Eliasof, S., Kavanaugh, M.P., & Amara, S.G. (1997). Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proceedings of the National Academy of Sciences of the U.S.A. 94, 41554160.CrossRefGoogle Scholar
Barnett, N.L. & Pow, D.V. (2000). Antisense knockdown of GLAST, a glial glutamate transporter, compromises retinal function. Investigative Ophthalmology and Visual Science 41, 585591.Google Scholar
Brandstätter, J.H., Koulen, P., & Wässle, H. (1998). Diversity of glutamate receptors in the mammalian retina. Vision Research 38, 13851397.CrossRefGoogle Scholar
Cai, W. & Pourcho, R.G. (1999). Localization of metabotropic glutamate receptors mGluR1α and mGluR2/3 in the cat retina. Journal of Comparative Neurology 407, 427437.3.0.CO;2-9>CrossRefGoogle Scholar
Chen, B. & Pourcho, R.G. (1995). Morphological diversity and glutamate immunoreactivity of retinal terminals in the suprachiasmatic nucleus of the cat. Journal of Comparative Neurology 361, 108118.CrossRefGoogle Scholar
Chen, Y. & Swanson, R.A. (2003). The glutamate transporters EAAT2 and EAAT3 mediate cysteine uptake in cortical neuron cultures. Journal of Neurochemistry 84, 13321339.CrossRefGoogle Scholar
Chen, W., Aoki, C., Mahadomrongkul, V., Gruber, C.E., Wang, G.J., Blitzblau, R., Irwin, N., & Rosenberg, P.A. (2002). Expression of a variant form of the glutamate transporter GLT1 in neuronal cultures and in neurons and astrocytes of the rat brain. Journal of Neuroscience 22, 21422152.Google Scholar
Chuhma, N., Zhang, J., Masson, J., Zhuang, X., Sulzer, D., Hen, R., & Rayport, S. (2004). Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses. Journal of Neuroscience 24, 972981.Google Scholar
Coco, S., Verderio, C., Trotti, D., Rothstein, J.D., Volterra, A., & Matteoli, M. (1997). Non-synaptic localization of the glutamate transporter EAAC1 in cultured hippocampal neurons. European Journal of Neuroscience 9, 19021910.CrossRefGoogle Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331345.Google Scholar
Derouiche, A. & Rauen, T. (1995). Coincidence of L-glutamate/L-aspartate transporter (GLAST) and glutamine synthetase (GS) immunoreactions in the retinal glia: Evidence for coupling of GLAST and GS in transmitter clearance. Journal of Neuroscience Research 42, 131143.CrossRefGoogle Scholar
Docherty, M., Bradford, H.F., & Wu, J.Y. (1987). Co-release of glutamate and aspartate from cholinergic and GABAergic synaptosomes. Nature 330, 6466.CrossRefGoogle Scholar
Eliasof, S. & Werblin, F. (1993). Characterization of the glutamate transporter in retinal cones of the tiger salamander. Journal of Neuroscience 13, 402411.Google Scholar
Eliasof, S., Arriza, J.L., Leighton, B.H., Amara, S.G., & Kavanaugh, M.P. (1998). Localization and function of five glutamate transporters cloned from the salamander retina. Vision Research 38, 14431454.CrossRefGoogle Scholar
Euler, T. & Wässle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. Journal of Comparative Neurology 361, 461478.CrossRefGoogle Scholar
Fairman, W.A., Vandenberg, R.J., Arriza, J.L., Kavanaugh, M.P., & Amara, S.G. (1995). An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375, 599603.CrossRefGoogle Scholar
Fisher, S.K. & Steinberg, R.H. (1982). Origin and organization of pigment epithelial apical projections to cones in cat retina. Journal of Comparative Neurology 206, 131145.CrossRefGoogle Scholar
Fyk-Kolodziej, B., Cai, W., & Pourcho, R.G. (2002). Distribution of protein kinase C isoforms in the cat retina. Visual Neuroscience 19, 549562.CrossRefGoogle Scholar
Fyk-Kolodziej, B., Qin, P., & Pourcho, R.G. (2003). Identification of a cone bipolar cell in cat retina which has input from both rod and cone photoreceptors. Journal of Comparative Neurology 464, 104113.CrossRefGoogle Scholar
Gaal, L., Roska, B., Picaud, S.A., Wu, S.M., Marc, R., & Werblin, F.S. (1998). Postsynaptic response kinetics are controlled by a glutamate transporter at cone photoreceptors. Journal of Neurophysiology 79, 190196.Google Scholar
Greferath, U., Grünert, U., & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433442.CrossRefGoogle Scholar
Grünert, U., Martin, P.R., & Wässle, H. (1994). Immunocytochemical analysis of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 361, 461478.Google Scholar
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 the two glutamate transporters GLAST and GLT-1 in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 95, 46634666.CrossRefGoogle Scholar
Hu, W.-H., Walters, W.M., Xia, A.-M., Karmally, S.A., & Bethea, J.R. (2003). Neuronal glutamate transporter EAAT4 is expressed in astrocytes. Glia 44, 1325.CrossRefGoogle Scholar
Jojich, L. & Pourcho, R.G. (1996). Glutamate immunoreactivity in the cat retina: A quantitative study. Visual Neuroscience 13, 117133.CrossRefGoogle Scholar
Kanai, Y. & Hediger, M.A. (1992). Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360, 467471.CrossRefGoogle Scholar
Kolb, H., Cuenca, N., Wang, H.-H., & DeKorver, L. (1990). The synaptic organization of the dopaminergic amacrine cell in the cat retina. Journal of Neurocytology 19, 343366.CrossRefGoogle Scholar
Kolb, H., Cuenca, N., & DeKorver, L. (1991). Postembedding immunocytochemistry for GABA and glycine reveals the synaptic relationship of the dopaminergic amacrine cell of the cat retina. Journal of Comparative Neurology 310, 267284.CrossRefGoogle Scholar
Kugler, P. & Beyer, A. (2003). Expression of glutamate transporters in human and rat retina and optic nerve. Histochemical Cell Biology 120, 199212.CrossRefGoogle Scholar
Land, P.Q., Kyonka, E., & Shamalla-Hannah, L. (2004). Vesicular glutamate transporters in the lateral geniculate nucleus: Expression of VGLUT2 by retinal terminals. Brain Research 996, 251254.CrossRefGoogle Scholar
Legault, M., Congar, P., Michel, F.J., & Trudeau, L.E. (2002). Presynaptic action of neurotensin on cultured ventral tegmental area dopaminergic neurones. Neuroscience 111, 177187.CrossRefGoogle Scholar
Lehre, K.P., Davanger, S., & Danbolt, N.C. (1997). Localization of the glutamate transporter protein GLAST in rat retina. Brain Research 744, 129137.CrossRefGoogle Scholar
Li, Q. & Puro, D.G. (2002). Diabetes-induced dysfunction of the glutamate transporter in retinal Müller cells. Investigative Ophthalmology and Visual Science 43, 31093116.Google Scholar
Lin, C.L., Tzingounis, AV., Jin, L., Furuta, A., Kavanaugh, M.P., & Rothstein, J.D. (1998). Molecular cloning and expression of the rat EAAT4 glutamate transporter subtype. Brain Research and Molecular Brain Research 63, 174179.CrossRefGoogle Scholar
Maenpaa, H., Gegelashvili, G., & Tahti, H. (2004). Expression of glutamate transporter subtypes in cultured retinal pigment epithelial and retinoblastoma cells. Current Eye Research 28, 159165.CrossRefGoogle Scholar
Marc, R.E., Murry, R.F., Fisher, S.K., Linberg, K.A., Lewis, G.P., & Kalloniatis, M. (1998). Amino acid signatures in the normal cat retina. Investigative Ophthalmology and Visual Science 39, 16851693.Google Scholar
Martin, K.R.G., Levkovitch-Verbin, H., Valenta, D., Baumrind, L., Pease, M.E., & Quigley, H.A. (2002). Retinal glutamate transporter changes in experimental glaucoma and after optic nerve transection in the rat. Investigative Ophthalmology and Visual Science 43, 22362243.Google Scholar
Miyamoto, Y. & DelMonte, M.A. (1994). Na+-dependent glutamate transporter in human retinal pigment epithelial cells. Investigative Ophthalmology and Visual Science 35, 35893598.Google Scholar
Montero, M.M. (1990). Quantitative immunogold analysis reveals high glutamate levels in synaptic terminals of retino-geniculate, cortico-geniculate, and geniculo-cortical axons of the cat. Visual Neuroscience 4, 437443.CrossRefGoogle Scholar
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, 929933.Google Scholar
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 11831195.CrossRefGoogle Scholar
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592614.Google Scholar
Palmer, M.J., Taschenberger, H., Hull, C., Tremere, L., & von Gersdorff, H. (2003). Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. Journal of Neuroscience 23, 48314841.Google Scholar
Pines, G., Danbolt, N.C., Bjoras, M., Zhang, Y., Bendahan, A., Eide, L., Koepsell, H., Storm-Mathisen, J., Seeger, E., & Kanner, B.I. (1992). Cloning and expression of a rat brain L-glutamate transporter. Nature 360, 464467.CrossRefGoogle Scholar
Pourcho, R.G. (1982). Dopaminergic amacrine cells in the cat retina. Brain Research 252, 101109.CrossRefGoogle Scholar
Pourcho, R.G. & Goebel, D.J. (1987). A combined Golgi and autoradiographic study of 3H-glycine-accumulating cone bipolar cells in the cat retina. Journal of Neuroscience 7, 11781188.Google Scholar
Pow, D.V. (2001). Amino acids and their transporters in the retina. Neurochemistry International 38, 463484.CrossRefGoogle Scholar
Pow, D.V. & Barnett, N.L. (1999). Changing patterns of spatial buffering of glutamate in developing rat retina are mediated by the Müller and glutamate transporter GLAST. Cell and Tissue Research 297, 5766.CrossRefGoogle Scholar
Pow, D.V. & Barnett, N.L. (2000). Developmental expression of excitatory amino acid transporter 5: A photoreceptor and bipolar cell glutamate transporter in rat retina. Neuroscience Letters 280, 2124.CrossRefGoogle Scholar
Pow, D.V., Barnett, N.L., & Penfold, P. (2000). Are neuronal transporters relevant in retinal glutamate homeostasis? Neurochemistry International 37, 191198.Google Scholar
Pow, D.V. & Crook, D.K. (1995). Immunocytochemical evidence for the presence of high levels of reduced glutathione in radial glial cells and horizontal cells in the rabbit retina. Neuroscience Letters 193, 2528.CrossRefGoogle Scholar
Pow, D.V. & Robinson, S.R. (1994). Glutamate in some retinal neurones is derived solely from glia. Neuroscience 60, 355366.CrossRefGoogle Scholar
Qin, P. & Pourcho, R.G. (1999). Localization of AMPA-selective glutamate receptor subunits in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 16, 169177.Google Scholar
Qin, P. & Pourcho, R.G. (2001). Immunocytochemical localization of kainate-selective glutamate receptor subunits GluR5, GluR6, and GluR7 in the cat retina. Brain Research 890, 211221.CrossRefGoogle Scholar
Rabl, K., Bryson, E.J., & Thoreson, W.B. (2003). Activation of glutamate transporters in rods inhibits presynaptic calcium currents. Visual Neuroscience 20, 557566.CrossRefGoogle Scholar
Rauen, T. (2000). Diversity of glutamate transporter expression and function in the mammalian retina. Amino Acids 19, 5362.CrossRefGoogle Scholar
Rauen, T. & Kanner, B.I.. (1994). Localization of the glutamate transporter GLT-1 in rat and macaque monkey retina. Neuroscience Letters 169, 137140.CrossRefGoogle Scholar
Rauen, T., Rothstein, J.D., & Wässle, H. (1996). Differential expression of three glutamate transporter subtypes in the rat retina. Cell and Tissue Research 286, 325336.CrossRefGoogle Scholar
Rauen, T., Taylor, W.R., Kuhlbrodt, K., & Wiessner, M. (1998). High-affinity glutamate transporters in the rat retina: A major role of the glial glutamate transporters GLAST-1 in transmitter clearance. Cell and Tissue Research 291, 1931.Google Scholar
Reye, P., Sullivan, R., Fletcher, E.L., & Pow, D.V. (2002). Distribution of two slice variants of the glutamate transporter GLT1 in the retinas of humans, monkeys, rabbits, rats, cats, and chickens. Journal of Comparative Neurology 445, 112.Google Scholar
Roska, B., Gaal, L., & Werblin, F.S. (1998). Voltage-dependent uptake is a major determinant of glutamate concentration at the cone synapse: An analytical study. Journal of Neurophysiology 80, 19511960.Google Scholar
Sarantis, M., Everett, K., & Attwell, D. (1988). A presynaptic action of glutamate at the cone output synapse. Nature 332, 451453.CrossRefGoogle Scholar
Schmitt, A., Asan, E., Lesch, K.P., & Kugler, P. (2002). A splice variant of glutamate transporter GLT1/EAAT2 expressesed in neurons: Cloning and localization in rat nervous system. Neuroscience 109, 4561.CrossRefGoogle Scholar
Schultz, K. & Stell, W.K. (1996). Immunocytochemical localization of the high-affinity glutamate transporter, EAAC1, in the retina of representative vertebrate species. Neuroscience Letters 211, 191194.CrossRefGoogle Scholar
Sepkudy, J.P., Cohen, A.S., Eccles, C., Rafiq, A., Behar, K., Ganel, R., Coulter, D.A., & Rothstein, J.D. (2002). A neuronal glutamate transporter contributes to neurotransmitter GABA synthesis and epilepsy. Journal of Neuroscience 22, 63726379.Google Scholar
Sullivan, R., Rauen, T., Fischer, F., Wiessner, M., Grewer, C., Bicho, A., & Pow, D.V. (2004). Cloning, transport properties, and differential localization of two splice variants of GLT-1 in the rat CNS: Implications for CNS glutamate homeostasis. Glia 45, 155169.CrossRefGoogle Scholar
Sulzer, D., Joyce, M.P., Lin, L., Geldwert, D., Haber, S.N., Hattori, T., & Rayport, S. (1998). Dopamine neurons make glutamatergic synapses in vitro. Journal of Neuroscience 18, 45884602.Google Scholar
Tachibana, M. & Kaneko, A. (1988). L-glutamate-induced depolarization in solitary photoreceptors: A process that may contribute to the interaction between photoreceptors in situ. Proceedings of the National Academy of Sciences of the U.S.A. 85, 53155319.CrossRefGoogle Scholar
Utsunomiya-Tate, N., Endou, H., & Kanai, Y. (1997). Tissue specific variants of glutamate transporter GLT1. FEBS Letters 416, 312316.CrossRefGoogle Scholar
Vandenbranden, C.A., Yazulla, S., Studholme, K.M., Kamphuis, W., & Kamermans, M. (2000). . Immunocytochemical localization of the glutamate transporter GLT-1 in goldfish (Carassius auratus) retina. Journal of Comparative Neurology 423, 440451.3.0.CO;2-7>CrossRefGoogle Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of AII amacrine cells in mammalian retina. Journal of Neuroscience 7, 41154128.Google Scholar
Vorwerk, C.K., Naskar, R., Schuettauf, F., Quinto, L., Zurakowski, D., Gochenauer, G., Robinson, M.B., Mackler, S.A., & Dreyer, E.B. (2000). Depression of retinal glutamate transporter function leads to elevated intravitreal glutamate levels and ganglion cell death. Investigative Ophthalmology and Visual Science 41, 36153621.Google Scholar
Wadiche, J.I., Amara, S.G., & Kavanaugh, M.P. (1995). Ion fluxes associated with excitatory amino acid transport. Neuron 15, 721728.CrossRefGoogle Scholar
Ward, M.M., Jobling, A.I., Puthussery, T., Foster, L.E., & Fletcher, E.L. (2004). Localization and expression of the glutamate transporter, excitatory amino acid transporter 4, within astrocytes of the rat retina. Cell and Tissue Research 315, 305310.CrossRefGoogle Scholar
Wiessner, M., Fletcher, E.L., Fischer, F., & Rauen, T. (2002). Localization and possible function of the glutamate transporter, EAAC1, in the rat retina. Cell and Tissue Research 310, 3140.CrossRefGoogle Scholar
Yang, C.Y. & Yazulla, S. (1994). Glutamate-, GABA-, and GAD-immunoreactivities co-localize in bipolar cells of tiger salamander. Visual Neuroscience 11, 11931203.CrossRefGoogle Scholar