Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-18T19:07:27.220Z Has data issue: false hasContentIssue false

Differential distribution of glycine transporters in Müller cells and neurons in amphibian retinas

Published online by Cambridge University Press:  19 July 2007

ZHENG JIANG
Affiliation:
Department of Biomedical Science, Florida Atlantic University, Boca Raton, Florida
BAOQIN LI
Affiliation:
Department of Biomedical Science, Florida Atlantic University, Boca Raton, Florida
FRANTISEK JURSKY
Affiliation:
Department of Neurobiology, Institute of Molecular Biology, Slovak Academy of Sciences, Bratislava, Slovak Republic
WEN SHEN
Affiliation:
Department of Biomedical Science, Florida Atlantic University, Boca Raton, Florida

Abstract

Amphibian retinas are commonly used for electrophysiological studies on neural function and transduction because they share the same general properties as higher vertebrate retinas. Glycinergic synapses have been well described in amphibian retinas. However, the role of glycine transporters in the synapses is largely unknown. We studied the distribution and function of glycine transporters in the retinas from tiger salamanders, mudpuppies, and leopard frogs by immunofluorescence labeling and whole-cell recording methods. Our results indicated that GlyT1- and GlyT2-like transporters were present in Müller cells and neurons, respectively. GlyT1 labeling was present in Müller glial cells and co-localized with Glial fibrillary acidic protein (GFAP), a Müller cell marker, whereas the GlyT2 immunoreactivity was present in the somas of amacrine cells (ACs) and processes in the inner plexiform layer (IPL) and the outer plexiform layer (OPL). Because the axon processes of glycinergic interplexiform cells (IPCs) are the only source of glycine input in the OPL, GlyT2 staining revealed a spatial pattern of the axon processes of IPCs in the OPL. The function of GlyT2 in the IPCs was studied in tiger salamander retinal horizontal cells (HCs) by whole-cell gramicidin perforated recording. The results demonstrated that inhibition of GlyT2 by a specific inhibitor, amoxapine, increased a tonic glycine input to HCs. Thus, the GlyT2 transporter is responsible for uptake of synaptic glycine in the outer retina. We also compared the distribution of glycine transporters in other amphibian species: salamander, mudpuppy, and frog. The results are consistent with the general pattern that GlyT1-like transporters are present in Müller cells and GlyT2-like transporters in neurons in amphibian retinas.

Type
Research Article
Copyright
2007 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

Bergeron, R., Meyer, T.M., Coyle, J.T. & Greene, R.W. (1998). Modulation of N-methyl-D-aspartate receptor function by glycine transport. Proceedings of the National Academy of Science USA 95, 1573015734.CrossRefGoogle Scholar
Cubelos, B., Gimenez, C. & Zafra, F. (2005). Localization of the GLYT1 glycine transporter at glutamatergic synapses in the rat brain. Cerebral Cortex 15, 448459.CrossRefGoogle Scholar
Deng, P., Cuenca, N., Doerr, T., Pow, D.V., Miller, R. & Kolb, H. (2001). Localization of neurotransmitters and calcium binding proteins to neurons of salamander and mudpuppy retinas. Vision Research 41, 17711783.CrossRefGoogle Scholar
Du, J.L., Xu, L.Y. & Yang, X.L. (2002). Glycine receptors and transporters on bullfrog retinal Muller cells. Neuroreport 13, 16531656.CrossRefGoogle Scholar
Ebihara, S., Yamamoto, T., Obata, K. & Yanagawa, Y. (2004). Gene structure and alternative splicing of the mouse glycine transporter type-2. Biochemical and Biophysical Research Communications 317, 857864.CrossRefGoogle Scholar
Eliasof, S., Arriza, J.L., Leighton, B.H., Kavanaugh, M.P. & Amara, S.G. (1998). Excitatory amino acid transporters of the salamander retina: Identification, localization and function. Journal of Neuroscience 18, 698712.Google Scholar
Eulenburg, V., Armsen, W., Betz, H. & Gomeza, J. (2005). Glycine transporters: Essential regulators of neurotransmission. Trends in Biochemical Sciences 30, 325333.CrossRefGoogle Scholar
Gomeza, J., Hulsmann, S., Ohno, K., Eulenburg, V., Szoke, K., Richter, D. & Betz, H. (2003). Inactivation of the glycine transporter 1 gene discloses vital role of glial glycine uptake in glycinergic inhibition. Neuron 40, 785796.CrossRefGoogle Scholar
Horiuchi, M., Nicke, A., Gomeza, J., Ashcrafi, A., Schmalzing, G. & Betz, H. (2001). Surface-localized glycine transporters 1 and 2 function as monoeric proteins in Xenooopus oocytes. Proceedings of the National Academy of Sciences of the United States of America 98, 14481453.CrossRefGoogle Scholar
Jursky, F. & Nelson, N. (1995). Localization of glycine neurotransmitter transporter (GLYT2) reveals correlation with the distribution of glycine receptor. Journal of Neurochemistry 64, 10261033.Google Scholar
Jursky, F., Tamura, S., Tamura, A., Mandiyan, S., Nelson, H. & Nelson, N. (1994). Structure, function and brain localization of neurotransmitter transporters. Journal of Experimental Biology 196, 283295.Google Scholar
Lee, S.C., Zhong, Y.M. & Yang, X.L. (2005). Expression of glycine receptor and transporter on bullfrog retinal Muller cells. Neuroscience Letters 387, 7579.CrossRefGoogle Scholar
Liepe, B.A., Stone, C., Koistinaho, J. & Copenhagen, D.R. (1994). Nitric oxide synthase in Muller cells and neurons of salamander and fish retina. Journal of Neuroscience 14, 76417654.Google Scholar
Lopez-Corcuera, B., Geerlings, A. & Aragon, C. (2001). Glycine neurotransmitter transporters: An update. Molecular Membrane Biology 18, 1320.CrossRefGoogle Scholar
Lukasiewicz, P.D. (2005). Synaptic mechanisms that shape visual signaling at the inner retina. Progress in Brain Research 147, 205218.CrossRefGoogle Scholar
Maple, B.R. & Wu, S.M. (1998). Glycinergic synaptic inputs to bipolar cells in the salamander retina. The Journal of Physiology 506 (Pt. 3), 731744.Google Scholar
Martinez-Maza, R., Poyatos, I., Lopez-Corcuera, B., Unez, N., Gimenez, C., Zafra, F. & Aragon, C. (2001). The role of N-glycosylation in transport to the plasma membrane and sorting of the neuronal glycine transporter GLYT2. Journal of Biological Chemistry 276, 21682173.CrossRefGoogle Scholar
Miller, R.F. & Dacheux, R.F. (1983). Intracellular chloride in retinal neurons: Measurement and meaning. Vision Research 23, 399411.CrossRefGoogle Scholar
Morrow, J.A., Collie, I.T., Dunbar, D.R., Walker, G.B., Shahid, M. & Hill, D.R. (1998). Molecular cloning and functional expression of the human glycine transporter GlyT2 and chromosomal localisation of the gene in the human genome. FEBS Letters 439, 334340.CrossRefGoogle Scholar
Nakashima, T., Tomi, M., Tachikawa, M., Watanabe, M., Terasaki, T. & Hosoya, K. (2005). Evidence for creatine biosynthesis in Müller Glia. Glia 52, 4752.CrossRefGoogle Scholar
Newman, E. & Reichenbach, A. (1996). The Muller cell: A functional element of the retina. Trends in Neurosciences 19, 307312.CrossRefGoogle Scholar
Nunez, E. & Aragon, C. (1994). Structural analysis and functional role of the carbohydrate component of glycine transporter. The Journal of Biological Chemistry 269, 1692016924.Google Scholar
O'Brien, B.J., Richardson, R.C. & Berson, D.M. (2003). Inhibitory network properties shaping the light evoked responses of cat alpha retinal ganglion cells. Visual Neuroscience 20, 351361.CrossRefGoogle Scholar
Olivares, L., Aragon, C., Gimenez, C. & Zafra, F. (1994). Carboxyl terminus of the glycine transporter GLYT1 is necessary for correct processing of the protein. The Journal of Biological Chemistry 269, 2840028404.Google Scholar
Olivares, L., Aragon, C., Gimenez, C. & Zafra, F. (1995). The role of N-glycosylation in the targeting and activity of the GLYT1 glycine transporter. The Journal of Biological Chemistry 270, 94379442.CrossRefGoogle Scholar
Olivares, L., Aragon, C., Gimenez, C. & Zafra, F. (1997). Analysis of the transmembrane topology of the glycine transporter GLYT1. The Journal of Biological Chemistry 272, 12111217.CrossRefGoogle Scholar
Perez-Leon, J.A., Lopez-Vera, E. & Salceda, R. (2004). Pharmacological properties of glycine transport in the frog retina. Neurochemical Research 29, 313318.CrossRefGoogle Scholar
Pow, D.V. (1998). Transport is the primary determinant of glycine content in retinal neurons. Journal of Neurochemistry 70, 26282636.Google Scholar
Pow, D.V. & Hendrickson, A.E. (1999). Distribution of the glycine transporter glyt-1 in mammalian and nonmammalian retinae. Visual Neuroscience 16, 231239.Google Scholar
Pow, D.V. & Hendrickson, A.E. (2000). Expression of glycine and the glycine transporter glyt-1 in the developing rat retina. Visual Neuroscience 17, 19.Google Scholar
Poyatos, I., Ponce, J., Aragon, C., Gimenez, C. & Zafra, F. (1997). The glycine transporter GLYT2 is a reliable marker for glycine-immunoreactive neurons. Brain Research. Molecular Brain Research 49, 6370.CrossRefGoogle Scholar
Pourch, R.G., Goebel, D.J. & McReynolds, J.S. (1984). Autoradiographic studies of [3H]-glycine, [3H]-GABA, and [3H]-muscimol uptake in the mudpuppy retina. Experimental Eye Research 39, 6981.CrossRefGoogle Scholar
Salceda, R. (2006). Pharmacological properties of glycine uptake in the developing rat retina. Neurochemistry International 49, 342346CrossRefGoogle Scholar
Sato, K., Yoshida, S., Fujiwara, K., Tada, K. & Tohyama, M. (1991). Glycine cleavage system in astrocytes. Brain Research 567, 6470.CrossRefGoogle Scholar
Shen, W. (2005). Repetitive light stimulation inducing glycine receptor plasticity in the retinal neurons. Journal of Neurophysiology 94, 22312238.CrossRefGoogle Scholar
Smiley, J.F. & Yazulla, S. (1990). Glycinergic contacts in the outer plexiform layer of the Xenopus laevis retina characterized by antibodies to glycine, GABA and glycine receptors. The Journal of Comparative Neurology 299, 375388.CrossRefGoogle Scholar
Smith, K.E., Borden, L.A., Hartig, P.R., Branchek, T. & Weinshank, R.L. (1992). Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors. Neuron 8, 927935.CrossRefGoogle Scholar
Stockton, R.A. & Slaughter, M.M. (1991). Depolarizing actions of GABA and glycine on amphibian retinal horizontal cells. Journal of Neurophysiology 65, 680692.CrossRefGoogle Scholar
Vitanova, L., Haverkamp, S. & Wassle, H. (2004). Immunocytochemical localization of glycine and glycine receptors in the retina of the frog Rana ridibunda. Cell and Tissue Research 317, 227235.Google Scholar
Voaden, M.J., Marshall, J. & Murani, N. (1974). The uptake of [3H]gamma-amino butyric acid and [3H]glycine by the isolated retina of the frog. Brain Research 67, 115132.CrossRefGoogle Scholar
Watt, C.B. & Florack, V.J. (1993). Colocalization of glycine in substance P-amacrine cells of the larval tiger salamander retina. Visual Neuroscience 10, 899906.CrossRefGoogle Scholar
Yang, C.Y. & Yazulla, S. (1988). Light microscopic localization of putative glycinergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 272, 343357.CrossRefGoogle Scholar
Zafra, F., Aragon, C., Olivares, L., Danbolt, N.C., Gimenez, C. & Storm-Mathisen, J. (1995a). Glycine transporters are differentially expressed among CNS cells. Journal of Neuroscience 15, 39523969.Google Scholar
Zafra, F., Gomeza, J., Olivares, L., Aragon, C. & Gimenez, C. (1995b). Regional distribution and developmental variation of the glycine transporters GLYT1 and GLYT2 in the rat CNS. European Journal of Neuroscience 7, 13421352.Google Scholar
Zafra, F., Poyatos, I. & Gimenez, C. (1997). Neuronal dependency of the glycine transporter GLYT1 expression in glial cells. Glia 20, 155162.3.0.CO;2-8>CrossRefGoogle Scholar
Zhang, J. & Wu, S.M. (2003). G labels ON bipolar cells in the tiger salamander retina. The Journal of Comparative Neurology 461, 276289.CrossRefGoogle Scholar