Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-18T23:11:52.011Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurochemical signatures revealed by glutamine labeling in the chicken retina

Published online by Cambridge University Press:  02 June 2009

Michael Kalloniatis ,
Guido Tomisich  and
Robert E. Marc
Michael Kalloniatis
Affiliation:
Department of Optometry, University of Melbourne, Parkville, Victoria, 3052, Australia
Guido Tomisich
Affiliation:
Department of Optometry, University of Melbourne, Parkville, Victoria, 3052, Australia
Robert E. Marc
Affiliation:
University of Utah, Health Sciences Center, 50 North Medical Drive, Salt Lake City
Get access Rights & Permissions [Opens in a new window]

Abstract

Postembedding immunocytochemistry was used to determine the retinal distribution of the amino acid glutamine, and characterize amino acid signatures in the avian retinal ganglion cell layer. Glutamine is a potential precursor of glutamate and some glutamatergic neurons may use this amino acid to sustain production of glutamate for neurotransmission. Ganglion cells, cells in the inner nuclear layer, and some photoreceptors exhibited glutamine immunoreactivity of varying intensity. Ganglion cells demonstrated the highest level of immunoreactivity which indicates either slow glutamine turnover or active maintenance of a large standing glutamine pool relative to other glutamatergic neurons. Müller's cells in the avian retina are involved in glutamate uptake and carbon recycling by the rapid conversion of glutamate to glutamine, thus explaining the low glutamate and high glutamine immunoreactivity found throughout Müller's cells. Most chicken retinal ganglion cells are glutamate (E) and glutamine (Q) immunoreactive but display diverse signatures with presumed functional subsets of cells displaying admixtures of E and Q with GABA (7) and/or glycine (G). The four major ganglion cell signatures are (1) EQ; (2) EQγ; (3) EQG; and (4) EQγG.

Keywords

GlutamineGlutamateGABAGlycineAmino acidsNeurotransmittersVision
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 4 , July 1994 , pp. 793 - 804
Copyright
Copyright © Cambridge University Press 1994

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

Agardh, E., Bruun, A., Ehinger, B., Ekstrom, P., van Veen, T. & Wu, J.-Y. (1987). Gamma-aminobutyric acid- and glutamic acid decarboxylase-immunoreactive neurons in the retina of different vertebrates. Journal of Comparative Neurology 258, 622–630.Google Scholar
Akiyama, H., Kaneko, T., Mizuno, N. & McGeer, P.L. (1990). Distribution of phosphate-activated glutaminase in the human cerebral cortex. Journal of Comparative Neurology 297, 239–252.Google Scholar
Aoki, C, Kaneko, T., Starr, A. & Pickel, V.M. (1991). Identification of mitochondrial and non-mitochondrial glutaminase within select neurons and glia of rat forebrain by electron microscopy. Journal of Neuroscience Research 28, 531–548.CrossRefGoogle Scholar
Ball, A. (1987). Immunocytochemical and autoradiographic localization of GABAergic neurons in the goldfish retina. Journal of Comparative Neurology 255, 317–325.Google Scholar
Bender, D.A. (1985). Amino acid metabolism. Chichester: John Wiley & Sons.Google Scholar
Bradford, H.F., Ward, H.K. & Thomas, A.J (1978). Glutamate as a substrate for nerve endings. Journal of Neurochemistry 30, 1453–1459.Google Scholar
Brecha, N.C., Johnson, D., Piechl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and γ-aminobutyric acid immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6187–6191.Google Scholar
Brttto, L.R.G., Hamassaki, D.E., Keyser, K.T. & Karten, H.J. (1989). Neurotransmitters, receptors, and neuropeptides in the accessory optic system: An immunohistochemical survey in the pigeon (Columba livia). Visual Neuroscience 3, 463–475.Google Scholar
Caruso, D.A., Owczarzak, M.T., Goebel, D.J., Hazlett, J.C. & Pourcho, R.G. (1989). GABA-immunoreactivity in ganglion cells of the rat retina. Brain Research 476, 129–134.Google Scholar
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells of the primate retina. Visual Neuroscience 9, 279–290.Google Scholar
Davanger, S., Ottersen, O.P. & Storm-Matheson, J. (1991). Glutamate, GABA, and glycine in the human retina: An immunocytochemical investigation. Journal of Comparative Neurology 311, 483–494.Google Scholar
Deroniche, A. & Frotscher, M. (1991). Astroglial processes around identified glutamatergic synapses contain glutamine synthetase: Evidence for transmitter degradation. Brain Research 552, 346–350.Google Scholar
Drejer, J., Larsson, O.M. & Schousboe, A. (1982). Characterization of L–glutamate uptake into and release from astrocytes and neurons cultured from different brain regions. Experimental Brain Research 47, 257–269.Google Scholar
Ehinger, B. (1977). Glial and neuronal uptake of GABA, glutamic acid, glutamine and glutathione in the rabbit retina. Experimental Eye Research 25, 221–234.CrossRefGoogle ScholarPubMed
Ehinger, B. (1989). Glutamate as a retinal neurotransmitter. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 1–14. Berlin: Springer-Verlag.Google Scholar
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. & Dowling, J.E. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 8321–8325.Google Scholar
Fite, K.V., Brecha, N., Karten, H.J. & Hunt, S.P. (1981). Displaced ganglion cells and the accessory optic system of pigeon. Journal of Comparative Neurology 195, 279–288.Google Scholar
Fletcher, E.L. & Kalloniatis, M. (1994). Neuronal and neurochemical architecture of the rat retina. Investigative Ophthalmology and Visual Science (Suppl.), 35, 1908.Google Scholar
Gebhard, R. (1992). Histochemical demonstration of glutamate dehydrogenase and phosphate-activated glutaminase activities in semithin sections of the rat retina. Histochemistry 97, 101–103.Google Scholar
Hamberger, A., Chiang, G., Nylen, E.S., Scheff, S.W. & Cotman, C.W. (1978). Stimulus evoked increase in the biosynthesis of the putative neurotransmitter glutamate in the hippocampus. Brain Research 143, 549–555.Google Scholar
Hampton, C.K. & Redburn, D.A. (1983). Autoradiographic analysis of 3H-glutamate, 3H-dopamine and 3H-GABA accumulation in rabbit retina after kainic acid treatment. Journal of Neuroscience Research 9, 239–251.Google Scholar
Hayes, B.P. & Holden, A.L. (1980). Size classes of ganglion cells in the central yellow field of the pigeon retina. Experimental Brain Research 39, 269–275.Google Scholar
Hayes, B.P. (1982). The structural organization of the pigeon retina. In Progress in Retinal Research, Vol. 1, ed. Osborne, N.N. & Chader, G.J., pp. 197–226. Oxford: Pergamon Press.Google Scholar
Hertz, L. (1979). Functional interactions between neurons and astrocytes, I. Turn over and metabolism of putative amino acid transmitters. Progress in Neurobiology 13, 277–323.Google Scholar
Hunt, S.P., Streit, P., Künzle, H. & Cuénod, M. (1977). Characterization of the pigeon isthmo-tectal pathway by selective uptake and retrograde movement of radioactive compounds and by Golgilike horseradish peroxide labelling. Brain Research 129, 197–212.Google Scholar
Hurd, L.B. II & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 9–20.CrossRefGoogle ScholarPubMed
Iversen, L.L. (1984). Amino acids and peptides: fast and slow chemical signals in the nervous system? Proceedings of the Royal Society B (London) 221, 245–260.Google Scholar
Kalloniatis, M. & Fletcher, E.L. (1993). Immunocytochemical localization of the amino acid neurotransmitters in the chicken retina. Journal of Comparative Neurology 336, 174–193.Google Scholar
Kalloniatis, M. & Marc, R.E. (1990). Interplexiform cells of the goldfish retina. Journal of Comparative Neurology 297, 340–358.Google Scholar
Kalloniatis, M. & Marc, R.E. (1992). Glutamate, GABA and glycine immunoreactivity in the macaque monkey retina. Society for Neuroscience Abstracts 18, 393.Google Scholar
Kalloniatis, M., Marc, R.E., Tomisich, G. & Barnes, G. (1994). Pathways of glutamate production in the mammalian retina. Investigative Ophthalmology and Visual Science (Suppl.), 35, 1908.Google Scholar
Karten, H.J., Fite, K.V. & Brecha, N. (1977). Specific projection of displaced retinal ganglion cells upon the accessory optic system in the pigeon (Columba livia). Proceedings of the National Academy of Sciences of the U.S.A. 74, 1753–1756.Google Scholar
Keyser, K.T., Britto, L.R.G., Woo, J.-I., Park, D.H., Joh, T.H. & Karten, H.J. (1990). Presumptive catecholinergic ganglion cells in the pigeon retina. Visual Neuroscience 4, 225–236.Google Scholar
Kvamme, E., Torgner, I.AA. & Svenneby, G. (1985). Glutaminase from mammalian tissues. Methods in Enzymology 113, 241–256.CrossRefGoogle ScholarPubMed
Lam, D.M.-K. (1988). Coexistence and co-function of neuroactive substances in the central nervous system: A view from the vertebrate retina. In Proceedings of the Retina Research Foundation Symposium, Vol. I, ed. Lam, D.M.-K., pp. 182–197. The Woodlands, Texas: Portfolio Publishing Co., Inc.Google Scholar
Lam, D.M.-K., Li, H.-B., Su, Y.-Y.T. & Watt, C.B. (1985). The signature hypothesis: Co-localizations of neuroactive substances as anatomical probes for circuitry analyses. Vision Research 25, 1353–1364.Google Scholar
Lam, D.M.K., Su, Y.Y.T., Swain, L., Marc, R.E., Brandon, C. & Wu, J.-Y. (1979). Immunocytochemical localization of L–glutamic decarboxylase in the goldfish retina. Nature 278, 565–567.Google Scholar
Lewis, G.P., Erickson, P.A., Kaska, D.B. & Fisher, S.K. (1988). Immunocytochemical comparison of Muller cells and astrocytes in the cat retina. Experimental Eye Research 47, 839–853.Google Scholar
Li, H.B., Watt, C.B. & Lam, D.M.-K. (1990). Double-label analyses of somatostatin’s coexistence with enkephalin and gamma-aminobutyric acid in amacrine cells of the chicken retina. Brain Research 525, 304–309.Google Scholar
Lugo-García, N. & Blanco, R.E. (1991). Localization of GAD- and GABA-like immunoreactivity in ground squirrel retina: Retrograde labeling demonstrates GAD-positive ganglion cells. Brain Research 564, 19–26.Google Scholar
Marc, R.E. (1985). The role of glycine in retinal circuitry. In Retinal Transmitters and Modulators: Models for the Brain, Vol. I, ed. Morgan, W.W., pp. 119–158. Boca Raton, Florida: CRC Press.Google Scholar
Marc, R.E. (1989 a). The role of glycine in the mammalian retina. In Progress in Retinal Research, Vol 8, ed. Osborne, N.N., & Chader, G.J., pp. 67–107. Oxford: Pergamon Press.Google Scholar
Marc, R.E. (1989 b). The anatomy of multiple GABAergic and glycinergic pathways in the inner plexiform layer of the goldfish retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 53–64. Berlin: Springer-Verlag.Google Scholar
Marc, R.E. (1992). Structural organization of GABAergic circuitry in ectotherm retina. In GABA in the Retina and Central Visual Pathways, ed. Mize, R.R., Marc, R.E. & Sillito, A.M., pp. 61–92. Amsterdam: Elsevier.Google Scholar
Marc, R.E. & Basinger, S.F. (1991). Glutamate, glutamine, aspartate, GABA and taurine levels in neurons, glia and vascular cells of the goldfish retina. Investigative Ophthalmology Visual Science (Suppl.) 32, 1188.Google Scholar
Marc, R.E., Li, H.-B., Kalloniatis, M. & Arnold, J. (1993). Cholinergic subsets of GABAergic amacrine cells in the goldfish retina. Investigative Ophthalmology Visual Science (Suppl.) 34, 1061.Google Scholar
Marc, R.E., Liu, W.-L., Kalloniatis, M., Raiguel, S.F. & Van Haesendonck, E. (1990). Patterns of glutamate immunoreactivity in the goldfish retina. Journal of Neuroscience 10, 4006–4034.Google Scholar
Marshall, J. & Voaden, M.J. (1974 a). An investigation of the cells incorporating [3H] GABA and [3H] glycine in the isolated retina of the rat. Experimental Eye Research 18, 367–370.Google Scholar
Marshall, J. & Voaden, M.J. (1974 b). An autoradiographic study of the cells accumulating 3H γ-aminobutyric acid in the isolated retinas of pigeons and chickens. Investigative Ophthalmology and Visual Science 13, 602–607.Google Scholar
Masland, R.H., Cassidy, C. & O'Malley, D.M. (1989). The release of acetylcholine and GABA by neurons of the rabbit retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 15–26. Berlin: Springer-Verlag.Google Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N. N. & Chader, G. J., pp. 399–425. Oxford: Pergamon Press.Google Scholar
Millar, T. J., Ishimoto, I., Chubb, I. W., Epstein, M.L., Johnston, C. D. & Morgan, I. G. (1987). Cholinergic amacrine cells of the chicken retina: A light- and electron-microscope immunocytochemical study. Neuroscience 21, 725–743.Google Scholar
Mize, R.R., Marc, R.E. & Sillito, A.M. (1992). GABA in the Retina and Central Visual Pathways. Amsterdam: Elsevier.Google Scholar
Montero, V. M. & Wenthold, R. J. (1989). Quantitative immunogold analysis reveals high glutamate levels in retinal and cortical synaptic terminals in the lateral geniculate nucleus of the macaque. Neuroscience 31, 639–647.Google Scholar
Moscona, A.A. (1983). On glutamine synthetase, carbonic anhydrase and Muller glia in the retina. In Progress in Retinal Research, Vol. 2, ed. Osborne, N.N. & Chader, G.J., pp. 111–135. Oxford: Pergamon Press.Google Scholar
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931–944.Google Scholar
Perry, V.H. (1982). The ganglion cell layer of the mammalian retina. In Progress in Retinal Research, Vol. I, ed. Osborne, N.N. & Chader, G.J., pp. 53–80. Oxford: Pergamon Press.Google Scholar
Perry, V.H. & Walker, M. (1980). Amacrine cells displaced amacrine cells and interplexiform cells in the retina of the rat. Proceedings of the Royal Society B 208, 415–431.Google Scholar
Prada, F.A., Quesada, A. & Genis-Galvez, J.M. (1989). Short axon ganglion cells in the chick retina. Experientia 45, 92–94.Google Scholar
Reiner, A., Brecha, N. & Karten, H.J. (1979). A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4, 1679–1688.Google Scholar
Ribak, C.E., Vaughn, J.E. & Roberts, E. (1980). GABAergic nerve terminals decrease in the substantia nigra following hemitransections of the striatonigral and pallidonigral pathway. Brain Research 192, 413–420.Google Scholar
Robin, L. N. & Kalloniatis, M. (1992). Interrelationship between retinal ischaemic damage and turnover and metabolism of putative amino acid neurotransmitters, glutamate and GABA. Documenta Ophthalmologica 80, 273–300.Google Scholar
Sarthy, P.V., Hendrickson, A.E. & Wu, J.Y. (1986). L–glutamate: A neurotransmitter candidate for cone photoreceptors in the monkey retina. Journal of Neuroscience 6, 637–643.Google Scholar
Sherry, D.M. & Ulshafer, R.J. (1992 a). Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of Anolis carolinensis, I: Gamma-amino butyric acid. Visual Neuroscience 8, 515–529.Google Scholar
Sherry, D.M. & Ulshafer, R.J. (1992 b). Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of A nolis carolinensis, II: Glutamate and aspartate. Visual Neuroscience 9, 313–323.Google Scholar
Smith, Y. & Bolam, J.P. (1989). Neurons of the substantia nigra reticulata receive a dense GABA-containing input from the globus pallidus in the rat. Brain Research 493, 160–167.Google Scholar
Stell, W.K. (1985). Putative peptide transmitters, amacrine cell diversity and function in the inner plexiform layer. In Neurocircuitry of the Retina: A Cajal Memorial, ed. Gallego, A. & Gouras, P., pp. 171–187. New York: Elsevier.Google Scholar
Vaney, D.I. (1985). The morphology and topographic distribution of An amacrine cells in the cat retina. Proceedings of the Royal Society B 224, 475–488.Google Scholar
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187–190.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.Google Scholar
Van Regenmortel, M.H.V., Briand, J.P., Muller, S. & Plaué, S. (1988). Synthetic peptides as antigens. In Laboratory Techniques in Biochemistry and Molecular Biology, Vol. 19, ed. Burdon, R.H. & van Knippenburg, P.H., pp. 95–130. Amsterdam: Elsevier.Google Scholar
Vaughn, J.E., Famiglietti, E.V. Jr, Barber, R.P., Saito, K., Roberts, E. & Ribak, C. (1981). GABAergic amacrine cells in rat retina: Immunocytochemical identification and synaptic connectivity. Journal of Comparative Neurology 197, 113–127.Google Scholar
Voaden, M.J. (1976). Gamma-aminobutyric acid and glycine as retinal neurotransmitters. In Transmitters in the Visual Process, ed. Bonting, S.L., pp, 107–125. Oxford: Pergamon Press.Google Scholar
Voaden, M.J. (1978). The localization and metabolism of neuroactive amino acids in the retina. In Amino Acids as Chemical Transmitters, ed. Fonnum, F., pp. 257–274New York: Plenum Press.Google Scholar
Watt, C.B., Li, H.-B. & Lam, D.M.-K. (1985). The presence of three neuroactive peptides in putative glycinergic amacrine cells of an avian retina. Journal of Comparative Neurology 348, 187–191.Google Scholar
Watt, C.B. & Su, Y.-Y.T. (1988). Enkephalinergic pathways in the retina. In Proceedings of the Retina Research Foundation Symposium, Vol. I, ed. Lam, D.M.-K., pp. 141–162. The Woodlands, Texas: Portfolio Publishing Co., Inc.Google Scholar
Wulle, I. & Wagner, H.-J. (1990). GABA and tyrosine hydroxylase immunocytochemistry reveal different patterns of colocalization in retinal neurons of various vertebrates. Journal of Comparative Neurology 296, 173–178.Google Scholar
Würdig, S. & Kugler, P. (1991). Histochemistry of glutamate metabolizing enzymes in the rat cerebellar cortex. Neuroscience Letters 130, 165–168.CrossRefGoogle ScholarPubMed
Yang, G., Millar, T.J. & Morgan, I.G. (1989). Co-lamination of cholinergic amacrine cell and displaced ganglion cell dendrites in the chicken retina. Neuroscience Letters 103, 151–156.Google Scholar
Yazulla, S. (1986). GABAergic mechanisms in the retina. In Progress in Retinal Research, Vol. 5, ed. Osborne, N.N. & Chader, G.J., pp. 1–51. Oxford: Pergamon Press.Google Scholar
Yazulla, S. & Brecha, N. (1980). Binding and uptake of the GABA analogue 3H-muscimol, in the retinas of goldfish and chicken. Investigative Ophthalmology and Visual Science 19, 1415–1426.Google Scholar
Yazulla, S. & Yang, C.-Y. (1988). Colocalization of GABA and glycine immunoreactivities in a subset of retinal neurons in tiger salamander. Neuroscience Letters 95, 37–41.Google Scholar
Yu, D.C.-Y., Watt, C.B., Lam, D.M.K. & Fry, K.R. (1988). GABAergic ganglion cells in the rabbit retina. Brain Research 439, 376–382.Google Scholar