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Displaced starburst amacrine cells of the rabbit retina contain the 67-kDa isoform, but not the 65-kDa isoform, of glutamate decarboxylase

Published online by Cambridge University Press:  02 June 2009

Christopher Brandon  and
Mark H. Criswell
Christopher Brandon
Affiliation:
Department of Cell Biology and Anatomy, The Chicago Medical School, North Chicago
Mark H. Criswell
Affiliation:
Department of Cell Biology and Anatomy, The Chicago Medical School, North Chicago
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Abstract

The cholinergic identity of retinal starburst amacrine neurons is well established, but recent evidence suggests that these cells are GABAergic as well. Confirmation of this dual transmitter function requires the demonstration of glutamate decarboxylase (GAD), the biosynthetic enzyme for GABA, within starburst cells. The current work was undertaken to determine whether rabbit retinal starburst amacrine neurons contain either of the two known isoforms of GAD. To do this, we have examined the localization of the following: (1) the 65-kDa isoform of GAD; (2) the 67-kDa isoform of GAD; (3) choline acetyltransferase; and (4) the fluorescent dye DAPI, a marker for cholinergic amacrine cells. In addition, we labeled displaced starburst neurons directly, by injecting them with Lucifer Yellow in vitro. Four strata within the inner plexiform layer contained immunoreactive GAD65. A non-GAD65-immunoreactive zone separated the two innermost strata (G3 and G4); this zone contained (1) the dendrites of individual Lucifer Yellow-injected, displaced starburst amacrine cells; (2) dendrites immunoreactive for choline acetyltransferase; and (3) processes of DAPI-labeled amacrine cells. Immunoreactive GAD67 appeared in the same strata that contained GAD65, and in at least two additional strata, one of which lay at precisely the same depth as the proximal cholinergic stratum. In addition, the somas of displaced starburst cells were strongly immunoreactive for GAD67, but not for GAD65. These results demonstrate (1) that displaced starburst amacrine cells contain the 67-kDa isoform of GAD, but not the 65-kDa isoform; and (2) that the dendrites of starburst (67-kDa GAD) amacrines, and the dendrites of 65-kDa-GAD-containing amacrines, occupy different strata within the inner plexiform layer. Thus, displaced starburst cells do contain GAD, and can, presumably, manufacture GABA. The reasons for their preferential use of the 67-kDa GAD isoform remain to be elucidated.

Keywords

Cholinergic neuronsGABAImmunocytochemistry
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 6 , November 1995 , pp. 1053 - 1061
Copyright
Copyright © Cambridge University Press 1995

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References

Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.Google Scholar
Ames, A. III. & Pollen, D.A. (1969). Neurotransmission in central nervous tissue: A study of isolated rabbit retina. Journal of Neurophysiology 32, 424–442.Google Scholar
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of direction-ally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.Google Scholar
Barlow, H.B. & Levick, W.R. (1965). The mechanism of direction-ally selective units in rabbit≈s retina. Journal of Physiology 178, 477–504.Google Scholar
Brandon, C. (1985 a). Improved immunocytochemical staining through the use of primary Fab fragments, Fab-specific second antibody, and FabHRP. Journal of Histochemistry and Cytochemistry 33, 715–719.Google Scholar
Brandon, C. (1985 b). Retinal GABA neurons: Localization in vertebrates species using an antiserum to rabbit brain glutamate decarboxylase. Brain Research 344, 286–295.CrossRefGoogle ScholarPubMed
Brandon, C. (1986). Purification of L-glutamate decarboxylase from rabbit brain and preparation of a monospecific antiserum. Journal of Neuroscience Research 15, 367–381.Google Scholar
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Immunocytochemical localization, and relationship to GABAergic and cholinesterase-containing neurons. Brain Research 401, 385–391.Google Scholar
Brandon, C. (1991). Cholinergic amacrine neurons of the dogfish retina. Visual Neuroscience 6, 553–562.Google Scholar
Brecha, N., Johnson, D., Peichl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyric acid immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 6187–6191.Google Scholar
Caldwell, J.H., Daw, N.W. & Wyatt, H.J. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: Lateral interactions for cells with more complex receptive fields. Journal of Physiology 276, 277–298.Google Scholar
Chang, Y.-C. & Gottleib, D.I. (1988). Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. Journal of Neuroscience 8, 2123–2130.Google Scholar
Erlander, M.G. & Tobin, A.J. (1991). The structural and functional heterogeneity of glutamic acid decarboxylase: A review. Neurochemical Research 16, 215–226.Google Scholar
Erlander, M.G., Tillakaratne, N.J.K., Feldblum, S., Patel, N. & Tobin, A.J. (1991). Two genes encode distinct glutamate decarboxylases. Neuron 7, 91–100.Google Scholar
Esclapez, M., Tillakaratne, N.J.K., Kaufman, D.L., Tobin, A.J. & Houser, C.R. (1994). Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. Journal of Neuroscience 14, 1834–1855.Google Scholar
Johnson, C.D. & Epstein, M.L. (1986). Monoclonal antibodies and polyvalent antiserum to chicken choline acetyltransferase. Journal of Neurochemistry 46, 968–976.Google Scholar
Kaufman, D.L., Houser, C.R. & Tobin, A.J. (1991). Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. Journal of Neurochemistry 56, 720–723.Google Scholar
Kosaka, T., Tauchi, M. & Dahl, J.L. (1988). Cholinergic neurons containing GABA-like and/or glutamate decarboxylase-like immuno-reactivities in various brain regions of the rat. Experimental Brain Research 70, 605–617.Google Scholar
Ma, W., Behar, T. & Barker, J. (1992). Transient expression of GABA immunoreactivity in the developing rat spinal cord. Journal of Comparative Neurology 325, 271–290.Google Scholar
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984). Acetylcholine-synthesizing amacrine cells: Identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society B (London) 223, 79–100.Google Scholar
Massey, S.C., Blankenship, K. & Mills, S.L. (1991). Cholinergic amacrine cells in the rabbit retina accumulate muscimol. Visual Neuroscience 6, 113–117.Google Scholar
Messersmith, E.K. & Redburn, D.A. (1992). Gamma-aminobutyric acid immunoreactivity in multiple cell types of the developing rabbit retina. Visual Neuroscience 8, 201–211.Google Scholar
Messersmith, E.K. & Redburn, D.A. (1993). The role of GABA during development of the outer retina in the rabbit. Neurochemical Research 18, 463–470.Google Scholar
Mosinger, J. & Yazulla, S. (1985). Co-localization of GAD-like immunoreactivity and 3H-GABA uptake in amacrine cells of rabbit retina. Journal of Comparative Neurology 240, 396–406.Google Scholar
Mosinger, J. & Yazulla, S. (1987). Double-label analysis of GAD- and GABA-like immunoreactivity in the rabbit retina. Vision Research 27, 23–30.CrossRefGoogle Scholar
O≈Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the U.S.A. 86, 3414–3418.CrossRefGoogle ScholarPubMed
Slemmon, J.R., Salvaterra, P.M. & Saito, K. (1980). Preparation and characterization of peroxidase:antiperoxidase-Fab complex. Journal of Histochemistry and Cytochemistry 28, 10–18.Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–119.Google Scholar
Vaney, D.I., Peichl, L. & Boycott, B.B. (1981). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers in the rabbit retina. Journal of Comparative Neurology 199, 373–391.Google Scholar
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society B (London) 220, 501–508.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.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 1–46.Google Scholar
Vardi, N., Kaufman, D.L. & Sterling, P. (1994). Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase. Visual Neuroscience 11, 135–142.Google Scholar
Whitlon, D.S. & Sobkowicz, H.M. (1989). GABA-like immunoreactivity in the cochlea of the developing mouse. Journal of Neuro-cytology 18, 505–518.Google Scholar