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Immunocytochemical localization of GABA, GABAA receptors, and synapse-associated proteins in the developing and adult ferret retina

Published online by Cambridge University Press:  02 June 2009

A. Karne ,
D. M. Oakley ,
G. K. Wong  and
R. O. L. Wong
A. Karne
Affiliation:
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis
D. M. Oakley
Affiliation:
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis
G. K. Wong
Affiliation:
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis
R. O. L. Wong
Affiliation:
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis
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Abstract

Gamma-aminobutyric acid (GABA) modulates the pattern of correlated spontaneous bursting activity between amacrine cells and ganglion cells of the ferret retina during the first postnatal month. Here, we demonstrate the presence of an anatomical network which may underlie these interactions throughout the period when correlated bursting activity is observed, by immunolabelling the neonatal ferret retina for GABA, GABAA receptors, and synapse-associated proteins. GABA immunoreactivity was detected in cell somata in the ganglion cell layer (GCL), in amacrine cells, and in the inner plexiform layer (IPL) by embryonic day 38. This pattern remained largely unchanged throughout neonatal development and in the adult. By contrast to other mammals, the outer plexiform layer (OPL) was only very weakly labelled for GABA, at all ages studied. Strong, punctate, immunolabelling for the β2/3 subunit of the GABAA receptor was apparent in the IPL by birth, and appeared in the OPL by the second postnatal week. The possibility that synaptic interactions in the IPL occur during bursting activity was examined by immunolabelling for synapse-associated proteins. Strong immunoreactivity for synaptic vesicle proteins, Synapsin I and II, and synaptic vesicle-2 (SV2), a synaptic vesicle transporter protein, was observed in the IPL by birth. Immunoreactivity for SNAP-25, a protein associated with vesicle fusion, was also intense at the level of the IPL and in the nerve fiber layer of the retina at birth. Taken together, these patterns of immunoreactivity suggest the presence of a GABAergic network in the IPL of the ferret retina by birth, coinciding with the appearance of correlated bursting activity in the inner retina.

Keywords

GABA and GABAA receptorsSynapsinSV2SNAP-25Retinal development
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 6 , November 1997 , pp. 1097 - 1108
Copyright
Copyright © Cambridge University Press 1997

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References

Blanco, R., Vaquero, C.F. & de la Villa, P. (1996). The effects of GABA and glycine on horizontal cells of the rabbit retina. Vision Research 36, 3987–3995.Google Scholar
Buckley, K. & Kelly, R.B. (1985). Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. Journal of Cell Biology 100, 1284–1294.Google Scholar
Catsicas, S., Larhammar, D., Blomqvist, A., Sanna, P.P., Milner, R.J. & Wilson, M.C. (1991). Expression of a conserved cell-type specific protein in nerve terminals coincides with synaptogenesis. Proceedings of the National Academy of Sciences of the U.S.A. 88, 785–789.CrossRefGoogle ScholarPubMed
Catsicas, S., Catsicas, M., Keyser, K.T., Karten, H.J., Wilson, M.C. & Milner, R.J. (1992). Differential expression of the presynaptic protein SNAP-25 in mammalian retina. Journal of Neuroscience Research 33, 1–9.Google Scholar
Czernick, A.J., Mathers, A.J., Tsou, K., Greengard, P. & Mische, S.M. (1995). Phosphorylation state-specific antibodies: Preparation and applications. Neuroprotocols 6, 56–61.Google Scholar
Feller, M.B., Wellis, D.P., Stellwagen, D., Werblin, F.S. & Shatz, C.J. (1996). Requirement for cholinergic transmission in the propagation of spontaneous retinal waves. Science 272, 1182–1186.Google Scholar
Fischer, K., Lukasiewicz, P.D. & Wong, R.O.L. (1997). Age-dependent modulation of retinal ganglion cell bursting activity by GABA (submitted).CrossRefGoogle Scholar
Fletcher, T.L., Cameron, P., De Camilli, P. & Banker, G. (1991). The distribution of Synapsin I and Synaptophysin in hippocampal neurons developing in culture. Journal of Neuroscience 11, 1617–1626.Google Scholar
Greferath, U., Müller, F., Wässle, H., Shivers, B. & Seeburg, P. (1993). Localization of GABA receptors in the rat retina. Visual Neuroscience 10, 551–561.CrossRefGoogle ScholarPubMed
Greferath, U., Grünert, U., Müller, F. & Wässle, H. (1994). Localization of GABAA receptors in the rabbit retina. Cell and Tissue Reseach 276. 295–307.Google Scholar
Greferath, U., Grünert, U., Fritschy, J.M., Stephenson, A., Möhler, H. & Wässle, H. (1995). GABAA receptor subunits have differential distributions in the rat retina: In situ hybridization and immunohistochemistry. Journal of Comparative Neurology 353, 553–571.CrossRefGoogle ScholarPubMed
Greiner, J.V. & Weidman, T.A. (1981). Histogenesis of the ferret retina. Experimental Eye Research 33, 315–332.Google Scholar
Grünert, U.Greferath, U., Boycott, B.B. & Wässle, H. (1993). Parasol (Pα) ganglion cells of the primate fovea: Immunocytochemical staining with antibodies against GABAA receptors. Vision Research 33, 1–14.CrossRefGoogle Scholar
Grünert, U. & Hughes, T.E. (1993). Immunohistochemical localization of GABAA receptor in scotopic pathway of the cat retina. Cell and Tisssue Resarch 274, 509–524.Google Scholar
Hass, C.A., DeGennaro, L.J., Müller, M. & Holländer, H. (1990). Synapsin I expression in the rat retina during postnatal development. Experimental Brain Research 82, 25–32.Google Scholar
Henderson, P.J.F. (1993). The 12-transmembrane helix transporters. Current Opinion in Cell Biology 5, 708–721.CrossRefGoogle ScholarPubMed
Hughes, T.E., Carey, R.G., Victoria, J., de Blas, A.L. & Karten, H.J. (1989). Immunohistochemical localization of GABAA receptors in the retina of the new world primate, Saimiri sciureus. Visual Neuroscience 2, 565–581.CrossRefGoogle ScholarPubMed
Hughes, T.E., Grünert, U. & Karten, H.J. (1991). GABAA receptors in the retina of the cat: An immunohistochemical study of wholemounts, sections and dissociated cells. Visual Neuroscience 6, 229–238.Google Scholar
Koontz, M.A. & Hendrickson, A.E. (1993). Comparison of immunolocalization patterns for the synaptic vesicle proteins p65 and Synapsin I in Macaque monkey retina. Synapse 14, 268–282.Google Scholar
Lam, D.M.-K., Fung, S.-C. & Kong, Y.-U. (1980). Postnatal development of GABAergic neurons in the rabbit retina. Journal of Comparative Neurology 193, 89–102.Google Scholar
Lukasiewicz, P.D. & Wong, R.O.L. (1997). GABAC receptors on ferret retinal bipolar cells; a diversity of subtypes in mammals? Visual Neuroscience 14, 989–994.Google Scholar
Mandell, J.W., Townes-Anderson, E., Czernik, A.J., Cameron, R., Greengard, P. & De Camilli, P. (1990). Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 5, 19–33.Google Scholar
Mandell, J.W., Czernik, A.J., Cameron, , De Camilli, P., Greengard, P. & Townes-Anderson, E. (1992). Differential expression of Synapsins I and II among rat retinal synapses. Journal of Neuroscience 12, 1736–1749.CrossRefGoogle ScholarPubMed
Maslim, J. & Stone, J. (1986). Synaptogenesis in the retina of the cat. Brain Research 373, 35–48.CrossRefGoogle ScholarPubMed
Meister, M., Wong, R.O.L., Baylor, D.A. & Shatz, C.J. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943.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
Nishimura, Y. & Rakic, P. (1985). Development of the Rhesus monkey retina: I. Emergence of the inner plexiform layer and its synapses. Journal of Comparative Neurology 241, 420–434.CrossRefGoogle ScholarPubMed
Nishimura, Y. & Rakic, P. (1987). Development of the Rhesus monkey retina: II. A three-dimensional analysis of the sequences of synaptic combinations in the inner plexiform layer. Journal of Comparative Neurology 262, 290–313.Google Scholar
Okada, M., Erickson, A. & Hendrickson, A. (1994). Light and electron microscopic analysis of synaptic development in Macaca monkey retina as detected by immunocytochemical labeling for synaptic vesicle protein, SV2. Journal of Comparative Neurology 339, 535–558.CrossRefGoogle ScholarPubMed
Osborne, N.N., Patel, S., Beaton, D.W. & Neuhoff, V. (1986). GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell and Tissue Research 243, 117–123.CrossRefGoogle ScholarPubMed
Osen-Sand, A., Catsicas, M., Staple, J.K., Jones, K.A., Ayala, G., Knowles, J., Grenningloh, G. & Catsicas, S. (1993). Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo. Nature 364, 445–448Google Scholar
Pieribone, V., Shupliakov, O., Brodin, L., Hilfiker-Rothenfluh, S., Czernick, A. & Greengard, P. (1995). Distinct pools of vesicles in neurotransmitter release. Nature 375, 493–497.Google Scholar
Pow, D.V., Crook, D.K. & Wong, R.O.L. (1994). Early appearance and transient expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: An immunocytochemical study. Visual Neuroscience 11, 1115–1134.Google Scholar
Pow, D.V., Wright, L.L. & Vaney, D.I. (1995). The immunocytochemical detection of amino-acid neurotransmitters in paraformaldehyde-fixed tissues. Journal of Neuroscience Methods 56, 115–123.Google Scholar
Redburn, D.A. & Madtes, P. Jr (1986). Postnatal development of 3H-GABA-accumulating cells in rabbit retina. Journal of Comparative Neurology 243, 41–57.Google Scholar
Reese, B.E., Johnson, P.T. & Baker, G.E. (1996). Maturational gradients in the retina of the ferret. Journal of Comparative Neurology 375, 252–273.Google Scholar
Richards, J.G., Schoch, P., Haring, P., Takacs, B. & Mohler, H. (1987). Resolving GABAA/benzodiazepine receptors: Cellular and subcellular localization in the CNS with monoclonal antibodies. Journal of Neuroscience 7, 1866–1886.Google Scholar
Robinson, S.R. (1991). Development of the mammalian retina. Neuroanatomy of the visual pathways and their development. In Vision and Visual Dysfunction, Vol. 3, pp. 69–128. ed. Dreher, B. & Robinson, S.R.U.K.: Macmillan.Google Scholar
Sassoé-Pognetto, M. & Wässle, H. (1997). Synaptogenesis in the rat retina: Subcellular localization of glycine receptors, GABAA receptors, and the anchoring protein Gephyrin. Journal of Comparative Neurology 379, 1–17.Google Scholar
Schnitzer, J. & Rusoff, A.C. (1984). Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. Journal of Neuroscience 4, 2948–2955.Google Scholar
Schoch, P. & Möhler, H. (1983). Purified benzodiazepene receptor retains modulation by GABA. European Journal of Pharmacology 95, 323–324.CrossRefGoogle Scholar
Shields, C., Lukasiewicz, P.D. & Wong, R.O.L. (1996). GABAergic modulation of spontaneous bursting activity in the developing ferret retina. Investigative Ophthalmology and Visual Science 37, 2918.Google Scholar
Söllner, T., Bennett, M.K., Whiteheart, S.W., Scheller, R.H. & Rothman, J.E. (1993). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409–418.Google Scholar
Südhof, T.C., Czernick, A.J., Kao, H., Takei, K., Johnston, P.A., Horiuchi, A., Wagner, M., Kanazir, S.D., Perin, P.S., De Camilli, P. & Grenngard, P. (1989). Synapsins: Mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science 245, 1474–1480.Google Scholar
Ullrich, B. & Südhof, T.C. (1994). Distribution of synaptic markers in the retina: Implications for synaptic vesicle traffic in ribbon synapses. Journal of Physiology 88, 249–257.Google Scholar
Vardi, N., Masarachia, P. & Sterling, P. (1992). Immunoreactivity to GABAa receptor in the outer plexiform layer of the cat retina. Journal of Comparative Neurology 320, 394–397.Google Scholar
Vardi, N. & Sterling, P. (1994). Subcellular localization of GABA(A) receptor on bipolar cells in macaque and human retina. Vision Research 24, 1235–1246.Google Scholar
Versaux-Botteri, C., Pochet, R. & Nguyen-Legros, J. (1989). Immu-nohistochemical localization of GABA-containing neurons during postnatal development of the rat retina. Investigative Ophthalmology and Visual Science 30, 652–659.Google Scholar
West Greenlee, M.H., Swanson, J.J., Simon, J.J., Elmquist, J.K., Jacobson, C.D. & Sakaguchi, D.S. (1996). Postnatal development and the differential expression of presynaptic terminal-associated proteins in the developing retina of the Brazilian opossum, Monodelphis domestica. Developmental Brain Research 96, 159–172.Google Scholar
Whitehart, S.W. & Kubalek, E.W. (1995). SNAPs and NSF: General members of the fusion apparatus. Trends in Cell Biology 5, 65–68.Google Scholar
Wickler, K.C. & Rakic, P. (1994). An array of early differentiating cones precedes the emergence of the photoreceptor mosaic in the fetal monkey retina. Proceedings of the National Academy of Sciences of the U.S.A. 91, 6534–6538.CrossRefGoogle Scholar
Wong, R.O.L., Meister, M. & Shatz, C.J. (1993). Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11, 923–938.Google Scholar
Wong, R.O.L., Chernjavsky, A., Smith, S.J. & Shatz, C.J. (1995). Early functional neural networks in the developing retina. Nature 374, 716–718.Google Scholar