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Bipolar cells of the chick retina containing α-bungarotoxin-sensitive nicotinic acetylcholine receptors

Published online by Cambridge University Press:  02 June 2009

Dânia E. Hamassaki-Britto ,
Agnieszka Brzozowska-Prechtl ,
Harvey J. Karten  and
Jon M. Lindstrom
Dânia E. Hamassaki-Britto
Affiliation:
Department of Neurosciences, University of California San Diego, La Jolla Department of Histology and Embryology/ICB, University of São Paulo, São Paulo, SP, Brazil
Agnieszka Brzozowska-Prechtl
Affiliation:
Department of Neurosciences, University of California San Diego, La Jolla
Harvey J. Karten
Affiliation:
Department of Neurosciences, University of California San Diego, La Jolla
Jon M. Lindstrom
Affiliation:
Institute of Neurological Sciences, University of Pennsylvania, Philadelphia
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Abstract

Two cDNA clones for nicotinic acetylcholine receptor (nAChR) subunits sensitive to α-bungarotoxin (α-Bgt) have been isolated, the so-called α-Bgt binding proteins α1 (or α7 nAChR subunit) and α2 (or α8 nAChR subunit). Immunohistochemical experiments have shown that both α7 and α8 subunits, as well as subunits insensitive to α-Bgt (β2 and α3), are present in amacrine and ganglion cells of the chick retina. However, only the α8 subunit was observed in presumptive bipolar cells. The present study investigated in detail the pattern of distribution of the bipolar cells containing the α8 nAChR subunit and its relation to the pattern of distribution of bipolar cells immunoreactive to protein kinase C (PKC). Presumptive α8-and PKC-like immunoreactive (α8-LI and PKC-LI) bipolar cells were observed sending their dendrites to the outer plexiform layers and their axons to the inner plexiform layer. Where as α8-LI bipolar cells corresponded to 40–53% of the whole population of bipolar cells, PKC-LI bipolar cells represented only 6–8% of the same population. The soma sizes of the α8-LI bipolar cells were slightly smaller (mean ± s.d.; 4.9 ± 0.8 μm) than the soma sizes of the PKC-LI bipolar cells (5.4 ± 0.9 μm). Double-labeling experiments indicated that probably all PKC-LI bipolar cells also contain α8-LI. This indicates that two distinct groups of cholinoceptive bipolar cells exist in the chick retina, one that contains PKC-LI, and another one that does not.

Keywords

Bipolar cellsNicotinic receptorsProtein kinase C.α-BgtRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 63 - 70
Copyright
Copyright © Cambridge University Press 1994

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References

Ariel, M. & Daw, N. (1982 a). Effects of cholinergic drugs on receptive-field properties of rabbit retinal ganglion cells. Journal of Physiology 324, 135–160.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N. (1982 b). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–186.CrossRefGoogle ScholarPubMed
Britto, L.R.G., Keyser, K.T., Lindstrom, J.M. & Karten, H.J. (1992). Immunohistochemical localization of nicotinic acetylcholine receptor subunits in the mesencephalon and diencephalon of the chick (Gallus gallus). Journal of Comparative Neurology 317, 325–340.CrossRefGoogle ScholarPubMed
Clarke, P.B.S. (1992). The fall and rise of neuronal α-bungarotoxin binding proteins. Trends in Pharmacological Sciences 13, 407–413.CrossRefGoogle ScholarPubMed
Conley, M., Fitzpatrick, D. & Lachica, E.A. (1986). Laminar asymmetry in the distribution of choline acetyltransferase-immunoreactive neurons in the retina of the tree shrew (Tupaia belangeri). Brain Research 399, 332–338.CrossRefGoogle ScholarPubMed
Couturier, S., Bertrand, D., Matter, J.-M., Hernandez, M.-C., Bertrand, S., Milla, N., Valera, S., Barkas, T. & Ballivet, M. (1990). A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5, 847–856.CrossRefGoogle Scholar
Cuenca, N., Fernández, E. & Kolb, H. (1990). Distribution of immunoreactivity to protein kinase C in the turtle retina. Brain Research 532, 278–287.CrossRefGoogle ScholarPubMed
Deneris, E.S., Connolly, J., Rogers, S.W. & Duvoisin, R. (1991). Pharmacological and functional diversity of neuronal nicotinic acetylcholine receptors. Trends in Pharmacological Sciences 12, 34–40.CrossRefGoogle ScholarPubMed
Eckenstein, F. & Thoenen, H. (1982). Production of specific antisera and monoclonal antibodies to choline acetyltransferase: Characterization and use for identification of cholinergic neurons. EMBO Journal 1, 363–368.CrossRefGoogle ScholarPubMed
Geertsen, S., Afar, R., Trifar⊙, J.-M. & Quik, M. (1990). Phorbol esters and d-tubocurarine up-regulate α-bungarotoxin sites in chromaffin cells in culture via distinct mechanisms. Neuroscience 34, 441–450.CrossRefGoogle ScholarPubMed
Golcich, M.A., Morgan, I.G. & Dvorak, D.R. (1990). Selective abolition of OFF responses in kainic acid-lesioned chicken retina. Brain Research 535, 288–300.CrossRefGoogle ScholarPubMed
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, 433–442.CrossRefGoogle ScholarPubMed
Hamassaki-Britto, D.E., Brzozowska-Prechtl, A., Karten, H.J., Lindstrom, J.M. & Keyser, K.T. (1991). GABA-like immunoreactive cells containing nicotinic acetylcholine receptors in the chick retina. Journal of Comparative Neurology 313, 394–408.CrossRefGoogle ScholarPubMed
Hughes, T.E., Carey, R.G., Vitorica, 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
Iniguez, C., Gayoso, M.J. & Carreres, J. (1985). A versatile and simple method for staining nervous tissue using Giemsa dye. Journal of Neuroscience Methods 13, 77–86.CrossRefGoogle ScholarPubMed
James, W.M. & Klein, W.L. (1985). Alpha-bungarotoxin receptors on neurons isolated from turtle retina: Molecular heterogeneity of bipolar cells. Journal of Neuroscience 5, 352–361.CrossRefGoogle ScholarPubMed
Keyser, K.T., Hughes, T.E., Whiting, P.J., Lindstrom, J.M. & Karten, H.J. (1988). Cholinoceptive neurons in the retina of the chick: An immunohistochemical study of the nicotinic acetylcholine receptors. Visual Neuroscience 1, 349–366.CrossRefGoogle ScholarPubMed
Keyser, K.T., Britto, L.R.G., Schoepfer, R., Whiting, P., Cooper, J., Conroy, W., Brzozowska-Prechtl, A., Karten, H.J. & Lindstrom, J.M. (1993). Three subtypes of α-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick retina. Journal of Neuroscience 13, 442–454.CrossRefGoogle ScholarPubMed
Lam, D.M.K. (1972). Biosynthesis of acetylcholine in turtle photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 69, 1987–1991.CrossRefGoogle ScholarPubMed
Lindstrom, J.M., Schoepfer, R. & Whiting, P. (1987). Molecular studies of the neuronal nicotinic acetylcholine receptor family. Molecular Neurobiology 1, 281–337.CrossRefGoogle ScholarPubMed
Ma, P.M. & Grant, P. (1984). Choline acetyltransferase and cholinesterases in the developing Xenopus retina. Journal of Neurochemistry 42, 1328–1337.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1987). Neuronal and synaptic organization of the outer plexiform layer of the pigeon retina. American Journal of Anatomy 179, 25–39.CrossRefGoogle ScholarPubMed
Martin, P.R. & Grünert, U. (1992). Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 323, 269–287.CrossRefGoogle ScholarPubMed
Masland, R.H. & Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.CrossRefGoogle Scholar
Millar, T.J., Ishimoto, I., Chubb, I.W., Epstein, M.L., Johnson, C.D. & Morgan, I.G. (1987). Cholinergic amacrine cells of the chicken retina: A light and electron microscope immunocytochemical study. Neuroscience 21, 725–743.CrossRefGoogle ScholarPubMed
Millar, T.J., Ishimoto, I., Johnson, C.D., Epstein, M.L., Chubb, I.W. & Morgan, I.G. (1985). Cholinergic and acetylcholinesterase-containing neurons of the chicken retina. Neuroscience Letters 74, 281–285.CrossRefGoogle Scholar
Millar, T.J., Winder, C., Ishimoto, I. & Morgan, I.G. (1988). Putative serotonergic bipolar and amacrine cells in the chicken retina. Brain Research 439, 77–87.CrossRefGoogle ScholarPubMed
Müller, B. & Peichl, L. (1991). Rod bipolar cells in the cone-dominated retina of the tree shrew Tupaia belangeri. Visual Neuroscience 6, 629–639.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 247–252.CrossRefGoogle ScholarPubMed
Pourcho, R. (1979). Localization of cholinergic synapses in mammalian retina with peroxidase-conjugated alpha-bungarotoxin. Vision Research 19, 287–292.CrossRefGoogle ScholarPubMed
Quik, M., Babu, U., Audhya, T. & Goldstein, G. (1991). Evidence for thymopoietin and thymopoietin/α-bungarotoxin/nicotinic receptors within the brain. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2603–2607.CrossRefGoogle ScholarPubMed
Rogers, J.H. (1989). Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 31, 697–709.CrossRefGoogle ScholarPubMed
Ross, C.D. & McDougal, D.B. Jr (1976). The distribution of choline acetyltransferase activity in vertebrate retina. Journal of Neurochemistry 26, 521–526.CrossRefGoogle ScholarPubMed
Sarthy, P.V. & Lam, D.M.K. (1979). Endogenous levels of neurotransmitter candidates in photoreceptor cells of the turtle retina. Journal of Neurochemistry 32, 455–461.CrossRefGoogle ScholarPubMed
Sattayasai, J., Rogers, L.J. & Ehrlich, D. (1985). Sequential treatment with low doses of kainic acid alters sensitivity of retinal cell types. Neuroscience Letters 54, 277–281.CrossRefGoogle ScholarPubMed
Schoepfer, R., Conroy, W.G., Whiting, P., Gore, M. & Lindstrom, J. (1990). Brain α-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 5, 35–48.CrossRefGoogle ScholarPubMed
Schwartz, I.R. & Bok, D. (1979). Electron microscopic localization of [125I] α-bungarotoxin binding sites in the outer plexiform layer of the goldfish retina. Journal of Neurocytology 8, 53–66.CrossRefGoogle ScholarPubMed
Spira, A.W., Millar, T.J., Ishimoto, I., Epstein, M.L., Johnson, C.D., Dahl, J.L. & Morgan, I.G. (1987). Localization of choline acetyltransferase-like immunoreactivity in the embryonic chick retina. Journal of Comparative Neurology 260, 526–538.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to the on-beta ganglion cell. Journal of Neuroscience 8, 623–642.CrossRefGoogle Scholar
TerBush, D.R. & Holz, R. W. (1986). Effects of phorbol esters, diglyceride, and cholinergic agonists on the subcellular distribution of protein kinase C in intact or digitonin-permeabilized adrenal chromaffin cells. Journal of Biological Chemistry 261, 17099–17106.CrossRefGoogle ScholarPubMed
Tumosa, N., Eckenstein, F. & Stell, W.K. (1984). Immunocytochemical localizations of putative cholinergic neurons in the goldfish retina. Neuroscience Letters 48, 255–259.CrossRefGoogle ScholarPubMed
Vogel, Z., Maloney, G.J., Ling, A. & Daniels, M.P. (1977). Identification of synaptic acetylcholine receptor sites in retina with peroxidase-labeled alpha-bungarotoxin. Proceedings of the National Academy of Sciences of the U.S.A. 74, 3268–3272.CrossRefGoogle ScholarPubMed
Vogel, Z. & Nirenberg, M. (1976). Localization of acetylcholine receptors during synaptogenesis in retina. Proceedings of the National Academy of Sciences of the U.S.A. 73, 1806–1810.CrossRefGoogle ScholarPubMed
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.CrossRefGoogle ScholarPubMed
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.Google ScholarPubMed
Wässle, H., Peichl, L. & Boycott, B.B. (1978). Topography of horizontal cells in the retina of the domestic cat. Proceedings of the Royal Society B (London) 203, 269–291.Google ScholarPubMed
Whiting, P., Schoepfer, R., Conroy, W.G., Gore, M.J., Keyser, K.T., Shimasaki, S., Esch, F. & Lindstrom, J.M. (1991). Differential expression of nicotinic acetylcholine receptor subtypes in brain and retina. Molecular Brain Research 10, 61–70.CrossRefGoogle ScholarPubMed
Witkowsky, P. & Schütte, M. (1991). The organization of dopaminergic neurons in vertebrate retinas. Visual Neuroscience 7, 113–124.CrossRefGoogle Scholar
Wood, J.G., Hart, C.E., Mazzei, G.J., Girard, P.R. & Kuo, J.F. (1988). Distribution of protein kinase C immunoreactivity in rat retina. Histochemical Journal 20, 63–68.CrossRefGoogle ScholarPubMed
Yazulla, S. (1979). Synaptic layers of the retina: A comparative analysis with [125I]-alpha-bungarotoxin. In Granda, A.M. & Maxwell, J.H., ed. Neural Mechanisms of Behavior in the Pigeon, pp. 353–369. New York: Plenum Press.Google Scholar
Yazulla, S. & Schmidt, J. (1976). Radioautographic localization of [125I] alpha-bungarotoxin binding sites in the retinas of goldfish and turtle. Vision Research 16, 878–880.CrossRefGoogle ScholarPubMed
Yazulla, S. & Schmidt, J. (1977). Two types of receptors for alpha-bungarotoxin in the synaptic layers of the pigeon retina. Brain Research 138, 45–47.CrossRefGoogle ScholarPubMed
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells. Journal of Comparative Neurology 310, 139–153.CrossRefGoogle ScholarPubMed
Zhang, D. & Yeh, H.H. (1991). Protein kinase C-like immunoreactivity in rod bipolar cells of the rat retina: A developmental study. Visual Neuroscience 6, 429–437.CrossRefGoogle ScholarPubMed
Zucker, C. & Yazulla, S. (1982). Localization of synaptic and non-synaptic nicotinic-acetylcholine receptors in the goldfish retina. Journal of Comparative Neurology 204, 188–195.CrossRefGoogle Scholar