Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-18T22:48:03.289Z Has data issue: false hasContentIssue false

Organization and development of horizontal cells in the goldfish retina, I: The use of monoclonal antibody AT101

Published online by Cambridge University Press:  02 June 2009

You-Wel Peng
Affiliation:
Alice R. McPherson Laboratory of Retina Research, The Center for Biotechnology, Baylor College of Medicine, The Woodlands
Dominic Man-Kit lam
Affiliation:
Alice R. McPherson Laboratory of Retina Research, The Center for Biotechnology, Baylor College of Medicine, The Woodlands

Abstract

We have produced and characterized a monoclonal antibody, AT101, which selectively labels both viable and formaldehyde-fixed horizontal cell axon terminals, but not their somas or axons, of the goldfish (Carassius auratus) retina. The antigen recognized by AT101 appears to be a cell surface glycoprotein with a molecular weight of about 35,000 Daltons, and is present exclusively or predominantly in nervous tissues of all vertebrate species examined. We have used AT101 as a probe to analyze immunocytochemically the organization of horizontal cell axon terminals (HCATs) in the adult goldfish retina, and the emergence and maturation of these terminals during retinal development. Because of continued growth at the retinal margin in adult goldfish, there is a peripheral-to-central gradient in the age of cells, with the most mature in the center and the youngest in the periphery. In the center and near periphery of the adult retina, HCATs have a fusiform morphology and form a dense network in the middle and proximal part of the inner nuclear layer. In the far peripheral retina, the axon terminals appear round or ellipsoid. The retina closest to the retinal margin is devoid of AT101 staining, indicating that either HCATs are absent or the antigen recognized by AT101 is not present on HCATs at this stage. A similar sequence of changes in staining pattern is seen during development. Although AT101 staining can first be demonstrated in the larval retina at 1 month after hatching, it appears mostly as punctate structures. At a later stage, there are round or ellipsoid structures that resemble in morphology and location (in the inner nuclear layer) those found in the far peripheral adult retina. Double-labeling experiments with AT101 and antiserum against tubulin also indicate that AT101 labels the HCATs when they first appear during development. These data suggest that the emergence and maturation of HCAT is a late event in retinal development.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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

Ayoub, G.S. & Lam, D.M.K. (1984). The release of γ-aminobutyric acid from horizontal cells of the goldfish (Carassius auratus) retina. Journal of Physiology 55, 191214.Google Scholar
Baylor, D.A.,Fuortes, M.G.F. & O'bryan, P.M. (1971).Receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265294.CrossRefGoogle ScholarPubMed
Cajal, S.R. (1972).The structure of retina. Translation by Thorpe, S.A. & Glickstein, M., p. 17. Springfield, IL: C.C. Thomas.Google Scholar
Dahl, D., Crosby, C.J. & Bignami, A. (1986). Neurofilament proteins in fish: a study with monoclonal antibodies reacting with mammalian NF 150k and 200k. Journal of Comparative Neurology 250,399402.CrossRefGoogle Scholar
Dowling, J.E. (1988). Neuromodulation in the retina: the role of dopamine and interplexiform cells in the fish. In Proceedings of the Retina Research Foundation Symposium, Vol. 1, ed. Lam, D.M.K., pp. 114127. The Woodlands, TX: Portfolio Publishing.Google Scholar
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system, I: Synapses of the dopaminergic neurons of the goldfish retina. Proceedings of the Royal Society B (London.) 201, 726.Google Scholar
Drujan, B.D. & Laufer, M. ed. (1982). The S-potential. New York: Liss.Google Scholar
Easter, S.S. (1983). Postnatal neurogenesis and changing connections. Trends in Neuroscience 6, 5356.Google Scholar
Elder, J.H.,& Alexander, S. (1982). Endo-beta-N-acetylglucosaminidase F: Endoglycosidase from Glavobacterium memingosepticum that cleaves both high-mannose and complex glycoproteins. Proceeding of the National Academy of Sciences of the U.S.A. 79, 45404544.Google Scholar
Hashimoto, Y., Kato, A.Inokuchi, M. & Watanabe, K. (1976). Reexamination of horizontal cells in the carp retina with procion yellow electrode. Vision Research 16, 2529.Google Scholar
Johns, P.R. (1977). Growth of the adult goldfish eye, III: Source of the new retinal cells. Journal of Comparative Neurology 176, 343358.CrossRefGoogle ScholarPubMed
Johns, P.R. (1982). Formation of photoreceptors in the growing retinas of larval and adult goldfish. Journal of Neuroscience 2, 179198.Google Scholar
Johns, P.R. & Easter, S.S. (1977). Growth of the adult goldfish eye—increase in retinal cell number. Journal of Comparative Neurology 176, 331342.Google Scholar
Jones, P.S. & Schechter, N. (1987). Distribution of specific intermediate-filament proteins in the goldfish retina. Journal of Comparative Neurology 266, 112121.Google Scholar
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar, and amacrine cells in goldfish retina. Journal of Physiology 207, 623633.CrossRefGoogle ScholarPubMed
Kaneko, A. & Stuart, A.E. (1984). Coupling between horizontal cells in the carp retina revealed by diffusion of Lucifer yellow. Neuroscience Letters 47, 17.CrossRefGoogle ScholarPubMed
Kock, J.-H. & Stell, W.K. (1985). Formation of new rod photoreceptor synapses onto differentiated bipolar cells in goldfish retina. Anatomy Records 211, 6974.CrossRefGoogle ScholarPubMed
Kouyama, N. & Watanabe, K. (1986). Gap-junctional contacts of luminosity-type horizontal cells in the carp retina: a novel pathway of signal conduction from the cell body to the axon terminal. Journal of Comparative Neurology 249, 404410.CrossRefGoogle Scholar
Lam, D.M.K. (1975). Biosynthesis of γ-aminobutyric acid by isolated axons of cone horizontal cells in the goldfish retina. Nature 254, 345347.Google Scholar
Lam, D.M.K. (1976). Synaptic chemistry of identified cells in the vertebrate retina. Cold Spring Harbor Symposia on Quantitative Biology XL 571579.Google Scholar
Lam, D.M.K. (1988 a). Development of neurotransmitter systems in the retina: biochemical, anatomical, and physiological correlates. In Retinal Diseases, ed. Tso, M., pp. 103111.Google Scholar
Lam, D.M.K. (1988b). Co-existence 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. 182198. The Woodlands, TX: Portfolio Publishing.Google Scholar
Lam, D.M.K. & Steinman, L. (1971). The uptake of [γ-3H]-aminobutyric acid in the goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 68, 27772781.CrossRefGoogle ScholarPubMed
Lasater, E.M. (1987). Retinal horizontal cell gap-junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase. Proceedings of the National Academy of Sciences of the U.S.A. 84, 73197323.Google Scholar
Linser, P.J., Smith, K. & Angelides, K. (1985). A comparative analysis of glial and neuronal markers in the retina of fish: variable character of horizontal cells. Journal of Comparative Neurology 237, 264272.Google Scholar
Littlefield, J.W. (1964). Selection of hybrids from mating of fibroblasts in vitro and their presumed recombinants. Science 145, 409.CrossRefGoogle ScholarPubMed
Marc, R.E. (1986). The development of retinal networks. In The Retina: A Model for Cell Biology Studies, ed. Adler, R.& Farber, D., Pt. I, pp. 1765.Google Scholar
Marc, R.E. & Liu, W.-L.S. (1984). Horizontal cell synapses onto glycine accumulating interplexiform cells. Nature 312, 266.CrossRefGoogle ScholarPubMed
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221246. New York: Academic Press.Google Scholar
Marshak, D.W. & Dowling, J.E. (1987). Synapses of cone horizontal cell axons in goldfish retina. Journal of Comparative Neurology 256, 430443.CrossRefGoogle ScholarPubMed
Meyer, R.L. (1978). Evidence from the thymidine labeling for continuing growth of retina and tectum in juvenile goldfish. Experimental Neurology 59, 99111.CrossRefGoogle ScholarPubMed
Mitarai, G., Asano, T. & Miyake, Y. (1974). Identification of five types of S-potential and their corresponding generating sites in the horizontal cells of the carp retina. Japan Journal of Ophthalmology 18, 161176.Google Scholar
Naka, K.I. (1977). Functional organization of catfish retina. Journal of Neurophysiology 40, 2643.CrossRefGoogle ScholarPubMed
Naka, K.I., & Rushton, W.A. (1967). The generation and spread of S-potentials in fish (Cyprinidae). Journal of Physiology (London) 192, 437461.Google Scholar
Ohtsuka, T. (1983). Axons connecting somata and axon terminals of luminosity-type horizontal cells in the turtle retina: receptive-field studies and intracellular injection of HRP. Journal of Comparative Neurology 220, 191198.Google Scholar
Olmsted, J.B. (1986). Microtubule-associated proteins. Annual Review of Cell Biology 2, 421457.Google Scholar
Parthe, V. (1981). Horizontal cell processes in teleost retina. Journal of Neuroscience Research 6, 113118.CrossRefGoogle ScholarPubMed
Raymond, P.A. (1985). Cytodifferentiation of photoreceptors in larval goldfish: delayed maturation of rods. Journal of Comparative Neurology 236, 90105.Google Scholar
Raymond, P.A. & Rivlin, P.K. (1987). Germinal cells in the goldfish retina that produce rod photoreceptors. Development Biology 122, 120138.CrossRefGoogle ScholarPubMed
Sakai, H. & Naka, K.-I. (1985). Novel pathway connecting the outer and inner vertebrate retina. Nature 315, 570571.CrossRefGoogle ScholarPubMed
Sakai, H. & Naka, K.-I. (1986). The synaptic organization of the cone horizontal cells in the catfish retina. Journal of Comparative Neurology 245, 107.Google Scholar
Sale, W.S., Besharse, J.C. & Piperno, .G. (1988). Distribution of acetylated a-tubulin in retina and in vitro-assembled microtubules. Cell Mobility 9, 243253.Google Scholar
Sarthy, P.V. & Lam, D.M.K. (1979). The uptake and release of [-3H]- dopamine in the goldfish retina. Journal of Neurochemistry 32, 12691277.Google Scholar
Stell, W.K. (1975). Horizontal cell axons and axon terminals in goldfish retina. Journal of Comparative Neurology 159, 503520.Google Scholar
Stell, W.K. & Lightfoot, D.O. (1975). Color-specific inter-connections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473502.CrossRefGoogle Scholar
Ternanishi, T. (1983). Lateral spread of light-induced response at the cell body and axon terminal levels of external horizontal cells in the carp retina. Japan Journal of Physiology 33, 417.Google Scholar
Ternanishi, T., Negish, K. & Kato, S. (1984). Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 12711280.CrossRefGoogle Scholar
Towbin, H., Stalhelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences of the U.S.A. 76, 43504354.CrossRefGoogle ScholarPubMed
Tucker, R.P., Binder, L.I. & Matus, A.I. (1988). Differential localization of the high- and low-molecular weight variants of MAP2 in the developing retina. Developmental Brain Research 38, 313318.CrossRefGoogle Scholar
Van Buskirk, R. & Dowling, J.E. (1981). Isolated horizontal cells from carp retina demonstrate dopamine-dependent accumulation of cyclic AMP. Proceedings of the National Academy of Sciences of the U.S.A. 78, 78257829.CrossRefGoogle ScholarPubMed
Weiler, R. & Zettler, F. (1979). The axon-bearing horizontal cells in the teleost retina are functional as well as structural units. Vision Research 19, 12611268.Google Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus, II: Intracellular recording. Journal of Neurophysiology 32, 339355.Google Scholar
Yagi, T. (1986). Interaction between the soma and the axon terminal of retinal horizontal cells in cyprinus carp. Journal of Physiology (London) 375, 121135.CrossRefGoogle Scholar
Yagi, T. & Kaneko, A. (1988). The axon terminal of goldfish retinal horizontal cells: a low membrane conductance measured in solitary preparation and its implication to the signal conduction from the soma. Journal of Neurophysiology 59, 482494.CrossRefGoogle Scholar
Yamada, E. & Ishikawa, T. (1965). The fine structure of the horizontal cells in some vertebrate retina. Cold Spring Harbor Symposium on Quantitative Biology 30, 383.Google Scholar
Young, L.H. & Dowling, J.E. (1984). Monoclonal antibodies distinguish subtypes of retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 81, 62556259.Google Scholar