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Serotonin synthesis and accumulation by neurons of the anuran retina

Published online by Cambridge University Press:  02 June 2009

Baosong Zhu ,
Robert Gábriel  and
Charles Straznicky
Baosong Zhu
Affiliation:
Department of Anatomy and Histology, School of Medicine, The Flinders University of South Australia, Adelaide, Australia
Robert Gábriel
Affiliation:
Department of Anatomy and Histology, School of Medicine, The Flinders University of South Australia, Adelaide, Australia
Charles Straznicky
Affiliation:
Department of Anatomy and Histology, School of Medicine, The Flinders University of South Australia, Adelaide, Australia
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Abstract

Serotonin-synthesizing and serotonin-accumulating neurons were studied in the retinas of Xenopus laevis and Bufo marinus. All previously identified cell types exhibiting serotonin-like immunoreactivity (SLI) were labeled by intravitreal injection of 5,7-dihydroxytryptamine (5,7-DHT). They included two amacrine cell types (large and small) in both species, and one bipolar cell type in Xenopus. Incubation of retinas in culture medium in the ambient light reduced SLI in amacrine cells and enhanced the labeling in bipolar cells. After incubation, some photoreceptor cell bodies and large numbers of outer segments also displayed SLI in both species. Incubation with the serotonin-uptake inhibitor, fluoxetine, reduced immunolabeling in bipolar cells and outer segments to the level in the untreated retinas.

Both large SLI and 5,7-DHT-accumulating amacrine cells in Xenopus and Bufo were labeled with an antibody raised against phenylalanine hydroxylase (PH), which binds to tryptophan 5-hydroxylase, one of the synthesizing enzymes for serotonin. Small SLI and 5,7-DHT-accumulating amacrine cells in both species represented two populations, one with and the other without PH-like immunoreactivity (PH-LI). The anti-PH antibody failed to label any SLI or 5,7-DHT-accumulating bipolar cells in Xenopus.

These observations indicate that all large and some small SLI amacrine cells in the retinas of Xenopus and Bufo synthesize serotonin, while other small SLI amacrine, bipolar and photoreceptor cell bodies, and outer segments only accumulate serotonin.

Keywords

SerotoninTryptophan 5-hydroxylaseImmunohistochemistryDouble labelingAnuran retina
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 3-4 , October 1992 , pp. 377 - 388
Copyright
Copyright © Cambridge University Press 1992

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References

Baker, K.G., Halliday, G.M., Hornung, J-P., Geffen, L.B., Cotton, R.G.H. & Törk, I. (1991). Distribution, morphology and number of monoamine-synthesizing and substance P-containing neurons in the human dorsal raphe nucleus. Neuroscience 42, 757–775.CrossRefGoogle ScholarPubMed
Baker, P.C. & Hoff, K.M. (1971). Melatonin localization in the eyes of larval Xenopus. Comparative Biochemistry and Physiology A 39, 879–881.CrossRefGoogle ScholarPubMed
Baker, P.C., Quay, W.B. & Axelrod, J. (1965). Development of hydroxyindole-O-methyltransferase activity in eye and brain of the amphibian, Xenopus laevis. Life Science 4, 1981–1987.CrossRefGoogle Scholar
Besharse, J.C. & Dunis, D.A. (1983). Methoxyindoles and photoreceptor metabolism: Activation of rod shedding. Science 219, 1341–1343.CrossRefGoogle ScholarPubMed
Bruun, A., Ehinger, B. & Sytsma, V.M. (1984). Neurotransmitter localization in the skate retina. Brain Research 295, 233–248.CrossRefGoogle ScholarPubMed
Cahill, G.M. & Besharse, J.C. (1990). Circadian regulation of melatonin in the retina of Xenopus laevis: Limitation by serotonin availability. Journal of Neurochemistry 54, 716–719.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. (1983). Melatonin is a potent modulator of dopamine release in the retina. Nature 306, 782–784.CrossRefGoogle ScholarPubMed
Ehinger, B. (1983). Connexions between retinal neurons with identified neurotransmitter. Vision Research 23, 1281–1291.CrossRefGoogle Scholar
Florén, I. & Hansson, H.C. (1980). Is 5-hydroxytryptamine a retinal transmitter? Investigative Ophthalmology 19, 117–125.Google Scholar
Frederick, J.M., Rayborn, M.E. & Hollyfield, J.G. (1989). Serotoninergic neurons in the retina of Xenopus laevis: Selective staining, identification, development and content. Journal of Comparative Neurology 281, 516–531.CrossRefGoogle ScholarPubMed
Gábriel, R., Zhu, B.-S. & Straznicky, C. (1991). Tyrosine hydroxylase-immunoreactive elements in the distal retina of Bufo marinus: A light and electron microscopic study. Brain Research 559, 225–232.CrossRefGoogle ScholarPubMed
Gläsener, G., Schmidt, C. & Himstedt, W. (1988). Two populations of serotonin-immunoreactive neurons in the frog (Rana esculenta) retina. Neuroscience Letters 84, 251–254.CrossRefGoogle ScholarPubMed
Haan, E.A., Jennings, I.G., Cuello, A.C., Nakata, H., Fujisawa, H., Chow, C.W., Kushinsky, R., Brittingham, J. & Cotton, R.G.H. (1987). Identification of serotonergic neurons in human brain by a monoclonal antibody binding to all three aromatic amino acid hydroxylases. Brain Research 426, 19–27.CrossRefGoogle ScholarPubMed
Iuvone, P.M. & Besharse, J.C. (1983). Regulation of indolamine N-acetyltransferase activity in the retina: Effects of light and dark, protein synthesis inhibitors and cyclic nucleotide analogs. Brain Research 273, 111–119.CrossRefGoogle Scholar
Marc, R.E., Liu, W-L.S., Scholz, K. & Muller, J.F. (1988). Serotonergic and serotonin-accumulating neurons in the goldfish retina. Journal of Neuroscience 8, 3427–3450.CrossRefGoogle ScholarPubMed
Messenger, E.A. & Warner, A.E. (1977). The action of melatonin on single amphibian pigment cells in tissue culture. British Journal of Pharmacology 61, 607–614.CrossRefGoogle ScholarPubMed
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
Osborne, N.N. (1984). Indoleamines in the eye with special reference to the serotonergic neurons of the retina. In Progress in Retinal Research, ed. Osborne, N.N. & Chader, G., pp. 61–103. Oxford: Pergamon Press.Google Scholar
Osborne, N.N., Nesselhut, T., Nicholas, D.A., Patel, S. & Cuello, C. (1982). Serotonin-containing neurons in the vertebrate retinas. Journal of Neurochemistry 39, 1519–1528.CrossRefGoogle ScholarPubMed
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movements. I. Interaction of melatonin and dopamine in the control of cone length. Journal of General Physiology 86, 671–689.CrossRefGoogle ScholarPubMed
Redburn, D.A. (1985). Serotonin neurotransmitter systems in vertebrate retina. In Retinal Transmitters and Modulators: Models for the Brain, Vol. 2, ed. Morgan, R.A., pp. 107–122. Boca Raton, Florida: CRC Press.Google Scholar
Redburn, D.A. & Churchill, L. (1987). An indolamine system in photoreceptor cell terminals of the Long-Evans rat retina. Journal of Neuroscience 7, 319–329.CrossRefGoogle Scholar
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. Journal of Neuroscience 6, 3331–3347.CrossRefGoogle ScholarPubMed
Schütte, M. & Witkovsky, P. (1990). Serotonin-like immunoreactivity in the retina of the clawed frog Xenopus laevis. Journal of Neurocytotogy 19, 504–518.CrossRefGoogle ScholarPubMed
Schütte, M. & Witkovsky, P. (1991). Dopaminergic interplexiform cells and centrifugal fibres in the Xenopus retina. Journal of Neurocytology 20, 195–207.CrossRefGoogle ScholarPubMed
Tornquist, K., Hansson, Ch. & Ehinger, B. (1983). Immunohistochemical and quantitative analysis of 5-hydroxytryptamine in the retina of some vertebrates. Neurochemistry International 5, 299–308.CrossRefGoogle Scholar
Vaney, D.I. (1986). Morphological identification of serotonin-accumulating neurons in the living retina. Science 233, 444–446.CrossRefGoogle ScholarPubMed
Wässle, H., Voigt, T. & Patel, B. (1987). Morphological and immunocytochemical identification of indoleamine-accumulating neurons in the cat retina. Journal of Neuroscience 7, 1574–1585.CrossRefGoogle ScholarPubMed
Weiler, R. & Schütte, M. (1985). Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of a turtle, Pseudemys scripta elegans. Cell and Tissue Research 241, 373–382.CrossRefGoogle ScholarPubMed
Wiechmann, A.F. & Hollyfield, J.G. (1987). Localization of hydroxyindole-O-methyltransferase-like immunoreactivity in photoreceptors and cone bipolar cells in the human retina: A light and electron microscope study. Journal of Comparative Neurology 258, 253–266.CrossRefGoogle ScholarPubMed
Wiechmann, A.F. & Hollyfield, J.G. (1989). HIOMT-like immunoreactivity in the vertebrate retina: A species comparison. Experimental Eye Research 49, 1079–1095.CrossRefGoogle ScholarPubMed
Wiechmann, A.F., Yang, X.L., Wu, S.M. & Hollyfield, J.G. (1988). Melatonin enhances horizontal cell sensitivity in salamander retina. Brain Research 453, 377–380.CrossRefGoogle ScholarPubMed
Witkovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholamine- and indolamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217–225.CrossRefGoogle Scholar
Wolf, K. & Quimby, M.C. (1964). Amphibian cell culture: Permanent cell line from the bullfrog (Rana catesbiana). Science 144, 1578–1580.CrossRefGoogle Scholar
Yang, S.-Z., Lam, D.M.-K. & Watts, C.B. (1989). Localization of serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 287, 28–37.CrossRefGoogle Scholar
Young, H.M. & Vaney, D. (1990). The retinae of prototherian mammals possess neuronal types that are characteristic of nonmammalian retinae. Visual Neuroscience 5, 61–66.CrossRefGoogle Scholar
Zhu, B.-S. & Straznicky, C. (1990). Morphology and distribution of serotonin-like immunoreactive amacrine cells in the retina of Bufo marinus. Visual Neuroscience 5, 371–378.CrossRefGoogle ScholarPubMed
Zhu, B.-S. & Straznicky, C. (1991). Morphology and retinal distribution of tyrosine hydroxylase-like immunoreactive amacrine cells in the retina of developing Xenopus laevis. Anatomy and Embryology 184, 33–45.CrossRefGoogle ScholarPubMed