Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-12-01T01:13:45.279Z Has data issue: false hasContentIssue false

Tryptophan hydroxylase is expressed by photoreceptors in Xenopus laevis retina

Published online by Cambridge University Press:  02 June 2009

Carla B. Green
Affiliation:
Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City
Gregory M. Cahill
Affiliation:
Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City
Joseph C. Besharse
Affiliation:
Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City

Abstract

Serotonin has important roles, both as a neurotransmitter and as a precursor for melatonin synthesis. In the vertebrate retina, the role and the localization of serotonin have been controversial. Studies examining serotonin immunoreactivity and uptake of radiolabeled serotonin have localized serotonin to inner retinal neurons, particularly populations of amacrine cells, and have proposed that these cells are the sites of serotonin synthesis. However, other reports identify other cells, such as bipolars and photoreceptors, as serotonergic neurons. Tryptophan hydroxylase (TPH), the rate-limiting enzyme in the serotonin synthetic pathway, was recently cloned from Xenopus laevis retina, providing a specific probe for localization of serotonin synthesis. Here we demonstrate that the majority of retinal mRNA encoding TPH is present in photoreceptor cells in Xenopus laevis retina. These cells also contain TPH enzyme activity. Therefore, in addition to being the site of melatonin synthesis, the photoreceptor cells also synthesize serotonin, providing a supply of the substrate needed for the production of melatonin.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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

Andrews, G.K., Lehman, L.D., Huet, Y.M. & Dey, S.K. (1987). Metallothionein gene regulation in the preimplantation rabbit blastocyst. Development 100, 463469.CrossRefGoogle ScholarPubMed
Besharse, J.C. & Dunis, D.A. (1983). Rod photoreceptor disc shedding in eye cups: Relationship to bicarbonate and amino acids. Experimental Eye Research 36, 567580.CrossRefGoogle ScholarPubMed
Bubenik, G.A., Brown, G.M. & Grota, L.J. (1976). Differential localization of N-acetylated indolealkylamines in CNS and the Harderian gland using immunohistology. Brain Research 118, 417427.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, 716719.CrossRefGoogle ScholarPubMed
Cahill, G.M. & Besharse, J.C. (1991). Resetting the circadian clock in cultured Xenopus eyecups: Regulation of retinal melatonin rhythms by light and D2 dopamine receptors. Journal of Neuroscience 11, 29592971.CrossRefGoogle ScholarPubMed
Cahill, G.M. & Besharse, J.C. (1992). Light-sensitive melatonin synthesis by Xenopus photoreceptors after destruction of the inner retina. Visual Neuroscience 8, 487490.CrossRefGoogle ScholarPubMed
Cahill, G.M. & Besharse, J.C. (1993). Circadian clock functions localized in Xenopus retinal photoreceptors. Neuron 10, 573577.CrossRefGoogle ScholarPubMed
Cassone, V.M., Lane, R.F. & Menaker, M. (1986). Melatonin-induced increases in serotonin concentrations in specific regions of the chicken brain. Neuroendocrinology 42, 3843.CrossRefGoogle ScholarPubMed
Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156159.CrossRefGoogle ScholarPubMed
Cleveland, D.W., Lopata, M.A., MacDonald, R.J., Cowan, N.J., Rutter, W.J. & Kirschner, M.W. (1980). Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta-and gamma-actin genes using specific cloned cDNA probes. Cell 20, 95105.CrossRefGoogle ScholarPubMed
De, S.K., McMaster, M.T. & Andrews, G.K. (1990). Endotoxin induction of murine metallothionine gene expression. Journal of Biological Chemistry 265, 1526715274.CrossRefGoogle Scholar
Dumas, S., Darmon, M.C., Delort, J. & Mallet, J. (1989). Differential control of tryptophan hydroxylase expression in raphe and in pineal gland: Evidence for a role of translation efficiency. Journal of Neuroscience Research 24, 537547.CrossRefGoogle ScholarPubMed
Ehinger, B. & Rose, B. (1988). Diurnal variation in chick retinal 5-hydroxytryptamine. Experimental Eye Research 46, 819821.CrossRefGoogle ScholarPubMed
Falcón, J. & Collin, J.-P. (1991). Pineal-retinal relationships: Rhythmic biosynthesis and immunocytochemical localization of melatonin in the retina of the pike (Esox lucius). Cell and Tissue Research 265, 601609.CrossRefGoogle Scholar
Floren, J. & Hansson, H.C. (1980). Investigations into whether 5-hydroxytryptamine is a neurotransmitter in the retina of rabbit and chicken. Investigative Ophthalmology 19, 117125.Google ScholarPubMed
Frederick, J.M., Rayborn, M.E. & Hollyfield, J.G. (1989). Serotoninergic neurons in the retina of Xenopus laevis: Selective staining, identification, development, and content. Acta Anatomy 11847, 30065–11365.Google Scholar
Glasener, G., Schmidt, C. & Himstedt, W. (1988). Two populations of serotonin-immunoreactive neurons in the frog (Rana esculenta) retina. Neuroscience Letters 84, 251254.CrossRefGoogle ScholarPubMed
Green, C.B. & Besharse, J.C. (1994). Tryptophan hydroxylase expression is regulated by a circadian clock in Xenopus laevis retina. Journal of Neurochemistry 62, 24202428.CrossRefGoogle ScholarPubMed
Green, C.B., Cahill, G.M., & Besharse, J.C. (1995). Regulation of tryptophan hydroxylase expression by a retinal circadian oscillator in vitro. Brain Research, in press.CrossRefGoogle Scholar
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 hydroxylases. Brain Research 426, 1927.CrossRefGoogle ScholarPubMed
Iuvone, P.M., Avendano, G., Butler, B.J. & Adler, R. (1990). Cyclic AMP-dependent induction of serotonin N-acetyltransferase activity in photoreceptor-enriched chick retinal cell cultures: Characterization and inhibition by dopamine. Journal of Neurochemistry 55, 673682.CrossRefGoogle ScholarPubMed
Jequier, E., Robinson, D.S., Lovenberg, W. & Sioerdsma, A. (1969). Further studies on tryptophan hydroxylase in rat brainstem and beef pineal. Biochemical Pharmacology 18, 10711081.CrossRefGoogle ScholarPubMed
Klein, D.C. & Weller, J.L. (1970). Indole metabolism in the pineal gland: A circadian rhythm in N-acetyltransferase. Science 169, 10931095.CrossRefGoogle ScholarPubMed
Lehrach, H., Diamond, D., Wozney, J.M. & Boedtker, H. (1977). RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry 16, 47434751.CrossRefGoogle ScholarPubMed
Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265275.CrossRefGoogle ScholarPubMed
Meek, J.L. & Neff, N.H. (1972). Tryptophan 5-hydroxylase: Approximation of half-life and rate of axonal transport. Journal of Neurochemistry 19, 15191525.CrossRefGoogle ScholarPubMed
Meier, D.A., Pastorek, D., James, R.G. & Hager, S.R. (1991). Quantitation of Glut1 and Glut4 mRNA using a solution hybridization assay. Biochemical and Biophysical Research Communications 179, 14201426.CrossRefGoogle ScholarPubMed
Millar, T.J., Winder, C., Peinado, M.-A. & Morgan, I.G. (1988). Putative serotonergic bipolar and amacrine cells in the chicken retina. Brain Research 439, 7787.CrossRefGoogle ScholarPubMed
Osborne, N.N. (1980). In vitro experiments on the metabolism, uptake, and release of 5-hydroxytryptamine in bovine retina. Brain Research 184, 283297.CrossRefGoogle Scholar
Osborne, N.N., Nesselhut, T., Nicholas, D.A. & Cuello, A.C. (1981). Serotonin: A transmitter candidate in the vertebrate retina. Neurochemistry International 3, 171176.CrossRefGoogle ScholarPubMed
Osborne, N.N., Nesselhut, T., Nicholas, D.A., Patel, S. & Cuello, A.C. (1982). Serotonin-containing neurones in vertebrate retinas. Journal of Neurochemistry 39, 15191528.CrossRefGoogle ScholarPubMed
Osborne, N.N. (1984). Indoleamines in the eye with special reference to the serotonergic neurones of the retina. Progress in Retinal Research 3, 61103.CrossRefGoogle Scholar
Osborne, N.N. & Barnett, N.L. (1989). Serotonin levels in the rabbit retina are elevated following intraocular injection of forskolin. Journal of Neurochemistry 53, 19551958.CrossRefGoogle ScholarPubMed
Osborne, N.N. & Barnett, N.L. (1990). What constitutes a serotonergic neurone in the retina? Neurochemistry International 17, 177187.CrossRefGoogle ScholarPubMed
Porrello, K., Bhat, S.P. & Bok, D. (1991). Detection of interphotoreceptor retinoid binding protein (IRBP) mRNA in human and conedominant squirrel retinas by in situ hybridization. Journal of Histochemistry and Cytochemistry 39, 171176.CrossRefGoogle ScholarPubMed
Redburn, D.A. & Churchill, L. (1987). An indoleamine system in photoreceptor cell terminals of the Long-Evans rat retina. Journal of Neuroscience 7, 319329.CrossRefGoogle ScholarPubMed
Redburn, D.A. (1988). Neurotransmitter systems in the outer plexiform layer of mammalian retina. Neurochemical Research 8, 127136.Google ScholarPubMed
Redburn, D.A. & Mitchell, C.K. (1989). Darkness stimulates rapid synthesis and release of melatonin in rat retina. Visual Neuroscience 3, 391403.CrossRefGoogle ScholarPubMed
Richter, K., Grunz, H. & Dawid, I.E. (1988). Gene expression in the embryonic nervous system of Xenopus laevis. Proceedings of the National Academy of Sciences of the U.S.A. 85, 80868090.CrossRefGoogle ScholarPubMed
Saha, M.S. & Grainger, R.M. (1993). Early opsin expression in Xenopus embryos precedes photoreceptor differentiation. Molecular Brain Research 17, 307318.CrossRefGoogle ScholarPubMed
Sale, W.S., Besharse, J.C. & Piperno, G. (1988). Distribution of acetylated a-tubulin in retina and in in vitro-assembled microtubules. Cell Motility and the Cytoskeleton 9, 243253.CrossRefGoogle Scholar
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edition. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Sandell, J.H. & Masland, R.H. (1989). Indoleamine accumulation by retinal neurons exposed to blood. Histochemistry 92, 5760.CrossRefGoogle ScholarPubMed
Schutte, M. & Witkovsky, P. (1990). Serotonin-like immunoreactivity in the retina of the clawed frog Xenopus laevis. Journal of Neurocytology 19, 504518.CrossRefGoogle ScholarPubMed
Sitaram, B.R. & Lees, G.J. (1978). Diurnal rhythm and turnover of tryptophan hydroxylase in the pineal gland of the rat. Journal of Neurochemistry 31, 10211026.CrossRefGoogle ScholarPubMed
Thomas, P.S. (1980). Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proceedings of the National Academy of Sciences of the U.S.A. 77, 52015205.CrossRefGoogle ScholarPubMed
Thomas, K.B. & Iuvone, P.M. (1991). Circadian rhythm of tryptophan hydroxylase activity in chicken retina. Cellular and Molecular Neurobiology 11, 511527.CrossRefGoogle ScholarPubMed
Thomas, K.B., Tigges, M. & Iuvone, P.M. (1993). Melatonin synthesis and circadian tryptophan hydroxylase activity in chicken retina following destruction of serotonin immunoreactive amacrine and bipolar cells by kainic acid. Brain Research 601, 303307.CrossRefGoogle ScholarPubMed
Tornqvist, K., Hansson, Ch. & Ehinger, B. (1983). Immunohistochemical and quantitative analysis of 5-hydroxytryptamine in the retina of some vertebrates. Neurochemistry International 5, 299308.CrossRefGoogle ScholarPubMed
Weiler, R. & Schutte, M. (1985). Kainic acid-induced release of serotonin from OFF-bipolar cells in the turtle retina. Brain Research 360, 379383.CrossRefGoogle ScholarPubMed
Wiechmann, A.F. & Craft, C.M. (1993). Localization of mRNA encoding the indolamine synthesizing enzyme, hydroxyindole-O-methyltransferase, in chicken pineal gland and retina by in situ hybridization. Neuroscience Letters 150, 207211.CrossRefGoogle ScholarPubMed
Wilhelm, M., Zhu, B., Gábriel, R. & Straznicky, C. (1993). Immunocytochemical identification of serotonin-synthesizing neurons in the vertebrate retina: A comparative study. Experimental Eye Research 56, 231240.CrossRefGoogle ScholarPubMed
Witkovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholamineand indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217225.CrossRefGoogle Scholar
Zawilska, J.B. & Iuvone, P.M. (1992). Melatonin synthesis in chicken retina: Effect of kainic acid-induced lesions on the diurnal rhythm and D2 dopamine receptor-mediated regulation of serotonin N-acetyltransferase activity. Neuroscience Letters 135, 7174.CrossRefGoogle ScholarPubMed
Zhu, B., Gábriel, R. & Straznicky, C. (1992). Serotonin synthesis and accumulation by neurons of the anuran retina. Visual Neuroscience 9, 377388.CrossRefGoogle ScholarPubMed
Zhu, B. & Straznicky, C. (1992). Large serotonin-like immunoreactive amacrine cells in the retina of developing Xenopus laevis. Developmental Brain Research 69, 109116.CrossRefGoogle ScholarPubMed
Zhu, B. & Straznicky, C. (1993). Co-localization of serotonin and GABA in neurons of the Xenopus laevis retina. Anatomy and Embryology 187, 549555.CrossRefGoogle ScholarPubMed