Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-05T15:43:01.422Z Has data issue: false hasContentIssue false
  • English
  • Français

Light-sensitive melatonin synthesis by Xenopus photoreceptors after destruction of the inner retina

Published online by Cambridge University Press:  02 June 2009

Gregory M. Cahill  and
Joseph C. Besharse
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
Get access Rights & Permissions [Opens in a new window]

Abstract

Several lines of evidence indicate that retinal photoreceptors produce melatonin. However, there are other potential melatonin sources in the retina, and melatonin synthesis can be regulated by feedback from the inner retina. To analyze cellular mechanisms of melatonin regulation in retinal photoreceptors, we have developed an in vitro method for destruction of the inner retina that preserves functional photoreceptors in contact with the pigment epithelium. Eyecups, which include the neural retina, retinal pigment epithelium, choroid, and sclera were prepared. The vitreal surface of the retina in each eyecup was washed sequentially with 1% Triton X-100, water, and culture medium. This lysed the ganglion cells and neurons and glia of the inner nuclear layer, causing the retina to split apart within the inner nuclear layer. The damaged inner retina was peeled away, leaving photoreceptors attached to the pigment epithelium. The cell density of the inner nuclear layer was reduced 94% by this method, but there was little apparent damage to the photoreceptors. Lesioned eyecups produced normal melatonin levels in darkness at night, and melatonin production was inhibited by light. These results indicate that the inner retina is not necessary for melatonin production nor for regulation of photoreceptor melatonin synthesis by light. The lesion method used in this study may be useful for other physiological and biochemical studies of photoreceptors.

Keywords

RetinaPhotoreceptorMelatoninCircadianLight
Type
Short Communication
Information
Visual Neuroscience , Volume 8 , Issue 5 , May 1992 , pp. 487 - 490
Copyright
Copyright © Cambridge University Press 1992

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

Axelrod, J. & Weissbach, H. (1959). Enzymatic O-methylation of N-acetylserotonin to melatonin. Science 131, 1312.CrossRefGoogle Scholar
Besharse, J.C. & Dunis, D.A. (1983). Methoxyindoles and photoreceptor metabolism: Activation of rod shedding. Science 219, 1341–1343.CrossRefGoogle ScholarPubMed
Besharse, J.C. & Iuvone, P.M. (1983). Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature 305, 133–135.CrossRefGoogle ScholarPubMed
Besharse, J.C., Iuvone, P.M. & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: A role for post-receptoral neurons. Progress in Retinal Research 7, 21–61.CrossRefGoogle Scholar
Besharse, J.C. & Spratt, G. (1988). Excitatory amino acids and rod photoreceptor disc shedding: Analysis using specific agonists. Experimental Eye Research 47, 609–620.CrossRefGoogle ScholarPubMed
Binkley, S., Hryshchyshyn, M. & Reilly, K. (1979). N-acetyltransferase activity responds to environmental lighting in the eye as well as in the pineal gland. Nature 281, 479–481.CrossRefGoogle ScholarPubMed
Boatright, J.H. & Iuvone, P.M. (1989 a). GABA and the regulation of serotonin N-acetyltransferase activity in amphibian retina – I. Effects of GABA agonists and antagonists. Neurochemistry International 15, 541–547.CrossRefGoogle ScholarPubMed
Boatright, J.H. & Iuvone, P.M. (1989 b). GABA and the regulation of serotonin N-acetyltransferase activity in amphibian retina – II. The role of dopamine. Neurochemistry International 15, 549–554.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, 417–427.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
Cahill, G.M. & Besharse, J.C. (1991a). Is the ocular circadian clock located in photoreceptors? Society for Neuroscience Abstracts 17, 1240.Google Scholar
Cahill, G.M. & Besharse, J.C. (1991b). Resetting the circadian clock in cultured Xenopus eyecups: Regulation of retinal melatonin rhythms by light and D2 dopamine receptors. Journal of Neuroscience 11, 2959–2971.CrossRefGoogle ScholarPubMed
Cahill, G.M., Grace, M.S. & Besharse, J.C. (1991). Rhythmic regulation of retinal melatonin: Metabolic pathways, neurochemical mechanisms and the ocular circadian clock. Cellular and Molecular Neurobiology 11, 529–560.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. (1983). Melatonin is a potent modulator of dopamine release in the retina. Nature 306, 782–784.CrossRefGoogle ScholarPubMed
Hamm, H.E. & Menaker, M. (1980). Retinal rhythms in chicks: Circadian variation in melatonin and serotonin N-acetyltransferase activity. Proceedings of the National Academy of Sciences of the U.S.A. 77, 4998–5002.CrossRefGoogle ScholarPubMed
Hollyfield, J.G., Rayborn, M.E. & Landers, R.A. (1990). A technique for isolation of the photoreceptor layer from other neurons in the human retina. Experimental Eye Research 50, 335–338.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, 673–682.CrossRefGoogle ScholarPubMed
Iuvone, P.M., & Besharse, J.C. (1986). Dopamine receptor-mediated inhibition of serotonin N-acetyltransferase activity in retina. Brain Research 369, 168–176.CrossRefGoogle ScholarPubMed
Johnson, L.V. & Hageman, G.S. (1989). Characterization of isolated cone matrix sheath substructure. Investigative Ophthalmology and Visual Science (Suppl.) 30, 490.Google Scholar
Johnson, L.V. & Hageman, G.S. (1991). Structural and compositional analyses of isolated cone matrix sheaths. Investigative Ophthalmology and Visual Science 32, 1951–1957.Google ScholarPubMed
Miller, A.M. & Schwartz, E.A. (1983). Evidence for the identification of synaptic transmitters released by photoreceptors of the toad retina. Journal of Physiology 334, 325–349.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
Rollag, M.D. & Niswender, G.D. (1976). Radioimmunoassay of serum concentrations of melatonin in sheep exposed to different lighting regimens. Endocrinology 98, 482–489.CrossRefGoogle ScholarPubMed
Wiechmann, A.G., Bok, D. & Horwitz, J. (1985). Localization of hydroxyindole-O-methyltransferase in the mammalian pineal gland and retina. Investigative Ophthalmology and Visual Science 26, 253–265.Google 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
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, 71–74.CrossRefGoogle ScholarPubMed