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Cellular and Molecular Neurobiology

, Volume 11, Issue 5, pp 529–560 | Cite as

Rhythmic regulation of retinal melatonin: Metabolic pathways, neurochemical mechanisms, and the ocular circadian clock

  • Gregory M. Cahill
  • Michael S. Grace
  • Joseph C. Besharse
Article

Summary

  1. 1.

    Current knowledge of the mechanisms of circadian and photic regulation of retinal melatonin in vertebrates is reviewed, with a focus on recent progress and unanswered questions.

     
  2. 2.

    Retinal melatonin synthesis is elevated at night, as a result of acute suppression by light and rhythmic regulation by a circadian oscillator, or clock, which has been localized to the eye in some species.

     
  3. 3.

    The development of suitablein vitro retinal preparations, particularly the eyecup from the African clawed frog,Xenopus laevis, has enabled identification of neural, cellular, and molecular mechanisms of retinal melatonin regulation.

     
  4. 4.

    Recent findings indicate that retinal melatonin levels can be regulated at multiple points in indoleamine metabolic pathways, including synthesis and availability of the precursor serotonin, activity of the enzyme serotoninN-acetyltransferase, and a novel pathway for degradation of melatonin within the retina.

     
  5. 5.

    Retinal dopamine appears to act through D2 receptors as a signal for light in this system, both in the acute suppression of melatonin synthesis and in the entrainment of the ocular circadian oscillator.

     
  6. 6.

    A recently developedin vitro system that enables high-resolution measurement of retinal circadian rhythmicity for mechanistic analysis of the circadian oscillator is described, along with preliminary results that suggest its potential for elucidating general circadian mechanisms.

     
  7. 7.

    A model describing hypothesized interactions among circadian, neurochemical, and cellular mechanisms in regulation of retinal melatonin is presented.

     

Key words

Melatonin retina circadian rhythm serotoninN-acetyltransferase tryptophan hydroxylase melatonin deacetylase D2 dopamine receptor cyclic AMP 

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References

  1. Avendano, G., Butler, B. J., and Iuvone, P. M. (1989). K+-Evoked depolarization induces serotonin N-acetyltransferase activity in photoreceptor-enriched retinal cell cultures. Involvement of calcium influx through L-type channels.Neurochem. Int. 17117–126.Google Scholar
  2. Axelrod, J. (1974). The pineal gland: A neurochemical transducer.Science 1841341–1348.Google Scholar
  3. Baker, P. C., Quay, W. B., and Axelrod, J. (1965). Development of hydroxyindole-O-methyltransferase activity in eye and brain of the amphibian,Xenopus laevis.Life Sci. 41981–1987.Google Scholar
  4. Baldridge, W. H., Ball, A. K., and Miller, R. G. (1987). Dopaminergic regulation of horizontal cell gap junction particle density in goldfish retina.J. Comp. Neurol. 265428–436.Google Scholar
  5. Baldridge, W. H., Ball, A. K., and Miller, R. G. (1989). Gap junction particle density of horizontal cells in goldfish retinas lesioned with 6-OHDA.J. Comp. Neurol. 287238–246.Google Scholar
  6. Balemans, M. G. M., Pévet, P., van Benthem, J., Haldar-Misra, C., Smith, I., and Hendriks, H. (1983). Day/night rhythmicity in the methylating capacities for different 5-hydroxyindoles in the pineal, the retina and the Harderian gland of the golden hamster (Mesocricetus auratus) during the annual seasons.J. Neural Transm. 5653–72.Google Scholar
  7. Bauer, B., Ehinger, B., and Aberg, L. (1980). (3H)-Dopamine release from the rabbit retina.Albrecht Von Graefes Arch. Klin. Exp. Ophthalmol. 21571–78.Google Scholar
  8. Beck, O., and Jonsson, G. (1981). In vivo formation of 5-methoxytryptamine from melatonin in rat.J. Neurochem. 362013–2018.Google Scholar
  9. Beck, O., and Pévet, P. (1984). Analysis of melatonin, 5-methoxytryptophol and 5-methoxyindoleacetic acid in the pineal gland and retina of hamster by capillary column gas chromatography-mass spectrometry.J. Chromatogr. 3111–8.Google Scholar
  10. Besharse, J. C. (1982). The daily light-dark cycle and rhythmic metabolism in the photoreceptor-pigment epithelial complex.Prog. Retinal Res. 181–124.Google Scholar
  11. Besharse, J. C., and Dunis, D. A. (1983a). Methoxyindoles and photoreceptor metabolism: activation of rod sheddingScience 2191341–1343.Google Scholar
  12. Besharse, J. C., and Dunis, D. A. (1983b). Rod photoreceptor disc shedding in eye cups: Relationship to bicarbonate and amino acids.Exp. Eye Res. 36567–580.Google Scholar
  13. Besharse, J. C., and Iuvone, P. M. (1983). Circadian clock inXenopus eye controlling retinal serotonin N-acetyltransferase.Nature 305133–135.Google Scholar
  14. Besharse, J. C., Terrill, R. O., and Dunis, D. A. (1980). Light-evoked disc shedding by rod photoreceptors in vitro: Relationship to medium bicarbonate concentration.Invest. Ophthalmol. Vis. Sci. 191512–1517.Google Scholar
  15. Besharse, J. C., Dunis, D. A., and Iuvone, P. M. (1984). Regulation and possible role of serotonin N-acetyltransferase in the retina.Fed. Proc. 432704–2708.Google Scholar
  16. Besharse, J. C., Iuvone, P. M., and Pierce, M. E. (1988). Regulation of rhythmic photoreceptor metabolism: A role for post-receptoral neurons.Prog. Retinal Res. 721–61.Google Scholar
  17. Binkley, S., Macbride, S. E., Klein, D. C., and Ralph, C. L. (1973). Pineal enzymes: Regulation of avian melatonin synthesis.Science 181273–275.Google Scholar
  18. Binkley, S., Hryshchyshyn, M., and Reilly, K. (1979). N-Acetyltransferase activity responds to environmental lighting in the eye as well as in the pineal gland.Nature 281479–481.Google Scholar
  19. Binkley, S., Reilly, K. B., and Hryshchyshyn, M. (1980a). N-Acetyltransferase in the chick retina I. Circadian rhythms controlled by environmental lighting are similar to those in the pineal gland.J. Comp. Physiol. [B]139103–108.Google Scholar
  20. Binkley, S., Reilly, K., and Hernandez, T. (1980b). N-Acetyltransferase in the chick retina II. Interactions of the eyes and pineal gland in response to light.J. Comp. Physiol. [B]140181–183.Google Scholar
  21. Block, G. D., and Khalsa, S. B. S. (1988). Cellular basis of circadian rhythmicity inBulla: A model system.Adv. Biosci. 7355–66.Google Scholar
  22. Boatright, J. H., and Iuvone, P. M. (1989a). GABA and the regulation of serotonin N-acetyltransferase activity in amphibian retina—I. Effects of GABA agonists and antagonists.Neurochem. Int. 15541–547.Google Scholar
  23. Boatright, J. H., and Iuvone, P. M. (1989b). GABA and the regulation of serotonin N-acetyltransferase activity in amphibian retina—II. The role of dopamine.Neurochem. Int. 15549–554.Google Scholar
  24. Boatright, J. H., Hoel, M. J., and Iuvone, P. M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light- and K+-evoked depolarization.Brain Res. 482164–168.Google Scholar
  25. Brann, M. R., and Jelsema, C. L. (1985). Dopamine receptors on photoreceptor membranes couple to a GTP-binding protein which is sensitive to both pertussis and cholera toxin.Biochem. Biophys. Res. Commun. 133222–227.Google Scholar
  26. Brann, M. R., and Young, W. S. (1986). Dopamine receptors are located on rods in bovine retina.Neurosci. Lett. 69221–226.Google Scholar
  27. Bubenik, G. A., Brown, G. M., Uhlir, I., and Grota, L. J. (1974). Immunohistological localization of N-acetylindole-alkylamines in pineal gland, retina and cerebellum.Brain Res. 81233–242.Google Scholar
  28. Bubenik, G. A., Brown, G. M., and Grota, L. J. (1976). Differential localization of N-acetylated indolealkylamines in CNS and the Harderian gland using immunohistology.Brain Res. 118417–427.Google Scholar
  29. Bubenik, G. A., Purtill, R. A., Brown, G. M., and Grota, L. J. (1978). Melatonin in the retina and the Harderian gland. Ontogeny, diurnal variations, and melatonin treatment.Exp. Eye Res. 27323–333.Google Scholar
  30. Bunzow, J. R., Van Tol, H. H. M., Grandy, D. K., Albert, P., Salon, J., Christie, M., Machida, C. A., Neve, K. A., and Civelli, O. (1988). Cloning and expression of a rat D2 dopamine receptor cDNA.Nature 336783–787.Google Scholar
  31. Cahill, G. M., and Besharse, J. C. (1989a). A D-2 dopamine receptor agonist resets the phase of a circadian clock in cultured eyecups fromXenopus laevis.Soc. Neurosci. Abstr. 1524.Google Scholar
  32. Cahill, G. M., and Besharse, J. C. (1989b). Retinal melatonin is metabolized within the eye ofXenopus laevis.Proc. Natl. Acad. Sci. USA 861098–1102.Google Scholar
  33. Cahill, G. M., and Besharse, J. C. (1990). Circadian regulation of melatonin in the retina ofXenopus laevis: Limitation by serotonin availability.J. Neurochem. 54716–719.Google Scholar
  34. Cahill, G. M., and Besharse, J. C. (1991). Resetting the circadian clock in culturedXenopus eyecups: Regulation of retinal melatonin rhythms by light and D2 dopamine receptors.J. Neurosci. (in press).Google Scholar
  35. Cardinali, D. P., Larin, F., and Wurtman, R. J. (1972). Action spectra for effects of light on hydroxyindole-O-methyl transferase in rat pineal, retina and Harderian gland.Endocrinology 91877–886.Google Scholar
  36. Cardinali, D. P., and Rosner, J. M. (1971a). Metabolism of serotonin by the rat retina in vitro.J. Neurochem. 181769–1770.Google Scholar
  37. Cardinali, D. P., and Rosner, J. M. (1971b). Retinal localization of the hydroxyindole-O-methyl transferase (HIOMT) in the rat.Endocrinology 89301–303.Google Scholar
  38. Cardinali, D. P., and Rosner, J. M. (1972). Ocular distribution of hydroxyindole-O-methyl transferase (HIOMT) in the duck (Anas platyrhinchos).Gen. Comp. Endocrinol. 18407–409.Google Scholar
  39. Cardinali, D. P., and Wurtman, R. J. (1972). Hydroxyindole-O-methyl transferase in rat pineal, retina and Harderian gland.Endocrinology 91247–252.Google Scholar
  40. Cassone, V. M., Lane, R. F., and Menaker, M. (1986). Melatonin-induced increases in serotonin concentrations in specific regions of the chicken brain.Neuroendocrinology 4228–33.Google Scholar
  41. Chèze, G., and Ali, M. A. (1976). Röle de l'épiphyse dans la migration du pigment épithélial rétinien chez quelques Téléostéens.Can. J. Zool. 54475–481.Google Scholar
  42. Cogburn, L. A., Wilson-Placentra, S., and Letcher, L. R. (1987). Influence of pinealectomy on plasma and extrapineal melatonin rhythms in young chickens (Gallus domesticus).Gen. Comp. Endocrinol. 68343–356.Google Scholar
  43. Cohen, A. I., and Blazynski, C. (1987). Tryptamine and some related molecules block the accumulation of a light-sensitive pool of cyclic AMP in the dark-adapted, dark-incubated mouse retina.J. Neurochem. 48729–737.Google Scholar
  44. Cohen, J., Hadjiconstantinou, M., and Neff, N. H. (1983). Activation of dopamine-containing amacrine cells of retina: Light-induced increase of acidic dopamine metabolites.Brain Res. 260125–127.Google Scholar
  45. Da Prada, M. (1977). Dopamine content and synthesis in retina and N. accumbens septi: Pharmacological and light-induced modifications.Adv. Biochem. Psychopharmacol. 16311–319.Google Scholar
  46. Dearry, A., and Burnside, B. (1986a). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas. I. Induction of cone contraction is mediated by D2 receptors.J. Neurochem. 461006–1021.Google Scholar
  47. Dearry, A., and Burnside, B. (1986b). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas. II. Modulation by gamma-aminobutyric acid and serotonin.J. Neurochem. 461022–1031.Google Scholar
  48. Dearry, A., and Burnside, B. (1988). Stimulation of distinct D2 dopaminergic and alpha2-adrenergic receptors induces light-adaptive pigment dispersion in teleost retinal pigment epithelium.J. Neurochem. 511516–1523.Google Scholar
  49. Dearry, A., and Burnside, B. (1989). Light-induced dopamine release from teleost retinas acts as a light-adaptive signal to the retinal pigment epithelium.J. Neurochem. 53870–878.Google Scholar
  50. Delgado, M. J., and Vivien-Roels, B. (1989). Effect of environmental temperature and photoperiod on the melatonin levels in the pineal, lateral eye, and plasma of the frog,Rana perezi: Importance of ocular melatonin,Gen. Comp. Endocrinol,7546–53.Google Scholar
  51. de Montigny, C., and Aghajanian, G. K. (1977). Preferential action of 5-methoxytryptamine and 5-methoxydimethyltryptamine on presynaptic serotonin receptors: A comparative iontophoretic study with LSD and serotonin.Neuropharmacology 16811–818.Google Scholar
  52. Dowling, J. E. (1987).The Retina, An Approachable Part of the Brain, Belknap-Harvard, Cambridge, MA, pp. 124–163.Google Scholar
  53. Dubocovich, M. L. (1983). Melatonin is a potent modulator of dopamine release in the retina.Nature 306782–784.Google Scholar
  54. Dubocovich, M. L. (1988). Pharmacology and function of melatonin receptors.FASEB J. 22765–2773.Google Scholar
  55. Dubocovich, M. L., and Weiner, N. (1985). Pharmacological differences between the D-2 autoreceptor and D-1 dopamine receptor in rabbit retina.J. Pharmacol. Exp. Ther. 233747–754.Google Scholar
  56. Dubocovich, M. L., Lucas, R. C., and Takahashi, J. S. (1985). Light-dependent regulation of dopamine receptors in mammalian retina.Brain Res. 335321–325.Google Scholar
  57. Ehinger, B., and Rose, B. (1988). Diurnal variation in chick retinal 5-hydroxytryptamine.Exp. Eye Res. 46819–821.Google Scholar
  58. Eichler, V. B., and Moore, R. Y. (1975). Studies on hydroxyindole-O-methyl transferase in frog brain and retina: Enzymology, regional distribution and environmental control of enzyme levels.Comp. Biochem. Physiol. 50C89–95.Google Scholar
  59. Eskin, A., Corrent, G., Lin, C.-Y., and McAdoo, D. J. (1982). Mechanism for shifting the phase of a circadian rhythm by serotonin: Involvement of cAMP.Proc. Natl. Acad. Sci. USA 79660–664.Google Scholar
  60. Flight, W. F. G., Mans, D., and Balemans, M. G. M. (1983). Methoxyindole synthesis in the retina of the frog (Rana esculenta) during a diurnal period.J. Neural Transm. 58223–230.Google Scholar
  61. Florén, I., and Hansson, Ch. (1980). Investigations into whether 5-hydroxytryptamine is a neurotransmitter in the retina of rabbit and chicken.Invest. Ophthalmol, Vis. Sci. 19117–125.Google Scholar
  62. Foley, P. B., Cairncross, K. D., and Foldes, A. (1986). Pineal indoles: significance and measurement.Neurosci. Biobehav. Rev. 10273–293.Google Scholar
  63. Frederick, J. M., Rayborn, M. E., and Hollyfield, J. G. (1989). Serotoninergic neurons in the retina ofXenopus laevis: Selective staining, identification, development, and content.J. Comp. Neurol. 281516–531.Google Scholar
  64. Frucht, Y., Vidauri, J., and Melamed, E. (1982). Light activation of dopaminergic neurons in rat retina is mediated through photoreceptors.Brain Res. 249153–156.Google Scholar
  65. Gern, W. A., and Ralph, C. L. (1979). Melatonin synthesis by the retina.Science 204183–184.Google Scholar
  66. Gern, W. A., Owens, D. W., and Ralph, C. L. (1978). The synthesis of melatonin by the trout retina.J. Exp. Zool. 206263–270.Google Scholar
  67. Gern, W. A., Wechsler, E., and Duvall, D. (1984). Characteristics and non-rhythmicity of retinal hydroxyindole-O-methyltransferase activity in trout (Salmo gairdneri).Gen. Comp. Endocrinol. 53169–178.Google Scholar
  68. Gläsener, G., Schmidt, C., and Himstedt, W. (1988). Two populations of serotonin-immunoreactive neurons in the frog (Rana esculenta) retina.Neurosci. Lett. 84251–254.Google Scholar
  69. Godley, B. F., and Wurtman, R. J. (1988). Release of endogenous dopamine from the superfused rabbit retina in vitro: Effect of light stimulation,Brain Res. 452393–395.Google Scholar
  70. Grace, M. S., and Besharse, J. C. (1990). Development of a melatonin deacetylase assay usingXenopus laevis retina.Invest. Ophthalmol. Vis. Sci. Suppl. 316 (abstr.).Google Scholar
  71. Grace, M. S., Cahill, G. M., and Besharse, J. C. (1991). Melatonin deacetylation: Retinal vertebrate class distribution andXenopus laevis tissue distribution.Brain Res. (in press).Google Scholar
  72. Hamasaki, D. I., Trattler, W. B., and Hajek, A. S. (1986). Lighton depresses and lightoff enhances the release of dopamine from the cat's retina.Neurosci. Lett. 68112–116.Google Scholar
  73. Hamm, H. E., and Menaker, M. (1980). Retinal rhythms in chicks: Circadian variation in melatonin and serotonin N-acetyltransferase activity.Proc. Natl. Acad. Sci. USA 774998–5002.Google Scholar
  74. Hamm, H. E., Takahashi, J. S., and Menaker, M. (1983). Light-induced decrease of serotonin N-acetyltransferase activity and melatonin in the chicken pineal gland and retina.Brain Res. 266287–293.Google Scholar
  75. Harrison, N. L., and Zatz, M. (1989). Voltage-dependent calcium channels regulate melatonin output from cultured chick pineal cells,J. Neurosci. 92462–2467.Google Scholar
  76. Heward, C. B., and Hadley, M. E. (1976). Structure-activity relationships of melatonin and related indoleamines.Life Sci. 171167–1178.Google Scholar
  77. Hirata, F., Hayaishi, O., Tokuyama, T., and Senoh, S. (1974).In vitro andin vivo formation of two new metabolites of melatonin.J. Biol. Chem. 2491311–1313.Google Scholar
  78. Hsu, L. L. (1982). Brain aryl acylamidase.Int. J. Biochem. 141037–1042.Google Scholar
  79. Illnerová, H., Vanecek, J., and Hoffman, K. (1983). Regulation of the pineal melatonin concentration in the rat (Rattus norvegicus) and in the djungarian hamster (Phodopus sungorus).Comp. Biochem. Physiol. [A]74155–159.Google Scholar
  80. Ishita, S., Teranishi, T., Shimada, Y., and Kato, S. (1988). GABAergic inhibition on dopamine cells of the fish retina: A [3H]dopamine release study with isolated cell fractions.J. Neurochem. 501–6.Google Scholar
  81. Iuvone, P. M. (1984). Regulation of retinal dopamine biosynthesis and tyrosine hydroxylase activity by light.Fed. Proc, 432709–2713.Google Scholar
  82. Iuvone, P. M. (1986a). Evidence for a D2 dopamine receptor in frog retina that decreases cyclic-AMP accumulation and serotonin N-acetyltransferase activity.Life Sci. 38331–342.Google Scholar
  83. Iuvone, P. M. (1986b). Neurotransmitters and neuromodulators in the retina: Regulation, interactions, and cellular effects. InThe Retina, a Model for Cell Biological Studies, Part II (R. Adler and D. Farber, Eds.), Academic Press, New York, pp. 1–72.Google Scholar
  84. Iuvone, P. M. (1986c). Rhythms of melatonin biosynthesis in retina: Involvement of calcium, cyclic AMP and dopamine in the regulation of serotonin N-acetyltransferase. InPineal and Retinal Relationships, (P. J. O'Brien and D. C. Klein, Eds.), Academic Press, New York, pp. 197–218.Google Scholar
  85. Iuvone, P. M. (1988). Dopamine: A light-adaptive modulator of melatonin synthesis in the frog retina. InDopaminergic Mechanisms in Vision (I. Bodis-Wollner, Ed.), Alan R. Liss, New York, pp. 95–107.Google Scholar
  86. Iuvone, P. M., and Besharse, J. C. (1983). Regulation of indoleamine N-acetyltransferase activity in the retina: Effects of light and dark, protein synthesis inhibitors and cyclic nucleotide analogues.Brain Res. 273111–119.Google Scholar
  87. Iuvone, P. M., and Besharse, J. C. (1986a). Cyclic AMP stimulates serotonin N-acetyltransferase activity inXenopus retina in vitro.J. Neurochem. 4633–39.Google Scholar
  88. Iuvone, P. M., and Besharse, J. C. (1986b). Dopamine receptor-mediated inhibition of serotonin N-acetyltransferase activity in retina.Brain Res. 369168–176.Google Scholar
  89. Iuvone, P. M., and Besharse, J. C. (1986c). Involvement of calcium in the regulation of serotonin N-acetyltransferase in retina.J. Neurochem. 4682–88.Google Scholar
  90. Iuvone, P. M., Galli, C. L., Garisson-Gund, C. K., and Neff, N. H. (1978a). Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine neurons.Science 202901–902.Google Scholar
  91. Iuvone, P. M., Galli, C. L., and Neff, N. H. (1978b). Retinal tyrosine hydroxylase: Comparison of short-term and long-term stimulation by light.Mol. Pharmacol. 141212–1219.Google Scholar
  92. Iuvone, P. M., Boatright, J. H., and Bloom, M. M. (1987). Dopamine mediates the light-evoked suppression of serotonin N-acetyltransferase activity in retina.Brain Res. 418314–324.Google Scholar
  93. Iuvone, P. M., Avendano, G., Butler, B. J., and Adler, R. (1990). Cyclic AMP-dependent induction of serotonin N-acetyltransferase activity in photoreceptor-enriched chick retinal cell cultures: Characterization and inhibition by dopamine.J. Neurochem. 55673–682.Google Scholar
  94. Janavs, J. L., Pierce, M. E., Barker, D., and Takahashi, J. S. (1989). Regulation of melatonin production in human retinoblastoma cells.Soc. Neurosci. Abstr. 151395.Google Scholar
  95. Kemali, M., Milici, N., and Kemali, D. (1986). Melatonin and LSD induce similar retinal changes in the frog.Biol. Psychiat. 21981–985.Google Scholar
  96. Klein, D. C. (1985). Photoneural regulation of the mammalian pineal gland. InPhotoperiodism, Melatonin and the Pineal Gland, Ciba Foundation Symposium 117 (D. Evered and S. Clark, Ed.), Pitmann, London, pp. 38–51.Google Scholar
  97. Klein, D. C., and Weller, J. L. (1970) Indole metabolism in the pineal gland: A circadian rhythm in N-acetyltransferase.Science 1691093–1095.Google Scholar
  98. Klein, D. C., Auerbach, D. A., Namboodiri, M. A. A., and Wheler, G. H. T. (1981). Indole metabolism in the mammalian pineal gland. InThe Pineal Gland: Anatomy and Biochemistry (R. Reiter, Ed.), CRC Press, Boca Raton, FL, pp. 199–227.Google Scholar
  99. Kopin, I. J., Pare, C. M. B., Axelrod, J., and Weissbach, H. (1961). The fate of melatonin in animals.J. Biol. Chem. 2363072–3075.Google Scholar
  100. Kramer, S. G. (1971). Dopamine: A retinal neurotransmitter. I. Retinal uptake, storage, and light-stimulated release of3H-dopamine in vivo.Invest. Ophthalmol. 10438–452.Google Scholar
  101. Kraus-Ruppert, R., and Lembeck, F. (1965). Die wirkung von melatonin auf die pigmentzellen der retina von fröschen.Pflugers Arch. 284160–168.Google Scholar
  102. Kveder, S., and McIsaac, W. M. (1961). The metabolism of melatonin (N-acetyl-5-methoxytryptamine) and 5-methoxytryptamine.J. Biol. Chem. 2363214–3220.Google Scholar
  103. Kyritsis, A. P., Wiechmann, A. F., Bok, D., and Chader, G. J. (1987). Hydroxyindole-O-methyltransferase in Y-79 human retinoblastoma cells: Effect of cell attachment.J. Neurochem. 481612–1616.Google Scholar
  104. Leone, R. M., and Silman, R. E. (1984). Melatonin can be differentially metabolized in the rat to produce N-acetylserotonin in addition to 6-hydroxymelatonin.Endocrinology 1141825–1832.Google Scholar
  105. Lerner, A. B., Case, J. D., and Heinzelman, R. V. (1959). Structure of melatonin.J. Am. Chem. Soc. 816084–6085.Google Scholar
  106. Lewy, A. J., Tetsuo, M., Markey, S. P., Goodwin, F. K., and Kopin, I. J. (1980). Pinealectomy abolishes plasma melatonin in the rat.J. Clin. Endocrinol. Metab. 50204–205.Google Scholar
  107. Marshburn, P. B., and Iuvone, P. M. (1981). The role of GABA in the regulation of dopamine/tyrosine hydroxylase-containing neurons of the rat retina.Brian Res. 214335–347.Google Scholar
  108. Melamed, E., Frucht, Y., Lemor, M., Uzzan, A., and Rosenthal, Y. (1984). Dopamine turnover in rat retina: A 24-hour light-dependent rhythm.Brain Res. 305148–151.Google Scholar
  109. Millar, T. J., Winder, C., Ishimoto, I., and Morgan, I. G. (1988). Putative serotonergic bipolar and amacrine cells in the chicken retina.Brain Res. 43977–87.Google Scholar
  110. Morgan, W. W., and Kamp, C. W. (1980). A GABAergic influence on the light-induced increase in dopamine turnover in the dark-adapted rat retina in vivo.J. Neurochem. 341082–1086.Google Scholar
  111. Nagle, C. A., Cardinali, D. P., and Rosner, J. M. (1972). Light regulation of rat retinal hydroxyindole-O-methyl transferase (HIOMT) activity.Endocrinology 91423–426.Google Scholar
  112. Namboodiri, M. A. A., Sugden, D., and Klein, D. C. (1983). 5-Hydroxytryptophan elevates serum melatonin.Science 221659–661.Google Scholar
  113. Namboodiri, M. A. A., Sugden, D., Klein, D. C., Tamarkin, L., and Mefford, I. N. (1985). Serum melatonin and pineal indoleamine metabolism in a species with a small day/night N-acetyltransferase rhythm.Comp. Biochem. Physiol. 80B731–736.Google Scholar
  114. O'Connor, P., Dorison, S. J., Watling, K., and Dowling, J. E. (1986). Factors affecting release of3H-dopamine from perfused carp retina.J. Neurosci. 61857–1865.Google Scholar
  115. Olcese, J., and Møller, M. (1989). Characterization of serotonin N-acetyltransferase activity in the retina of the Mongolian gerbil,Meriones unguiculates.Neurosci. Lett. 102235–240.Google Scholar
  116. Oommen, A., and Balasubramanian, A. S. (1978). Aryl acylamidase of monkey brain and liver: Response to inhibitors and relationship to acetylcholinesterase.Biochem. Pharmacol. 27891–895.Google Scholar
  117. Oommen, A., and Balasubramanian, A. S. (1979). Tissue-specific inhibition characteristics of aryl acylamidase and possible association of serotonin-sensitive aryl acylamidase with true cholinesterase.Ind. J. Biochem. Biophys. 16264–266.Google Scholar
  118. Osborne, N. N. (1984). Indoleamines in the eye with special reference to the serotonergic neurones of the retina.Prog. Retinal Res. 361–104.Google Scholar
  119. Osborne, N. N., Nesselhut, T., Nicholas, D. A., and Cuello, A. C. (1981). Serotonin: A transmitter candidate in the vertebrate retina.Neurochem. Int. 3171–176.Google Scholar
  120. Osborne, N. N., Nesselhut, T., Nicholas, D. A., Patel, S., and Cuello, A. C. (1982). Serotonin-containing neurones in vertebrate retinas.J. Neurochem. 391519–1528.Google Scholar
  121. Osol, G., Schwartz, B., and Foss, D. C. (1985). Effects of time, photoperiod, and pinealectomy on ocular and plasma melatonin concentrations in the chick.Gen. Comp. Endocrinol. 58415–420.Google Scholar
  122. Pang, S. F., and Yew, D. T. (1979). Pigment aggregation by melatonin in the retinal pigment epithelium and choroid of guinea pigs,Cavia porcellus.Experientia 35231–233.Google Scholar
  123. Pang, S. F., Yu, H. S., Suen, H. C., and Brown, G. M. (1980). Melatonin in the retina of rats: A diurnal rhythm.J. Endocrinol,8789–93.Google Scholar
  124. Pang, S. F., Yu, H. S., and Tang, P. L. (1982). Regulation of melatonin in the retinae of guinea pigs: Effects of environmental lighting.J. Exp. Zool. 22211–15.Google Scholar
  125. Pang, S. F., Chow, P. H., Wong, T. M., and Tso, E. C. F. (1983). Diurnal variations of melatonin and N-acetylserotonin in the tissues of quails (Coturnix sp.), pigeons (Columba livia), and chickens (Gallus domesticus).Gen. Comp. Endocrinol. 511–7.Google Scholar
  126. Pang, S. F., Shiu, S. Y. W., and Tse, S. F. (1985). Effect of photic manipulation on the level of melatonin in the retinas of frogs (Rana tigrina regulosa).Gen. Comp. Endocrinol. 58464–470.Google Scholar
  127. Parkinson, D., and Rando, R. R. (1981). Evidence for a neurotransmitter role for 5-hydroxytryptamine in chick retina.J. Neurosci. 11211–1217.Google Scholar
  128. Parkinson, D., and Rando, R. R. (1983a). Effects of light on dopamine metabolism in the chick retina.J. Neurochem. 4039–46.Google Scholar
  129. Parkinson, D., and Rando, R. R. (1983b). Effect of light on dopamine turnover and metabolism in rabbit retina.Invest. Ophthalmol. Vis. Sci. 24384–388.Google Scholar
  130. Pelham, R. W. (1975). A serum melatonin rhythm in chickens and its abolition by pinealectomy.Endocrinology 96543–546.Google Scholar
  131. Pévet, P., Balemans, M. G. M., Bary, F. A. M., and Noordegraaf, E. M. (1978). The pineal gland of the mole (Talpa europaea, L.) V) Activity of hydroxyindole-O-methyl transferase (HIOMT) in the formation of melatonin/5-methoxytryptophol in the eyes and the pineal gland.Ann. Biol. Anim. Bioch. Biophys. 18259–264.Google Scholar
  132. Pévet, P., Balemans, M. G. M., Legerstee, W. C., and Vivien-Roels, B. (1980). Circadian rhythmicity of the activity of hydroxyindole-O-methyl transferase (HIOMT) in the formation of melatonin and 5-methoxytryptophol in the pineal, retina, and Harderian gland of the golden hamster.J. Neural Transm. 49229–245.Google Scholar
  133. Pévet, P., Balemans, M. G. M., and Reuver, G. F. (1981). The pineal gland of the mole (Talpa europaea L). VII. Activity of hydroxyindole-O-methyltransferase (HIOMT) in the formation of 5-methoxtryptophan, 5-methoxytryptamine, 5-methoxyindole-3-acetic acid, 5-methoxytryptophol and melatonin in the eyes and the pineal gland.J. Neural Transm. 51217–282.Google Scholar
  134. Pierce, M. E., and Besharse, J. C. (1985). Circadian regulation of retinomotor movements. I. Interaction of melatonin and dopamine in the control of cone length.J. Gen. Physiol. 86671–689.Google Scholar
  135. Pierce, M. E., and Besharse, J. C. (1986). Melatonin and dopamine interactions in the regulation of rhythmic photoreceptor metabolism. InPineal and Retinal Relationships (P. J. O'Brien, and D. C. Klein, Eds.), Academic Press, New York, pp. 219–237.Google Scholar
  136. Pierce, M. E., and Besharse, J. C. (1987). Melatonin and rhythmic photoreceptor metabolism: Melatonin-induced cone elongation is blocked at high light intensity.Brain Res. 405400–404.Google Scholar
  137. Pierce, M. E., and Besharse, J. C. (1988). Circadian regulation of retinomotor movements. II. The role of GABA in the regulation of cone position.J. Comp. Neurol. 270279–287.Google Scholar
  138. Pierce, M. E., Barker, D., Harrington, J., and Takahashi, J. S. (1989). Cyclic AMP-dependent melatonin production in Y79 human retinoblastoma cells.J. Neurochem. 53307–310.Google Scholar
  139. Pittendrigh, C. S. (1981a). Circadian systems: General Perspective. InHandbook of Behavioral Neurobiology, Vol. 4. Biological Rhythms (J. Aschoff, Ed.), Plenum, New York, pp. 57–80.Google Scholar
  140. Pittendrigh, C. S. (1981b). Circadian systems: Entrainment. InHandbook of Behavioral Neurobiology, Vol. 4. Biological Rhythms (J. Aschoff, Ed.), Plenum, New York, pp. 95–124.Google Scholar
  141. Pulido, O., and Clifford, J. (1986). Age-associated changes in the circadian rhythm of retinal N-acetylserotonin and melatonin in rats with pigmented eyes.Exp. Gerontol. 2123–30.Google Scholar
  142. Qu, Z.-X., Fertel, R., Neff, N. H., and Hadjiconstantinou, M. (1989). Pharmacological characterization of rat retinal dopamine receptors.J. Pharmacol. Exp. Ther. 248621–625.Google Scholar
  143. Quay, W. B. (1965). Retinal and pineal hydroxyindole-O-methyl transferase activity in vertebrates.Life Sci. 4983–991.Google Scholar
  144. Redburn, D. A. (1985). Serotonin neurotransmitter systems in vertebrate retina. InRetinal Transmitters and Modulators: Models for the Brain (W. W. Morgan, Ed.), CRC Press, Boca Raton, FL, pp. 107–122.Google Scholar
  145. Redburn, D. A., and Churchill, L (1987). An indoleamine system in photoreceptor cell terminals of the Long-Evans rat retina.J. Neurosci. 7319–329.Google Scholar
  146. Redburn, D. A., and Mitchell, C. K. (1989). Darkness stimulates rapid synthesis and release of melatonin in rat retina.Vis. Neurosci. 3391–403.Google Scholar
  147. Reiter, R. J., Richardson, B. A., and Hurlbut, E. C. (1981). Pineal, retinal and Harderian gland melatonin in a diurnal species, the Richardson's ground squirrel (Spermophilus richardsonii).Neurosci. Lett. 22285–288.Google Scholar
  148. Reiter, R. J., Richardson, B. A., Matthews, S. A., Lane, S. J., and Ferguson, B. N. (1983). Rhythms in immunoreactive melatonin in the retina and Harderian gland of rats: Persistence after pinealectomy.Life Sci. 321229–1236.Google Scholar
  149. Reppert, S. M., and Sagar, S. M. (1983). Characterization of the day-night variation of retinal melatonin content in the chick.Invest. Ophthalmol. Vis. Sci. 24294–300.Google Scholar
  150. Rogawski, M. A., Roth, R. H., and Aghajanian, G. K. (1979). Melatonin: Deacetylation to 5-methoxytryptamine by liver but not brain aryl acylamidase.J. Neurochem. 321219–1226.Google Scholar
  151. Sarthy, P. V., Rayborn, M. E., Hollyfield, J. G., and Lam, D. M. K. (1981). The emergence, localization, and maturation of neurotransmitter systems during development of the retina inXenopus laevis. III. Dopamine.J. Comp. Neurol. 195595–602.Google Scholar
  152. Stoof, J., and Kebabian, J. W. (1984). Two dopamine receptors: Biochemistry, physiology, and pharmacology.Life Sci. 352281–2296.Google Scholar
  153. Stormann, T. M., Gdula, D. C., Weiner, D. M., and Brann, M. R. (1990). Molecular cloning and expression of a dopamine D2 receptor from human retina.Mol. Pharmacol. 371–6.Google Scholar
  154. Takahashi, J. S., Hamm, H., and Menaker, M. (1980). Circadian rhythms of melatonin release from individual superfused chicken pineal glands in vitro.Proc. Natl. Acad. Sci. USA 772319–2322.Google Scholar
  155. Takahashi, J. S., Murakami, N., Nikaido, S. S., Pratt, B. L., and Robertson, L. M. (1989). The avian pineal, a vertebrate model system of the circadian oscillator: Cellular regulation of circadian rhythms by light, second messengers, and macromolecular synthesis.Recent Prog. Horm. Res. 45279–352.Google Scholar
  156. Thomas, K. B., and Iuvone, P. M. (1989). Tryptophan hydroxylase activity in chicken retina and pineal gland displays circadian rhythmicity.Soc. Neurosci. Abstr. 151396.Google Scholar
  157. Todd, R. D., Khurana, T. S., Sajovic, P., Stone, K. R., and O'Malley, K. L. (1989). Cloning of ligand-specific cell lines via gene transfer: Identification of a D2 dopamine receptor subtype.Proc. Natl. Acad. Sci. USA 8610134–10138.Google Scholar
  158. Tornqvist, K., Hansson, Ch., and Ehinger, B. (1983). Immunohistochemical and quantitative analysis of 5-hydroxytryptamine in the retina of some vertebrates.Neurochem. Int. 5299–308.Google Scholar
  159. Tsang, C. W., Chan, S. F., Lee, P. P. N., and Pang, S. F. (1989). Mass spectrometric identification and quantification of 5-methoxytryptophol in quail retina.Biochem. Biophys. Res. Commun. 1651331–1336.Google Scholar
  160. Underwood, H., and Siopes, T. (1985). Melatonin rhythms in quail: Regulation by photoperiod and circadian pacemakers.J. Pineal Res. 2133–143.Google Scholar
  161. Underwood, H., Binkley, S., Siopes, T., and Mosher, K. (1984). Melatonin rhythms in the eyes, pineal bodies, and blood of japanese quail (Coturnix coturnix japonica).Gen. Comp. Endocrinol. 5670–81.Google Scholar
  162. Underwood, H., Siopes, T., and Barrett, R. K. (1988). Does a biological clock reside in the eye of quail?J. Biol. Rhythms 3323–331.Google Scholar
  163. Vakkuri, O., Rintamäki, H., and Leppäluoto, J. (1985). Plasma and tissue concentrations of melatonin after midnight light exposure and pinealectomy in the pigeon.J. Endocrinol. 105263–269.Google Scholar
  164. Vakkuri, O., Tervo, J., Luttinen, R., Ruotsalainen, H., Rahkamaa, E., and Leppäluoto, J. (1987). A cyclic isomer of 2-hydroxymelatonin: a novel metabolite of melatonin.Endocrinology 1202453–2459.Google Scholar
  165. Vivien-Roels, B., Pévet, P., Dubois, M. P., Arendt, J., and Brown, G. M. (1981). Immunohistochemical evidence for the presence of melatonin in the pineal gland, the retina and the Harderian gland.Cell Tissue Res. 217105–115.Google Scholar
  166. Voisin, P., Guerlotté, J., and Collin, J.-P. (1988). An antiserum against chicken hydroxyindole-O-methyltransferase reacts with the enzyme from pineal gland and retina and labels pineal modified photoreceptors.Mol. Brain Res. 453–61.Google Scholar
  167. Wainwright, S. D. (1979). Development of hydroxyindole-O-methyl transferase activity in the retina of the chick embryo and young chick.J. Neurochem. 321099–1101.Google Scholar
  168. Weiler, R., and Schütte, M. (1985). Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of a turtle,Pseudemys scripta elegans.Cell Tissue Res. 241373–382.Google Scholar
  169. Weiler, R., Kohler, K., Kirsch, M., and Wagner, H. (1988). Glutamate and dopamine modulate synaptic plasticity in horizontal cell dendrites of fish retina.Neurcsci. Lett. 87205–209.Google Scholar
  170. Wiechmann, A. F. (1986). Melatonin: Parallels in pineal gland and retina.Exp. Eye Res. 42507–527.Google Scholar
  171. Wiechmann, A. F., and 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.J. Comp. Neurol. 258253–266.Google Scholar
  172. Wiechmann, A. F., and Hollyfield, J. G. (1989). HIOMT-like immunoreactivity in the vertebrate retina: A species comparison.Exp. Eye Res. 491079–1095.Google Scholar
  173. Wiechmann, A. F., and O'Steen, W. K. (1990). Hydroxyindole-O-methyltransferase in rat retinal bipolar cells: Persistence following photoreceptor destruction.Brain Res. 50614–18.Google Scholar
  174. Wiechmann, A. F., Bok, D., and Horwitz, J. (1985). Localization of hydroxyindole-O-methyltransferase in mammalian pineal gland and retina.Invest. Ophthalmol. Vis. Sci. 26253–265.Google Scholar
  175. Wiechmann, A. F., Bok, D., and Horwitz, J. (1986). Melatonin-binding in the frog retina: Autoradiographic and biochemical analysis.Invest. Ophthalmol. Vis. Sci. 27153–163.Google Scholar
  176. Wirz-Justice, A., Da Prada, M., and Remé, C. (1984). Circadian rhythm in rat retinal dopamine.Neurosci. Lett. 4521–25.Google Scholar
  177. Witkovsky, P., Eldred, W., and Karten, H. J. (1984). Catecholamine- and indoleamine-containing neurons in the turtle retina.J. Comp. Neurol. 228217–225.Google Scholar
  178. Witkovsky, P., Stone, S., and Besharse, J. C. (1988). Dopamine modifies the balance of rod and cone inputs to horizontal cells of theXenopus retina.Brain Res. 449332–336.Google Scholar
  179. Witkovsky, P., Stone, S., and Tranchina, D. (1989). Photoreceptor to horizontal cell synaptic transfer in theXenopus retina: Modulation by dopamine ligands and a circuit model for interactions of rod and cone inputs.J. Neurophysiol. 62864–881.Google Scholar
  180. Wurtman, R. J., and Ozaki, Y. (1978). Physiological control of melatonin synthesis and secretion: Mechanisms generating rhythms in melatonin, methoxytryptophol, and arginine vasotocin levels and effects on the pineal of endogenous catecholamines, the estrous cycle, and environmental lighting.J. Neural Transm. 4359–70.Google Scholar
  181. Yazulla, S. (1985). Evoked efflux of [3H]-GABA from goldfish retina in the dark.Brain Res. 325171–180.Google Scholar
  182. Yu, H. S., Pang, S. F., and Tang. P. L. (1981). Increase in the level of retinal melatonin and persistence of its diurnal rhythm in rats after pinealectomy.J. Endocrinol. 91477–481.Google Scholar
  183. Yu, H. S., Chow, P. H., Tang, P. L., and Pang, S. F. (1982). Effect of light and darkness on the in vitro release of N-acetylserotonin and melatonin by the retina of guinea pigs.Neuroendocrinology 34265–268.Google Scholar
  184. Zatz, M. (1989). Relationship between light, calcium influx and cAMP in the acute regulation of melatonin production by cultured chick pineal cells.Brain Res. 47714–18.Google Scholar
  185. Zatz, M., and Mullen, D. A. (1988). Does calcium influx regulate melatonin production through the circadian pacemaker in chick pineal cells? Effects of nitrendipine, Bay K 8644, Co2+, Mn2+ and low external Ca2+.Brain Res. 463305–316.Google Scholar
  186. Zatz, M., and Mullen, D. A. (1989). Photoendocrine transduction in cultured chick pineal cells. III. Ouabain (or dark) pulses can block, overcome, or alter the phase response of the melatonin rhythm to light pulses.Brain Res. 50146–57.Google Scholar
  187. Zawilska, J., and Iuvone, P. M. (1989). Catecholamine receptors regulating serotonin N-acetyltransferase activity and melatonin content of chicken retina and pineal gland: D2-dopamine receptors in retina andalpha 2-adrenergic receptors in pineal gland.J. Pharmacol. Exp. Ther. 25086–92.Google Scholar

Copyright information

© Plenum Publishing Corporation 1991

Authors and Affiliations

  • Gregory M. Cahill
    • 1
  • Michael S. Grace
    • 1
  • Joseph C. Besharse
    • 1
  1. 1.Department of Anatomy and Cell BiologyThe University of Kansas Medical CenterKansas CityUSA

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