Summary
By means of radioimmunoassay a clear-cut peak of melatonin concentration was found in the pineal organ of the pigeon at the middle of the scotophase (Voisin et al. 1982a). The aim of the present study was to identify the cell type responsible for the nocturnal indole metabolism, including melatonin synthesis, in the pineal of this avian species. After a short-term incubation or organ culture in the presence of [3H]-indolic precursors, [3H]-5-hydroxytryptophan or [3H]-5-hydroxytryptamine, the relative amounts of deaminated and acetylated products occurring in the pineal organ were measured by the use of thin layer chromatography and liquid-scintillation counting. It was possible to modify the relative amounts of deaminated and acetylated indoles by the application of some inhibitors of monoamine oxidase and cyclic nucleotide phosphodiesterase. Irrespective of the experimental conditions, high-resolution autoradiography combined with the above-mentioned radiochemical experiments showed that the cells of the receptor line (modified photoreceptor cells) are responsible for indole storage and metabolism, and very probably also for melatonin biosynthesis. The other cell types of the pineal parenchyma did not display significant labeling.
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References
Balemans M (1981) Indole metabolism in the pineal gland, the harderian gland and the retina of mammals. In: Oksche A, Pévet P (eds) The pineal organ: Photobiology, biochronometry, endocrinology. Developments in endocrinology, Vol 14, Elsevier/North-Holland Biomedical Press, Amsterdam 261–279
Balemans M, Juillard MT, Van Benthem J, Collin JP Retention and loss of exogenous [3H]-indoles during preparation of specimens for electron microscopic autoradiography: a study in the parakeet pineal organ (submitted for publication)
Binkley S, Riebman JB, Reilly K (1978) The pineal gland: a biological clock in vitro. Science 202:1198–1201
Collin JP, Calas A, Juillard MT (1976) The avian pineal organ. Distribution of exogenous indoleamines: a qualitative study of the rudimentary photoreceptor cells by electron microscopic radioautography. Exp Brain Res 25:15–33
Collin JP, Balemans M, Juillard MT, Legerstee WC, Van Benthem J, Voisin P (1982) Indole metabolism at the cellular level: an in vivo combined radiobiochemical and highresolution autoradiographic study in the avian pineal, with special reference to melatonin/5-methoxytryptophol. Biol Cell 44:25–34
Deguchi T (1979a) Circadian rhythm of serotonin N-acetyltransferase activity in organ culture of chicken pineal gland. Science 203:1245–1247
Deguchi T (1979b) Role of adenosine 3′,5′-monophosphate in the regulation of circadian oscillation of serotonin N-acetyltransferase activity in cultured chicken pineal gland. J Neurochem 33:45–51
Deguchi T (1979c) A circadian oscillator in cultured cells of chicken pineal gland. Nature 282:94–96
Gwinner E, Benzinger I (1978) Synchronization of a circadian rhythm in pinealectomized European starlings by daily injections of melatonin. J Comp Physiol 127:209–213
Juillard MT, Collin JP (1976) L'organe pineal aviaire: étude ultracytochimique et pharmacologique d'un “pool” granulaire de 5-hydroxytryptamine chez la Perruche (Melopsittacus undulatus, Shaw) J Microsc Biol Cell 26:133–138
Juillard MT, Hartwig HG, Collin JP (1977) The avian pineal organ. Distribution of endogenous monoamines; a fluorescence microscopic, microspectrofluorimetric and pharmacological study in the parakeet. J Neural Transm 40:269–287
Juillard MT, Balemans M, Collin JP, Legerstee WC, Van Benthem J 1983. An in vitro combined radiobiochemical and high resolution autoradiographic study predicating evidence for indolic cells in the avian pineal organ. Biol Cell 47 (in press)
Kasal CA, Menaker M, Perez-Polo JR (1979) Circadian clock in organ culture: N-acetyltransferase activity of chick pineal glands oscillates in vitro. Science 203:656–658
Klein DC, Notides A (1969) Thin layer chromatographic separation of pineal gland derivatives of serotonin-14C. Anal Biochem 31:480–483
Menaker M, Binkley S (1981) Neural and endocrine control of circadian rhythms in the vertebrates. In: Aschoff J (ed) “Handbook of behavioral neurobiology”, vol 4, Plenum Publishing Corporation, New York 243–255
Reiter RJ (1981) The pineal. Vol 6:209–212. Eden Press Inc., Montréal
Takahashi JS, Menaker M (1979) Physiology of avian circadian pacemakers. Fed Proc 38:2583–2588
Takahashi JS, Hamm H, Menaker M (1980) Circadian rhythms of melatonin release from individual superfused chicken pineal gland in vitro. Proc Natl Acad Sci USA 77:2319–2322
Ueck M (1973) Fluoreszenzmikroskopische und elektronenmikroskopische Untersuchungen am Pinealorgan verschiedener Vogelarten. Z Zellforsch 137:37–62
Voisin P (1982a) Les cellules de la lignée réceptrice dans l'épiphyse aviaire et le problème des horloges cellulaires. (Etude immunologique, autoradiographique et radiobiochimique). Thèse de 3ème cycle, Univ. Poitiers (n∘ 839)
Voisin P (1982b) Etude de l'épithélium épiphysaire du Pigeon dans les conditions naturelles et in vitro. Ultrastructure et mise en évidence histochimique d'hydroxyindoles dans les cellules de la lignée réceptrice. Arch Anat Micr Morphol Exper (in press)
Voisin P, Geffard M, Delaage M, Collin JP (1982a) Mélatonine dans l'organe pinéal, la rétine et le plasma. Etude immunologique chez le Pigeon. Reprod Nutr Dév 22:959–971
Voisin P, Juillard MT, Collin JP (1982b) Etude radioautographique de l'incorporation in vitro d'hydroxyindoles-[3H] et de melatonine-[3H] dans l'organe pinéal de Pigeon. Arch Anat Micr Morphol Exper (in press)
Wainwright SD (1977) Metabolism of tryptophan and serotonin by the chick pineal gland in organ culture. Can J Biochem 55:415–423
Wainwright SD (1980) Diurnal cycles in serotonin acetyltransferase activity and cyclic GMP content of cultured chick pineal glands. Nature 285:478–480
Wainwright SD, Wainwright LK (1978) Regulation of the diurnal cycle in activity of serotonin N-acetyltransferase in the chick pineal gland. Can J Biochem 56:685–690
Wurtman RJ, Larin F, Axelrod J, Shein HM, Rosasco K (1968) Formation of melatonin and 5-hydroxyindole acetic acid from 14C-tryptophan by rat pineal glands in organ culture. Nature 217:953–954
Yang HYT, Goridis C, Neff NH (1972) Properties of monoamine oxidases in sympathetic nerve and pineal gland. J Neurochem 19:1241–1250
Zenser TV, Craven PA, de Rubertis FR, Davis BB (1977) Differential inhibition of c-AMP and c-GMP hydrolysis in rat renal cortex. Arch Biochem Biophys 178:598–606
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A preliminary report on these findings was presented on the occasion of the “First European Congress on Cell Biology” (July 18–23, 1982, Paris), Biol. Cell. (1982) 45:143
Supported by grants from DGRST Paris (80.7.0330), the Fondation Langlois, Rennes, and by INSERM, Paris (79.1.539.4)
The authors are very grateful to Dr. M.G.M. Balemans (Utrecht, The Netherlands) for his critical reading of the manuscript. They also acknowledge the technical assistance of F. Chevalier and D. Decourt
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Voisin, P., Juillard, M.T. & Collin, J.P. Indole metabolism in the pineal organ of the pigeon with special reference to melatonin-synthesizing cells. Cell Tissue Res. 230, 155–169 (1983). https://doi.org/10.1007/BF00216036
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DOI: https://doi.org/10.1007/BF00216036