Summary
The day and night rhythms in the activity of HIOMT in the formation of melatonin and of 5-methoxytryptophol have been determined in the pineal, retina and Harderian gland of the adult male golden hamster.
In all hamsters used there was no detectable HIOMT activity in the deep pineal. In the superficial pineal HIOMT activity, involved in the synthesis of melatonin (Mel), was observed to be high at the end of the dark period and at the middle of the light period. Considering the HIOMT activity involved in the production of 5-methoxytryptophol (5-MTL), an increase in 5-MTL synthesis was observed only during the light period. Comparing the peak of Mel-production with that of 5-MTL it appears that during the light period the pineal produces more 5-MTL than Mel.
In the Harderian glands, the circadian course of HIOMT activity involved in the synthesis of Mel seems to run parallel to that of the enzyme implicated in 5-MTL synthesis, both being stimulated at the end of the dark period. The activity of HIOMT in 5-MTL production is, however, always approximately 2 times higher than for Mel synthesis.
In the retina the synthesis of Mel and 5-MTL is not significantly higher during the dark period than during the light period. However, the production of 5-MTL is larger than that of Mel.
It appears that (1) with the exception of the end of the dark period, the extra-pineal synthesis of Mel and 5-MTL is always higher than that in the pineal; (2) the circadian synthesis of 5-methoxyindoles is different in each organ, and (3) in the pineal the circadian activity of HIOMT involved in 5-MTL formation is different from that of the same enzyme involved in the formation of Mel. The results are discussed.
Similar content being viewed by others
References
Ariëns Kappers, J., Pévet, P.: The pineal gland of vertebrates including man. Progr. Brain Res.52 (1979).
Balemans, M. G. M. Age-dependent effects of 5-methoxytryptophol and melatonin on testes and comb growth of the white leghorn (Gallus domesticus, L.). J. Neural Transm.33, 179–194 (1972).
Balemans, M. G. M. The stimulatory effects of several concentrations of 5-methoxytryptophol on testicular growth in the white leghorn (Gallus domestkus, L.). J. Neural Transm.34, 49–60 (1973 a).
Balemans, M. G. M. The inhibitory effect of 5-methoxytryptophol on ovarian weight, follicular growth and egg production of adult white leghorn hens (Gallus domesticus, L.). J. Neural Transm.34, 159–169 (1973 b).
Balemans, M. G. M.: The pineal gland. A study on the presence and the biological significance of melatonin and 5-methoxytryptophol. Thesis, Utrecht, 1974.
Balemans, M. G. M., Bary, F. A. M., Legerstee, W. C.: Seasonal variations in HIOMT activity during the night in the pineal gland of rats of several ages. Melatonin Symposium, September 28–30, Bremen, Federal Republic of Germany (1980a).
Balemans, M. G. M., Legerstee, W. C., Van Benthem, J. Day and light rhythms in the methylation of N-acetylserotonin/5-hydroxytryptophol in the pineal gland of male rats of different ages. J. Neural Transm.45, 265–272 (1979).
Balemans, M. G. M., Noordegraaf, E. M., Bary, F. A. M., Van Berlo, M. F. Estimation of the methylating capacity of the pineal gland. With special reference to indole metabolism. Experientia (Basel)34, 887–888 (1978 a).
Balemans, M. G. M., Bary, F. A. M., Legerstee, W. C., Van Benthem, J. Estimation of the methylating capacity of the pineal gland of the rat with special reference to the methylation of N-acetylserotonin and 5-hydroxytryptophol separately. Experientia (Basel)34, 1434–1435 (1978 b).
Balemans, M. G. M., Pévet, P., Legerstee, W. C., Neva, E. Melatonin and 5-methoxytryptophol synthesis in the pineal, the retina and the Harderian gland of the mole-rat (Spalax ehrenbergi, Nehring) and in the pineal of the mouse “eyeless”. J. Neural Transm.49, 247–255 (1980 b).
Benson, B. Current status of pineal peptides. Neuroendocrinology24, 241 to 258 (1977).
Benson, B., Krasovich, M. Circadian rhythm in the number of granulated vesicles in the pinealocytes of mice. Effect of sympathectomy and melatonin treatment. Cell Tiss. Res.184, 499–506 (1977).
Berndtson, W. E., Desjardins, C. Circulating LH and FSH levels and testicular function in hamsters during light deprivation and subsequent photoperiodic stimulation. Endocrinology95, 195–199 (1974).
Bridges, R., Tamarkin, L., Goldman, B. Effects of photoperiod and melatonin on reproduction in the Syrian hamster. Ann. Biol. Anim. Biochem. Biophys.16, 399–408 (1976).
Cardinali, D. P., Rosner, J. M. Retinal localization of the hydroxyindole-O-methyltransferase (HIOMT) in the rat. Endocrinology89, 301–303 (1971).
Cardinali, D. P., Rosner, J. M. Ocular distribution of hydroxyindole-O-methyltransferase (HIOMT) in the duck (Anas platyrbincbos). Gen. comp. Endocrinol.18, 407–409 (1972).
Cardinali, D. P., Wurtman, R. J. Hydroxyindole-O-methyltransferase in rat pineal, retina and Harderian gland. Endocrinology91, 247–252 (1972).
Eichler, V. B., Moore, R. Y. Studies on hydroxyindole-O-methyltransferase in frog brain and retina: enzymology, regional distribution and environmental control of enzyme levels. Comp. Biochem. Physiol.50c, 89–95 (1975).
Flight, W. F. G.: On the pineal body of the urodele,Diemictylus viridescens. Thesis, Univ. of Utrecht, 1975.
Flight, W. F. G. Morphological and functional comparison between the retina and the pineal organ of lower vertebrates. In: The Pineal Gland of Vertebrates Including Man (Ariëns Kappers, J., Pévet, P., eds.), Progress in Brain Research, Vol. 52, pp. 131–139. Amsterdam: Elsevier/North-Holland Biomed. Press. 1979.
Freire, F., Cardinali, D. P. Effects of melatonin treatment and environmental lighting on the ultrastructural appearance, melatonin synthesis, norepinephrine turnover and microtubule protein content of the rat pineal gland. J. Neural Transm.37, 237–257 (1975).
Gern, W. A., Owens, D. W., Ralph, Ch. L. The synthesis of melatonin by the trout retina. J. exp. Zool.206, 263–269 (1978).
Hoffmann, K. Photoperiod, pineal, melatonin and reproduction in hamsters. In: The Pineal Gland of Vertebrates Including Man (Ariëns Kappers, J., Pévet, P., eds.), Progress in Brain Research, Vol. 52, pp. 397–415. Amsterdam: Elsevier/North-Holland Biomed. Press. 1979.
Holloway, W. R., Grota, L. J., Brown, G. M. Determination of immunoreactive melatonin in the colon of the rat by immunocytochemistry. J. Histochem. Cytochem.28, 255–262 (1980).
Joss, J. M. P. A rhythm in hydroxyindole-O-methyltransferase (HIOMT) activity in the scincid lizard,Lampropholas guichenoti. Gen. Comp. Endocrinol.36, 521–525 (1978).
Kennaway, D. J., Frith, R. G., Phillipou, G., Matthews, C. D., Seamark, R. F. A specific radioimmunoassay for melatonin in biological tissue and fluids and its validation by gas chromatography-mass spectrometry. Endocrinology101, 119–127 (1977).
Lerner, A. B., Case, J. D., Biemann, K., Heinzelman, R. V., Szmuszkovicz, J., Anthony, W. C., Krivis, A. Isolation of 5-methoxyindole-3-acetic acid from bovine pineal glands. J. Am. Chem. Soc.81, 5264 (1959).
McIsaac, W. N., Tahorsky, R. J., Farrel, G. 5-Methoxytryptophol: effect on estrus and ovarian weight. Science145, 63–64 (1964).
Mullen, P. E., Leone, R. M., Hooper, J., Smith, I., Silman, R. E., Finnie, M., Carter, S., Linsell, C. Pineal 5-methoxytryptophol in man. Psychoneuroendocrinol.2, 117–126 (1979).
Nagle, C. A., Cardinali, D. P., Rosner, J. M. Light regulation of rat retinal hydroxyindole-O-methyltransferase (HIOMT) activity. Endocrinology91, 423–426 (1972).
Nir, J., Hirschmann, N., Sulman, F. G. The effect of heat on rat pineal hydroxyindole-O-methyltransferase activity. Experientia (Basel)31, 867–868 (1975).
Ozaki, Y., Lynch, H. J. Presence of melatonin in plasma and urine of pinealectomized rats. Endocrinology99, 641–644 (1976).
Pang, S. F., Brown, G. M., Grota, L. J., Chambers, J. W., Rodman, R. L. Determination of N-acetylserotonin and melatonin activities in the pineal gland, retina, Harderian gland, brain and serum of rats and chickens. Neuroendocrinology23, 1–13 (1977).
Pang, S. F., Yew, O. T. Pigment aggregations by melatonin in the retinal pigment epithelium and choroid of guinea-pig,Cavia porcellus. Experientia (Basel)35, 231–232 (1979).
Panke, E. S., Rollag, M. K., Reiter, R. J. Pineal melatonin concentrations in the Syrian hamster. Endocrinology104, 194–197 (1979).
Peat, F., Kinson, G. A. Testicular steroidogenesisin vitro in the rat in response to blinding, pinealectomy, and to the addition of melatonin. Steroids17, 251–253 (1971).
Pelham, R. W., Ralph, C. L., Campbell, I. M. Mass spectral identification of melatonin in blood. Biochem. biophys. Res. Comm.46, 1236–1241 (1972).
Pévet, P., Balemans, M. G. M., Bary, F. A. M., Noordegraaf, E. M. The pineal gland of the mole (Talpa europaea, L.). V. Activity of hydroxy-indole-O-methyltransferase (HIOMT) in the formation of melatonin/ 5-hydroxytryptophol in the eyes and the pineal gland. Ann. Biol. anim. Biochem. Biophys.18, 259–264 (1978).
Quay, W. B. Differential extractions for the spectrophotofluorometric measurement of diverse 5-hydroxy- and 5-methoxyindoles. Anal. Biochem.5, 51–54 (1963).
Quay, W. B. Retinal and pineal hydroxyindole-O-methyltransferase activity in vertebrates. Life Sci.4, 983 (1965).
Quay, W. B. Pineal Chemistry in Cellular and Physiological Mechanisms. Springfield, Ill.: Charles C Thomas. 1974.
Quay, W. B., Ma, Y. H. Demonstration of gastrointestinal hydroxyindole-O-methyltransferase. I. R. C. S. Med. Sci.4, 563 (1976).
Reiter, R. J. Interaction of photoperiod, pineal and seasonal reproduction as exemplified by findings in the hamster. Prog, reprod. Biol.4, 169–190 (1978).
Reiter, R. J., Vaughan, M. K. A study of indoles which inhibit pineal antigonadotrophic activity in male hamsters. Endocrin. Res. Comm.2, 299–308 (1975).
Reiter, R. J., Vaughan, M. K., Vaughan, G. M., Sorrentino, jr., S., Donofrio, R. J. The pineal gland as an organ of internal secretion. In: Frontiers of Pineal Physiology (Altschule, M., ed.), pp. 54–174. Cambridge, Mass.: The MIT Press. 1975.
Rollag, M. D., Panke, E. S., Trakulrungski, W., Trakulrungski, C., Reiter, R. J. Quantification of daily melatonin synthesis in the hamster pineal gland. Endocrinology106, 231–236 (1980).
Sheridan, M. N., Reiter, R. J. Observations in the pineal system in the hamster. II. Fine structure of the deep pineal. J. Morph.131, 163–171 (1970).
Tamarkin, L., Hollister, C. W., Lefebvre, N. G., Goldman, B. D. Melatonin induction of gonadal quiescence in pinealectomized Syrian hamsters. Science198, 953 (1977).
Tamarkin, L., Reppert, S. M., Klein, D. C. Regulation of pineal melatonin in the Syrian hamster. Endocrinology104, 385–389 (1979).
Tamarkin, L., Westrom, W. K., Hamill, A. L., Goldman, B. D. Effect of melatonin on the reproductive systems of male and female Syrian hamsters: a diurnal rhythm in sensitivity to melatonin. Endocrinology99, 1534–1538 (1976).
Turek, F. W., Desjardins, C., Menaker, M. Melatonin: antigonadal and progonadal effects in male golden hamsters. Science190, 280 (1975).
Vivien-Rœls, B.: L'épiphyse des Chéloniens. Étude embryologique, structurale, ultrastructurale; analyse qualitative et quantitative de la sérotonine dans des conditions normales et expérimentales. Thèse, Univ. de Strasbourg, 1976.
Vivien-Rœls, B., Arendt, J.: Relative roles of environmental factor, photoperiod and temperature in the control of serotonin and melatonin circadian variations in the pineal organ and plasma of the tortoise,Testudo hermanni, Gmelin. Melatonin Symposium, September 28–30, Bremen, Federal Republic of Germany (1980).
Vivien-Rœls, B., Arendt, J., Bradtke, J. Circadian and circannual fluctuations of pineal indoleamines (serotonin and melatonin) inTestudo bermanni Gmelin (Reptilia, Chelonia). Gen. Comp. Endocrinol.37, 197–210 (1979).
Vlahakes, G. J., Wurtman, R. J. A Mg2-dependent hydroxyindole-O-methyltransferase in rat Harderian gland. Biochem. biophys. Acta261, 194–198 (1972).
Vollrath, L. Comparative morphology of the vertebrate pineal complex. In: The Pineal Gland of Vertebrates Including Man (Ariëns Kappers, J., Pévet, P., eds.), Progress in Brain Research, Vol. 52, pp. 25–38. Amsterdam: Elsevier/North-Holland Biomed. Press. 1979.
Wetterberg, L., Geller, E., Yuwiller, A. Harderian gland: an extraretinal photoreceptor influencing the pineal gland in neonatal rats. Science167, 884–885 (1970).
Wiklund, L. Development of serotonin-containing cells and the sympathetic innervation of the habenular region in the rat brain: a fluorescence histochemical study. Cell Tiss. Res.155, 231–243 (1974).
Wurtman, R. J., Axelrod, J., Potter, L. T. The uptake of H3-melatonin in endocrine and nervous tissues and the effects of constant light exposure. J. Pharmacol. Exp. Ther.143, 314–315 (1964).
Wurtman, R. J., Ozaki, Y. 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. Suppl.13, 59–70 (1978).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pévet, P., Balemans, M.G.M., Legerstee, W.C. et al. 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 Transmission 49, 229–245 (1980). https://doi.org/10.1007/BF01252128
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF01252128