Abstract
The rhythmic production of melatonin is governed by intrapineal oscillators in all fish species so far investigated except the rainbow trout. To determine whether the latter represents an exception among fish, we measured in vitro melatonin secretion in pineal organs of nine wild freshwater and six marine teleost species cultured at constant temperature and under different photic conditions. The results demonstrate that pineal organs of all species maintain a rhythmic secretion of melatonin under light:dark cycles and complete darkness, and strongly suggest that most fish possess endogenous intrapineal oscillators driving the rhythm of melatonin production, with the exception of the rainbow trout.
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Abbreviations
- LD :
-
light:dark
- DD :
-
dark:dark
- NAT :
-
N-acetyltransferase
- RIA :
-
radioimmunoassay
References
Bolliet V, Ali MA, Anctil M, Zachmann A (1993) Melatonin secretion in vitro from the pineal complex of the lamprey, Petromyzon marinus. Gen Comp Endocrinol 89: 101–106
Bolliet V, Bégay V, Ravault JP, Ali MA, Collin JP, Falcón J (1994) Multiple circadian oscillators in the photosensitive pike pineal organ. A study using organ and cell structure. J Pineal Res 16: 77–84
Collin JP, Brisson P, Voisin P, Falcón J (1986) Multiple cell types in the pineal. Functional aspects. In: O'Brien PJ, Klein DC (eds) Pineal and retinal relationships. Academic Press, New York, pp 15–32
Collin JP, Voisin P, Falcón J, Faure JP, Brisson P, Defaye JR (1989) Pineal transducers in the course of evolution: molecular organisation, rhythmic metabolic activity and role. Arch Histol Cytol 52: 441–449
Delgado MJ, Viviens-Roels B (1989) Effect of environmental temperature and photoperiod on the melatonin levels in the pineal, lateral eyes, and plasma of the frog. Rana perezi: importance of ocular melatonin. Gen Comp Endocrinol 75: 46–53
Falcón J, Guerlotté J, Voisin P, Collin JP (1987) Rhythmic melatonin biosynthesis in a photoreceptive pineal organ: a study in the pike. J Neuroendocrinol 45: 479–486
Falcón J, Brun-Marmillon J, Claustrat B, Collin JP (1989) Regulation of melatonin secretion in a photoreceptive pineal organ: a study in the pike. J. Neurosci 9: 1943–1950
Falcón J, Thibault C, Bégay V, Zachmann A, Collin JP (1992) Regulation of the rhythmic melatonin secretion by fish pineal photoreceptor cells. In: Ali MA (ed) Rhythm in fishes. NATO ASI series. Series A, Life sciences 236: 167–198
Falcón J, Bégay V, Goujon JM, Voisin P, Guerlotté J, Collin JP (1994a) Immunocytochemical localization of hydroxyindole-O-methyltransferase in pineal photoreceptor cells of several fish species. J Comp Neurol 341: 559–566
Falcón J, Bolliet V, Ravault JP, Chesneau D, Ali MA, Collin JP (1994b) Rhythmic secretion of melatonin by the superfused pike pineal organ: thermo- and photoperiod interaction. Neuroendocrinology 60: 535–543
Gern WA, Greenhouse SS (1988) Examination of in vitro melatonin secretion from superfused trout (Salmo gairdneri) pineal organ maintained under diel illumination or continuous darkness. Gen Comp Endocrinol 71: 163–174
Gern WA, Greenhouse SS, Nervina JM, Gasser PJ (1992) The rainbow trout pineal organ: an endocrine photometer. In: Ali MA (ed) Rhythm in fishes. NATO ASI series. Series A, Life sciences 236: 199–218
Hastings JW, Rusak B, Boulos Z (1991) Circadian rhythms: the physiology of biological timing. In: Prosser C (ed) Neural and integrative animal physiology. Wiley-Liss, New York, pp 435–546
Iigo M, Kezuka H, Aida K, Hanyu I (1991) Circadian rhythms of melatonin secretion from superfused goldfish (Carassius auratus) pineal glands in vitro. Gen Comp Endocrinol 83: 152–158
Kezuka H, Aida K, Hanyu I (1989) Melatonin secretion from gold-fish pineal gland in organ culture. Gen Comp Endocrinol 75: 217–221
Legendre L, Legendre P (1983) Numerical ecology. Developments in environmental modelling 3. In: Jorgensen SE (ed) Elsevier, pp 344–347
Legendre L, Fréchette M, Legendre P (1981) The contingency periodogramm: a method of identifying rhythms in series of non-metric ecological data. J Ecol 69: 965–979
Max M, Menaker M (1992) Regulation of melatonin production by light, darkness and temperature in the trout pineal. J Comp Physiol A 170: 479–489
Menaker M, Wissner S (1983) Temperature-compensated circadian clock in the pineal of Anolis. Proc Natl Acad Sci USA 80: 6119–6121
Morton DJ, Forbes HJ (1988) Pineal gland N-acetyltransferase and hydroxyindole-O-methyltransferase activity in the rainbow trout (Salmo gairdneri): seasonal variation linked to photoperiod. Neurosci Lett 94: 333–337
Pickard GE, Tang W (1993) Individual pineal cells exhibit a circadian rhythm in melatonin secretion. Brain Res 627: 141–146
Pickard GE, Tang W (1994) Pineal photoreceptors rhythmically secrete melatonin. Neurosci Lett 171: 109–112
Randall C, Thrush M, Bromage N (1991) Absence of an endogenous component regulating melatonin secretion in the rainbow trout. In: Arendt J (ed) Advance in pineal research, vol 5. Libbey, London, pp 279–281
Takahashi JS, Murakami N, Nikaido SS, Pratt BL, Robertson LM (1989) The avian pineal, a vertebrate model system of the circadian oscillator: cellular regulation of circadian rhythm by light, second messengers and macromolecular synthesis. Rec Prog Horm Res 45: 279–349
Thibault C, Collin JP, Falcón J (1993) Intrapineal circadian oscillator(s), cyclic nucleotides and melatonin production in the pike pineal photoreceptor cells. In: Touitou Y et al., (eds) Melatonin and the pineal gland. From basic science to clinical application. Elsevier, Amsterdam, pp 11–18
Underwood H (1989) The pineal and melatonin: regulators of circadian function in lower vertebrates. Experientia 45: 914–922
Vivien-Roels B, Pévet P, Claustrat B (1988) Pineal and circulating melatonin rhythms in the box turtle, Terrapene carolina triunguis: effect of photoperiod, light pulse, and environmental temperature. Gen Comp Endocrinol 69: 163–173
Zachmann A, Knijff SCM, Bolliet V, Ali MA (1991) Effects of temperature cycle and photoperiod on rhythmic melatonin secretion from the pineal organ of a teleost (Catostomus commersoni) in vitro. Neuroendocrinol Lett 13: 325–330
Zachmann A, Knijff SCM, Ali MA, Anctil M (1992a) Effects of photoperiod and different intensities of light exposure on melatonin levels in the blood, pineal organ and retina of the brook trout (Salvelinus fontinalis) Mitchill). Can J Zool 70: 25–29
Zachmann A, Falcón J, Knijff SCM, Bolliet V, Ali MA (1992b) Effects of photoperiod and temperature on rhythmic melatonin secretion from the pineal organ of the white sucker (Catostomus commersoni) in vitro. Gen Comp Endocrinol 86: 26–33
Zatz M, Wang H (1991) High salt mimics effects of light pulses on circadian pacemaker in cultured chick pineal cells. Am J Physiol 260: R769-R776
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Bolliet, V., Ali, M.A., Lapointe, F.J. et al. Rhythmic melatonin secretion in different teleost species: an in vitro study. J Comp Physiol B 165, 677–683 (1996). https://doi.org/10.1007/BF00301136
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DOI: https://doi.org/10.1007/BF00301136