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Journal of Comparative Physiology A

, Volume 170, Issue 4, pp 479–489 | Cite as

Regulation of melatonin production by light, darkness, and temperature in the trout pineal

  • Marianna Max
  • Michael Menaker
Article

Summary

The pineal gland of the rainbow trout, Salmo gairdneri, when kept under in vitro perifusion culture conditions, displays a consistently elevated level of melatonin production in darkness (Gern and Greenhouse 1988). Upon light exposure melatonin production falls and stabilizes at a new lower level that is dependent upon the irradiance of the stimulus. To achieve the maximal response for each irradiance, the duration of the stimulus must exceed 30 min. The response amplitude is maximally sensitive to photons presented over durations of 30–45 min; is very insensitive to shorter light exposures; and is maintained with no evidence of adaptation over longer exposures. Temperature plays a role in regulation of melatonin production both in darkness and during light exposure; increased temperature increases melatonin production in darkness and also increases the sensitivity of the response to light. The action spectrum for the response is best fit by the Dartnall nomogram for a vitamin A1 based rhodopsin with peak sensitivity near 500 nm. The possible adaptive significance of control of melatonin synthesis by light and temperature is considered.

Key words

Pineal Melatonin Photoreceptor Trout Temperature 

Abbreviations

L∶D

light∶dark cycle

RIA

radioimmunoassay

I125

Iodine

HIOMT

hydroxyindole-O-methyltransferase

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References

  1. Asahina K, Hanu I (1985) Development of photoperiodism involved in the gonadal activity of rose bitterling Rhodeus ocellatus ocellatus. Bull PPN Soc Sci Fish 51:1665–1670Google Scholar
  2. Baehr W, Applebury ML (1986) Exploring visual transduction with recombinant DNA techniques. Trends in Neurosci 9:198–203Google Scholar
  3. Binkley S (1981) Pineal biochemistry: comparative aspects and circadian rhythms. In: Reiter RJ (ed) The pineal gland, anatomy and biochemistry, vol 1. CRC, Forida, pp 155–172Google Scholar
  4. Binkley S, Riebman JB, Reilly KB (1977) Timekeeping by the pineal gland. Science 197:1181–1183Google Scholar
  5. Bito LZ, Turansky DG (1975) Photoactivation of pupillary constriction in the isolated in vitro iris of mammal Mesocricetus auratus. Comp Biochem Physiol 50A:413Google Scholar
  6. Bloch AM (1885) Experiences sur la vision. C R Soc Biol Paris 37:493–495Google Scholar
  7. Bromage N, Duston J, Randall C, Brool A, Thrush M, Carrillo M, Zanuy S (1990) Photoperiodic control of teleost reproduction. Progr Clin Biol Res 342Google Scholar
  8. Cahill GM, Besharse JC (1990) Circadian regulation of melatonin in the retina of Xenopus laevis: Limitation by serotonin availability. J Neurochem 54:716–719Google Scholar
  9. Davies PR, Hanyu I, Furukawa K, Nomura M (1986) The effect of temperature and photoperiod on sexual maturation and spawning of the common carp Cyprinus carpio under conditions of low temperature. Aquaculture 52:51–58Google Scholar
  10. Deguchi T (1979) A circadian oscillator in cultured cells of chicken pineal gland. Nature 282:94–96Google Scholar
  11. Deguchi T (1981) Rhodopsin-like photosensitivity of isolated chicken pineal gland. Nature 290:702–704Google Scholar
  12. DeLean A, Munsen PJ, Rodbard D (1978) Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves. Am J Physiol 235:97–102Google Scholar
  13. Dodt E (1963) Photosensitivity of the pineal organ in the teleost Salmo irideus. Experientia 19:642–643Google Scholar
  14. Dodt E (1973) The parietal eye (pineal and parietal organs) of lower vertebrates. In: Jung R (ed) Handbook of sensory physiology, vol VII/3B. Springer, Berlin Heidelberg New York, pp 112–140Google Scholar
  15. Ebrey TG, Honig B (1977) New wavelength dependent visual pigment nomograms. Vision Res 17:147–151Google Scholar
  16. Ekström P (1987) Photoreceptors and CSF-contacting neurons in the pineal organ of a teleost fish have direct axonal connections with the brain: an electron microscope study. J Neurosci 7:987–995Google Scholar
  17. Ekström P, Meissl H (1988) Intracellular staining of physiologically identified photoreceptor cells and hyperpolarizing interneurons in the teleost pineal organ. Neuroscience 25:1061–1070Google Scholar
  18. Ekström P, Foster RG, Korf H-W, Schalken JJ (1987) Antibodies against retinal photoreceptor-specific proteins reveal axonal projections from the photosensory pineal organ in teleosts. J Comp Neurobiol 265:25–33Google Scholar
  19. Fain GL, Lisman JE (1981) Membrane conductances of photoreceptors. Prog Biophys Mol Biol 37:91–147Google Scholar
  20. Falcon J, Meissl H (1981) The photosensory function of the pineal organ of the pike (Esox lucius L.): correlation between structure and function. J Comp Physiol 144:127–137Google Scholar
  21. Falcon J, Geffard M, Juillard MT, Delaage M, Collin JP (1981) Melatonin-like immunoreactivity in photoreceptor cell. A study in the teleost pineal organ and the concept of photoneuroendocrine cells. Biol Cell 42:65–68Google Scholar
  22. Falcon J, Guerlotte JF, Voison P, Collin J-P (1987) Rhythmic melatonin biosynthesis in a photoreceptive pineal organ: A study in the pike. Neuroendocrinology 45:479–486Google Scholar
  23. Foster RG, Follett BK, Lythgoe JN (1985) Rhodopsin-like sensitivity of extra-retinal photoreceptors mediating the photoperiodic response in quail. Nature 313:50–52Google Scholar
  24. Garg SK (1987) Seasonal effects of pinealectomy on testicular recrudescence and secretory activity of seminal vesicles in the catfish Heteropreustes fossilis Block. J Fish Biol 30:377–388Google Scholar
  25. Gern WA, Greenhouse SS (1988) Examination of in vitro melatonin secretion from superfused trout (Salmo gairdneri) pineal organs maintained under diel illumination or continuous darkness. Gen Comp Endocrinol 71:163–174Google Scholar
  26. Gern WA, Owens DW, Ralph CL (1977) Plasma melatonin in the trout: Day-night change demonstrated by radioimmunoassay. Gen Comp Endocrinol 34:453–458Google Scholar
  27. Geusz ME, Page TL (1991) An opsin-based photopigment mediates phase shifts of the Bulla circadian pacemaker. J Comp Physiol A 168:565–570Google Scholar
  28. Hafeez MA, Zerihun L (1987) Studies on central projections of the pineal nerve tract in rainbow trout Salmo gairdneri Richardson using cobalt chloride electrophoresis. Cell Tissue Res 154:485–510Google Scholar
  29. Harrison NL, Zatz M (1989) Voltage-dependent calcium channels regulate melatonin output from cultured chick pineal cells. JNeurosci 9:2462–2467Google Scholar
  30. Hubbel WL, Bownds MD (1979) Visual transduction in vertebrate photoreceptors. Annu Rev Neurosci 2:17–29Google Scholar
  31. Jagger J (1977) Phototechnology and biological experimentation. In: Smith K (ed) The science of photobiology. Plenum, New York, pp 1–26Google Scholar
  32. Kezuka H, Aida K, Hanyu I (1989) Melatonin secretion from goldfish pineal gland in organ culture. Gen Comp Endocrinol 75:217–221Google Scholar
  33. Klein DC (1985) In: Evered D, Clark S (eds) Photoperiodism, melatonin and the pineal. Pitman, London, pp 51–50Google Scholar
  34. Kuo CH, Tamotsu S, Morita Y, Shinozuwa T, Akiyama M, Miki N (1988) Presence of retina-specific proteins in the lamprey pineal complex. Brain Res 442:147–151Google Scholar
  35. Lolley RN, Lee RH (1990) Cyclic GMP and photoreceptor function. FASEB 4:3001–3008Google Scholar
  36. Lythgoe JN (1975) The ecology of vision. Oxford University Press, OxfordGoogle Scholar
  37. Max M (1991) Photic regulation of pineal melatonin synthesis in the trout. PhD thesis, University of VirginiaGoogle Scholar
  38. McNulty JA (1981) A quantitative morphological study of the pineal organ in the goldfish Carassius auratus. Can J Zool 59:1312–1325Google Scholar
  39. Meissl H, Dodt E (1981) Comparative physiology of pineal photoreceptor organs. In: Oksche A, Pevet P (eds) The pineal organ: photobiology — biochronometry — endocrinology. Elsevier, Amsterdam, pp 61–80Google Scholar
  40. Meissl H, Ekström P (1988) Photoreceptor responses to light in the isolated pineal organ of the trout, Salmo gairdneri. Neuroscience 25:1071–1076Google Scholar
  41. Meissl H, Martin C, Tabata M (1990) Melatonin modulates the neural activity in the photosensory pineal organ of the trout; evidence for endocrine-neuronal interactions. J Comp Physiol A 167:641–648Google Scholar
  42. Menaker M (1982) The search for principles of physiological organization in vertebrate circadian systems. In: Aschoff J, Daan S, Groos G (eds) Vertebrate circadian systems. Springer, Berlin, pp 1–12Google Scholar
  43. Menaker M, Wisner S (1983) Temperature-compensated circadian clock in the pineal of Anolis. Proc Natl Acad Sci USA 80:6119–6121Google Scholar
  44. Menaker M, Takahashi JS, Eskin A (1978) The physiology of circadian pacemaker. Annu Rev Physiol 40:501–520Google Scholar
  45. Morita T (1966) Absence of electrical activity of the pigeon's pinealorgan in response to light. Experientia 22:402–406Google Scholar
  46. Morita Y (1975) Direct photosensory activity of the pineal. In: Knigge KM, Scot DE, Kobayashi H, Ishii S (eds) Brain endocrine interaction II. Karger, Basel, pp 376–387Google Scholar
  47. Münz FW, Beatty DD (1965) A critical analysis of the visual pigments of salmon and trout. Vision Res 5:1–17Google Scholar
  48. Naka KI, Rushton WAH (1966a) S-potential from color units in the retina of fish (Cyprinidae). J Physiol 185:536–555Google Scholar
  49. Naka KI, Rushton WAH (1966b) An attempt to analyze color reception by electrophysiology. J Physiol 185:556–586Google Scholar
  50. Nelson DE, Takahashi JS (1991) Sensitivity of a visual pathway for entrainment of a circadian pacemaker: Temporal integration of photic inputs. J Physiol 439:115–145Google Scholar
  51. Omura Y, Ali MA (1980) Responses of pineal photoreceptors in the brook and rainbow trout. Cell Tissue Res 239:599–610Google Scholar
  52. Oshima N, Kasukawa H, Fujii R (1989) Control of chromatophore movements in the blue-green damsel fish. Comp Biochem Physiol 93:239–246Google Scholar
  53. Pugh EN, Lamb TD (1990) Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Res 12:1923–1948Google Scholar
  54. Ralph CL, Dawson DC (1968) Failure of the pineal body of two species of birds (Coturnix japonica and Passer domesticus) to show electrical responses to illumination. Experientia 24:147–148Google Scholar
  55. Robertson LM (1990) The avian pineal: characterization of a cellular circadian system. Diss Northwestern UniversityGoogle Scholar
  56. Rollag MD, Niswender GD (1976) Radioimmunoassay of serum concentrations of melatonin in sheep exposed to different lighting regimes. Endocrinology 98:482–489Google Scholar
  57. Rubin LJ, Nolte JF (1984) Modulation of the response of a photosensitive muscle by β-adrenergic regulation of cyclic AMP levels. Lett Nature 307:551–553Google Scholar
  58. Stryer L (1986) Cyclic GMP cascade of vision. Annu Rev Neurosci 87–119Google Scholar
  59. Tabata M, Suzuki T, Niwa H (1985) Chromophores in the extraretinal photoreceptor (pineal organ) of teleosts. Brain Res 338:173–176Google Scholar
  60. Takahashi JS, Hamm H, Menaker M (1980) Circadian rhythms of melatonin release from individual superfused chicken pineal glands in vitro. Proc Natl Acad Sci USA 77:2319–2322Google Scholar
  61. Takahashi JS, DeCoursey PJ, Bauman L, Menaker M (1984) Spectral sensitivity of a novel photoreceptive system mediating entrainment of mammalian circadian rhythms. Nature 308:186–188Google Scholar
  62. Takahashi JS, Murakami N, Nikaido SS, Pratt BL, Robertson L (1989) The avian pineal, a vertebrate model system of the circadian oscillator: Cellular regulation of circadian rhythms by light, second messengers, and macromolecular synthesis. Hormone Res 45:279–352Google Scholar
  63. Uchida K, Morita Y (1990) Intracellular responses from UV-sensitive cells in the photosensory pineal organ. Brain Res 534:237–242Google Scholar
  64. Van Dop C, Yamanaka G, Steinberg F, Sekura RD, Manclark CR, Stryer L, Bourne HR (1984) ADP-ribosylation of transducin by pertussis toxin blocks the light-stimulated hydrolysis of GTP and cGMP in retinal photoreceptors. J Biol Chem 259:23–26Google Scholar
  65. Vigh B, Vigh-Teichmann I (1981) Light- and electron-microscopic demonstration of immunoreactive opsin in the pinealocytes of various vertebrates. Cell Tissue Res 221:451–463Google Scholar
  66. Vigh-Teichmann I, Röhlich P, Vigh B, Aros B (1980) Comparison of the pineal complex, retina and cerebrospinal fluid contacting neurons by immunocytochemical antirhodopsin reaction. Z Mikrosk-anat Forsch, Leipzig 94:623–640Google Scholar
  67. Vivien-Roels B, Pevet P, Duois M, Arendt J, Brown GM (1981) Immunohistochemical evidence for the presence of melatonin in the pineal gland, the retina and the Harderian gland. Cell Tissue Res 217:105–115Google Scholar
  68. Wiechman AF, Hollyfield JG (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 258:253–266Google Scholar
  69. Wiechman AF, Bok D, Horwitz J (1985) Localization of hydroxyindole-O-methyltransferase in the mammalian pineal gland and retina. Invest Ophthal Visual Sci 26:253–265Google Scholar
  70. Zatz M (1982) The role of cyclic nucleotides in the pineal gland. In: Kebabian JW, Nathanson JA (eds) Cyclic nucleotides II: physiology and pharmacology. Springer, New York, pp 691–710Google Scholar
  71. Zatz M, Mullen DA (1988) Two mechanisms of photoendocrine transduction in cultured chick pineal cells: pertussis toxin blocks the acute but not the phase-shifting effects of light on the melatonin rhythm. Brain Res 453:63–71Google Scholar
  72. Zatz M, Mullen DA, Moskal JR (1988) Photoendocrine transduction in cultured chick pineal cells: effects of light, dark, and potassium on the melatonin rhythm. Brain Res 438:199–215Google Scholar
  73. Zucker R, Nolte J (1978) Light-induced calcium release in a photosensitive vertebrate smooth muscle. Nature 274:78–80Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • Marianna Max
    • 1
  • Michael Menaker
    • 1
  1. 1.Department of BiologyUniversity of VirginiaCharlottesvilleUSA

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