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An attempt to correlate brain areas containing melatonin-binding sites with rhythmic functions: a study in five hibernator species

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Abstract

High affinity melatonin-binding sites have been described, by means of autoradiography with 2-125I-melatonin as the ligand, in more than 60 brain areas of about 20 mammalian species, with dramatic variations in the nature and number of labelled structures among the different species studied. As melatonin is involved in the synchronization of biological rhythms, we have tried to correlate the brain areas containing melatonin-binding sites with some rhythmic functions typical of give species. Therefore, we have studied the location of melatonin-binding sites in the complete brain of five long-day breeders with hibernation cycles, viz. one insectivore and four rodents. With the exception of the suprachiasmatic nuclei and the pars tuberalis of the pituitary, both of which contain binding sites in all five species, few reactive structures are common, even among species from the same family, e.g. the edible dormouse and the garden dormouse.

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References

  • Armstrong SM (1989) Melatonin and circadian control in mammals. Experientia 45:932–938

    Google Scholar 

  • Bittman EL (1993) Melatonin binding sites in the central nervous system. Methods Neurosci 11:105–121

    Google Scholar 

  • Bittman EL, Weaver DR (1990) The distribution of melatonin binding sites in neuroendocrine tissues of the ewe. Biol Reprod 43:986–993

    Google Scholar 

  • Boissin-Agasse L, Barberis C, Audigier S, Roch G, Boissin J (1992) Localization of melatonin binding sites in the pars tuberalis of the mink at three times during the seasonal testicular cycle. Neurosci Lett 144:147–151

    Google Scholar 

  • Bonnefond C, Mounerie R, Richard JP, Martinet L (1993) Melatonin and the circadian clock in mink. Effects of daily injections of melatonin on circadian rhythms of locomotor activity and autoradiographic localization of melatonin binding sites. J Neuroendocrinol 5:241–246

    Google Scholar 

  • Brooks DS, Cassone VM (1992) Daily and circadian regulation of 2-(125I)iodomelatonin binding in chick brain. Endocrinology 131:1297–1304

    Google Scholar 

  • Cassone VM (1991) Melatonin and suprachiasmatic nucleus function. In: Klein DC, Moore RY, Reppert SM (eds) Suprachiasmatic nucleus. The mind's clock. Oxford University Press, New York Oxford, pp 309–323

    Google Scholar 

  • Cassone VM, Brooks DS (1991) Sites of melatonin action in the brain of the house sparrow, Passer domesticus. J Exp Zool 260:302–309

    Google Scholar 

  • Cassone VM, Chesworth MJ, Armstrong S (1986a) Entrainment of rat circadian rhythms by daily injection of melatonin depends upon the hypothalamic suprachiasmatic nucleus. Physiol Behav 36:1111–1121

    Google Scholar 

  • Cassone VM, Chesworth MJ, Armstrong SM (1986b) Dose-dependent entrainment of rat circadian rhythms by daily injection of melatonin. J Biol Rhythms 1:219–229

    Google Scholar 

  • De Reviers MM, Ravault JP, Tillet Y, Pelletier J (1989) Melatonin binding sites in the pars tuberalis of the sheep. Neurosci Lett 100:89–93

    Google Scholar 

  • De Reviers MM, Tillet Y, Pelletier J (1991) Melatonin binding sites in the brain of sheep exposed to light or pinealectomized. Neurosci Lett 121:17–20

    Google Scholar 

  • Deveson S, Howarth JA, Arendt J, Forsyth JA (1992) In vitro autoradiographic localization of melatonin binding sites in the caprine brain. J Pineal Res 13:6–12

    Google Scholar 

  • Devries MJ, Ferreira SA, Glass JD (1989) Evidence that short photoperiod-induced gonadal regression in the Mongolian gerbil is mediated by the action of melatonin in the medial hypothalamus. Brain Res 494:241–246

    Google Scholar 

  • Duncan MJ, Mead RA (1992) Autoradiographic localization of binding sites for 2-[125]iodomelatonin in the pars tuberalis of the western spotted skunk (Spilogale putorius latifrons). Brain Res 569:152–155

    Google Scholar 

  • Duncan MJ, Takahashi JS, Dubocovich ML (1989) Characteristics and autoradiographic localization of 2-[125]iodomelatonin binding sites in Djungarian hamster brain. Endocrinology 125:1011–1018

    Google Scholar 

  • Duranti E, Stankov B, Spadoni G, Duranti A, Lucini V, Capsoni S, Biella G, Fraschini F (1992) 2-Bromomelatonin: synthesis and characterization of a potent melatonin agonist. Life Sci 51:479–485

    Google Scholar 

  • Gauer F, Masson-Pévet M, Pévet P (1992 a) Effect of constant light, pinealectomy and guanosine triphosphate-gamma-S on the density of melatonin receptors in the rat suprachiasmatic nucleus: a possible implication of melatonin action. J Neuroendocrinol 4:455–459

    Google Scholar 

  • Gauer F, Masson-Pévet M, Pévet P (1992 b) Pinealectomy and constant illumination increase the density of melatonin binding sites in the pars tuberalis of rodents. Brain Res 575:32–38

    Google Scholar 

  • Gauer F, Masson-Pévet M, Pévet P (1993 a) Melatonin receptor density is regulated in rat pars tuberalis and suprachiasmatic nuclei by melatonin itself. Brain Res 602:153–156

    Google Scholar 

  • Gauer F, Masson-Pévet M, Pévet P (1993 b) Daily rhythms of melatonin binding sites in the rat pars tuberalis and suprachiasmatic nuclei; evidence for a regulation of melatonin receptors by melatonin itself. Neuroendocrinology 57:120–126

    Google Scholar 

  • Gauer F, Masson-Pévet M, Saboureau M, George D, Pévet P (1993 c) Differential seasonal regulation of melatonin receptor density in the pars tuberalis and the suprachiasmatic nuclei: a study in the hedgehog (Erinaceus europaeus L.). J Neuroendocrinol 5:685–690

    Google Scholar 

  • Goldman BD, Darrow JM (1983) The pineal gland and mammalian photoperiodism. Neuroendocrinology 37:386–396

    Google Scholar 

  • Helliwell RJA, Williams LM (1992) Melatonin binding sites in the ovine brain and pituitary: characterization during the oestrous cycle. J Neuroendocrinol 4:287–294

    Google Scholar 

  • Jennes L, Stumpf WE (1980) LHRH systems in the brain of the golden hamster. Cell Tissue Res 209:239–256

    Google Scholar 

  • Karsch FJ, Bittman EI, Foster DL, Goodman RL, Legan SJ, Robinson JE (1984) Neuroendocrine basis of seasonal reproduction. Recent Prog Horm Res 40:185–232

    Google Scholar 

  • Kirsch R, Belgnaoui S, Gourmelen S, Pévet P (1993) Free running Syrian and Siberian hamsters are entrained by daily infusions of melatonin. In: Wetterberg I (ed) Light and biological rhythms in man. Pergamon Press, Oxford, pp 107–120

    Google Scholar 

  • Laitinen JT, Saavedra JM (1990) Characterization of melatonin receptors in the rat suprachiasmatic nuclei: modulation of affinity with cations and guanine nucleotides. Endocrinology 126:2110–2115

    Google Scholar 

  • Laitinen JT, Flügge G, Saavedra JM (1990) Characterization of melatonin receptors in the rat area postrema: modulation of affinity with cations and guanine nucleotides. Neuroendocrinology 51:619–624

    Google Scholar 

  • Lindroos OFC, Leinonen LM, Laasko ML (1992) Melatonin binding to the anteroventral and anterodorsal thalamic nuclei in the rat. Neurosci Lett 143:219–222

    Google Scholar 

  • Martinoli MG, Williams LM, Kah O, Titchener LT, Pelletier G (1991) Distribution of central melatonin binding sites in the goldfish (Carassius auratus). Mol Cell Neurosci 2:78–85

    Google Scholar 

  • Masson-Pévet M, George D, Gauer F, Pévet P (1993) Demonstration of melatonin binding sites in cyclohexylamine-formaldehyde-fixed brain tissue. Cell Tissue Res 274:207–209

    Google Scholar 

  • Meijer JH, Rietveld WJ (1989) Neurophysiology of the suprachiasmatic circadian pacemaker in rodents. Physiol Rev 69:671–707

    Google Scholar 

  • Morgan PJ, Williams LM, Davidson G, Lawson W, Howell HE (1989) Melatonin receptors on ovine pars tuberalis; characterization and autoradiographic localization. J Neuroendocrinol 1:1–4

    Google Scholar 

  • Nakazawa K, Marubayashi U, McCann SM (1991) Mediation of the shortloop negative feedback of luteinizing release by melatonin-induced inhibition of LH release from the pars tuberalis. Proc Natl Acad Sci USA 8:7576–7579

    Google Scholar 

  • Nazarali AJ, Gutkind JS, Saavedra JM (1989) Calibration of 125I-polymer with 125I-brain paste standards for use in quantitative receptor autoradiography. J Neurosci Methods 30:247–253

    Google Scholar 

  • Pelletier J, Castro B, Roblot G, Wylde R, De Reviers MM (1990) Characterization of melatonin receptors in the ram pars tuberalis: influence of light. Acta Endocrinol 123:557–562

    Google Scholar 

  • Pévet P (1988) The role of the pineal gland in the photoperiodic control of reproduction in different hamster species. Reprod Nutr Dev 28:443–458

    Google Scholar 

  • Ralph MR, Foster RG, Davis FC, Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975–978

    Google Scholar 

  • Redman JR, Armstrong SM, Ng KT (1983) Free running activity rhythms in the rat entrainment by melatonin. Science 219:1089–1091

    Google Scholar 

  • Reiter RJ (1991) Melatonin: that ubiquitously acting pineal hormone. News in Physiol Sci 6:223–227

    Google Scholar 

  • Reppert SM, Weaver DR, Rivkees SA, Stopa EG (1988) Putative melatonin receptors in a human biological clock. Science 242:78–81

    Google Scholar 

  • Rivkees SA, Cassone VM, Weaver DR (1989) Melatonin receptors in chick brain: characterization and localization. Endocrinology 125:363–368

    Google Scholar 

  • Rollag MD, Niswender GD (1976) Radioimmunoassay of serum concentrations in sheep exposed to different lighting regimens. Endocrinology 98:482–489

    Google Scholar 

  • Rusak B, Zucker I (1979) Neural regulation of circadian rhythms. Physiol Rev 59:449–526

    Google Scholar 

  • Skene DJ, Masson-Pévet M, Pévet P (1992) Characterization of melatonin binding sites in the pars tuberalis of the European hamster. J Neuroendocrinol 4:189–192

    Google Scholar 

  • Skene DJ, Masson-Pévet M, Pévet P (1993) Seasonal changes in melatonin binding sites in the pars tuberalis of male European hamsters and the effect of testosterone manipulation. Endocrinology 132:1682–1686

    Google Scholar 

  • Stankov B, Fraschini F (1993) High affinity melatonin binding sites in the vertebrate brain. Neuroendocrinol Lett 15:149–164

    Google Scholar 

  • Stankov B, Cozzi B, Lucini V, Capsoni S, Fauteck J, Fumagalli P, Fraschini F (1991 a) Localization and characterization of melatonin binding sites in the brain of the rabbit (Oryctolagus cuniculus) by autoradiography and in vitro ligand-receptor binding. Neurosci Lett 133:68–72

    Google Scholar 

  • Stankov B, Fraschini F, Reiter RJ (1991 b) Melatonin binding sites in the central nervous system. Brain Res Rev 16:245–256

    Google Scholar 

  • Stankov B, Fraschini F, Reiter RJ (1993) The melatonin receptor: distribution, biochemistry, and pharmacology. In: Yu Hs, Reiter RJ (eds) Melatonin: biosynthesis, physiological effects, and clinical applications. CRC Press, Boca Raton Ann Arbor London, pp 155–186

    Google Scholar 

  • Stankov B, Capsoni S, Lucini V, Fauteck J, Gatti S, Gridelli B, Biella G, Cozzi B, Fraschini F (1993) Autoradiographic localization of putative melatonin receptors in the brain of two old world primates: Cercopithecus aethiops and Papio ursinus. Neuroscience 52:459–468

    Google Scholar 

  • Stanton TL, Siuciak JA, Dubocovich ML, Krause DN (1991) The area of 2-125I-melatonin binding in the pars tuberalis of the ground squirrel is decreasing during hibernation. Brain Res 557:285–288

    Google Scholar 

  • Stehle J (1990) Melatonin binding sites in brain of the 2-day-old chicken: an autoradiographic localization. J Neural Transm 81:83–89

    Google Scholar 

  • Stehle J, Vanecek J, Vollrath L (1989) Effects of melatonin on spontaneous electrical activity of neurons in rat suprachiasmatic nuclei: an in vitro iontophoretic study. J Neural Transm 78:173–177

    Google Scholar 

  • Tamarkin L, Baird CJ, Almeida OFX (1985) Melatonin: a coordinating signal for mammalian reproduction Science 227:714–720

    Google Scholar 

  • Vakkuri O, Leppaluoto J, Vuolteenaho C (1984) Development and validation of a melatonin radioimmunoassay using radioiodinated melatonin as tracer. Acta Endocrinol 106:152–157

    Google Scholar 

  • Vanecek J, Jansky L (1989) Short days induce changes in specific melatonin binding in hamster median eminence and anterior pituitary. Brain Res 477:387–390

    Google Scholar 

  • Vanecek J, Pavlik A, Illnerova H (1987) Hypothalamic melatonin receptor sites revealed by autoradiography. Brain Res 435:359–362

    Google Scholar 

  • Weaver DR, Reppert SM (1990) Melatonin receptors are present in the ferret pars tuberalis and pars distalis, but not in the brain. Endocrinology 127:2607–2609

    Google Scholar 

  • Weaver DR, Rivkees SA, Reppert SM (1989) Localization and characterization of melatonin receptor in rodent brain by in vitro autoradiography. J Neurosci 9:2581–2590

    Google Scholar 

  • Weaver DR, Carlson LL, Reppert SM (1990) Melatonin receptors and signal transduction in melatonin-sensitive and melatonininsensitive populations of white-footed mice (Peromyscus leucopus). Brain Res 506:353–357

    Google Scholar 

  • Weaver DR, Rivkees SA, Carlson LL, Reppert SM (1991) Localization of melatonin receptors in mammalian brain. In: Klein DC, Moore RY, Reppert SM (eds) Suprachiasmatic nucleus. The mind's clock. Oxford University Press, New York Oxford, pp 289–308

    Google Scholar 

  • Weaver DR, Stehle JH, Stopa EG, Reppert SM (1993) Melatonin receptors in human hypothalamus and pituitary. Implications for circadian and reproductive responses to melatonin. J Clin Endocrinol Metab 76:295–301

    Google Scholar 

  • Wiechmann AF, Wirsig-Wiechmann CR (1992) Asymmetric distribution of melatonin receptors in the brain of the lizard Anolis carolinensis. Brain Res 593:281–286

    Google Scholar 

  • Wiechmann AF, Wirsig-Wiechmann CR (1993) Distribution of melatonin receptors in the brain of the frog Rana pipiens as revealed by in vitro autoradiography. Neuroscience 52:459–468

    Google Scholar 

  • Williams LM (1989) Melatonin binding sites in the rat brain and pituitary mapped by in vitro autoradiography. J Mol Endocrinol 3:71–75

    Google Scholar 

  • Williams LM, Morgan PJ (1988) Demonstration of melatonin-binding sites on the pars tuberalis of the rat. J Endocrinol 119:R1-R3

    Google Scholar 

  • Williams LM, Morgan PJ, Hastings MH, Lawson W, Davidson G, Howell HE (1989) Melatonin receptor sites in the Syrian hamster brain and pituitary. Localization and characterization using [125]iodomelatonin. J Neuroendocrinol 1:315–320

    Google Scholar 

  • Yous S, Andrieux J, Howell HE, Morgan PJ, Renard P, Pfeiffer B, Lesieur D, Guardiola-Lemaître B (1992) Novel naphthalencic ligands with high affinity for the melatonin receptor. J Med Chem 35:1484–1486

    Google Scholar 

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Masson-Pévet, M., George, D., Kalsbeek, A. et al. An attempt to correlate brain areas containing melatonin-binding sites with rhythmic functions: a study in five hibernator species. Cell Tissue Res 278, 97–106 (1994). https://doi.org/10.1007/BF00305781

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  • DOI: https://doi.org/10.1007/BF00305781

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