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5′-Nucleotidase activity in the pineal organ of the pike

An electron-microscopic study

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Summary

To date, it is still unknown whether the metabolism of purine nucleotides and nucleosides plays an important role in the pineal organ of lower vertebrates. We have therefore investigated the sites of 5′-nucleotidase activity in the pineal organ of the pike (Esox lucius L.). Various ultracytochemical procedures were used. An intense ecto-5′-nucleotidase activity was characteristic of the entire plasma membrane of the phototransducers (cone-like and modified photoreceptor elements) and the interstitial cells, with exception of the portions facing the basal lamina of the pericapillary spaces. Additionally, intracellular sites of activity were also visualized in the inner segment and the pedicle of the phototransducers. Most of the intracellular deposits were apparently cytosolic and only few seemed to be associated with the membrane of the clear “synaptic” vesicles of the pedicle. Phagocytotic cells in the pineal lumen also showed a strong enzymatic activity on the outer surface of their plasmalemma (in ectoposition). This was apparently not the case for the cell types of the tissues surrounding the pineal vesicle. The present study emphasizes the importance of the occurrence and metabolism of purine nucleotides and nucleosides in a photoreceptive pineal organ.

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References

  • Andersson Forsman C, Gustafsson LE (1985) Cytochemical localization of 5′-nucleotidase in the enteric ganglia and in smooth muscle cells of the guinea-pig. J Neurocytol 14:551–562

    Google Scholar 

  • Bisserbe JC, Patel J, Marangos PJ (1985) Autoradiographic localization of adenosine uptake sites in rat brain using [3H]nitrobenzylthioinosine. J Neurosci 5:544–550

    Google Scholar 

  • Cobbs WH, Barkdoll III AE, Pugh Jr EN (1985) Cyclic GMP increases photocurrent and light sensitivity of retinal cones. Nature 317:64–66

    Google Scholar 

  • Cohen P, Houslay MD (1985) Molecular mechanisms of transmembrane signalling. Molecular aspects of cellular regulation. Vol. 4., Elsevier, Amsterdam pp 1–487

    Google Scholar 

  • Collin JP, Oksche A (1981) Structural and functional relationships in the nonmammalian pineal organ. In: Reiter RJ (ed) The pineal gland, Vol. 1: Anatomy and biochemistry. CRC Press, Boca Raton, pp 27–67

    Google Scholar 

  • Collin JP, Brisson P, Falcon J, Voisin P (1986a) 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

    Google Scholar 

  • Collin JP, Meissl H, Voisin P, Brisson P, Falcon J (1986b) Rhythmic signals of pineal transducers: physiological, biochemical and cytochemical evidence. In: Reiter RJ, Karasek M (eds) Advances in pineal research. J Libbey & Co. Ltd, London, pp 41–50

    Google Scholar 

  • Collin JP, Mirshahi M, Brisson P, Falcon J, Guerlotté J, Faure JP (1986c) Pineal-retinal molecular relationships: distribution of “S-antigen” in the pineal complex. Neuroscience 19:657–666

    Google Scholar 

  • Deguchi T (1979) 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

    Google Scholar 

  • Falcon J (1979) L'organe pineal du Brochet (Esox lucius, L.). II. Etude en microscopie électronique de la différenciation et de la rudimentation partielle des photorécepteurs; conséquences possibles sur l'élaboration des messages photosensoriels. Ann Biol Anim Bioch Biophys 19:661–688

    Google Scholar 

  • Falcon J, Collin JP (1985) In vitro uptake and metabolism of [3H] indole compounds in the pineal organ of the pike. II. A radioautographic study. J Pineal Res 2:357–373

    Google Scholar 

  • 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 144:127–137

    Google Scholar 

  • Falcon J, Balemans MGM, Benthem J van, Collin JP (1985) In vitro uptake and metabolism of [3H]-indole compounds in the pineal organ of the pike. I. A radiochromatographic study. J Pineal Res 2:341–356

    Google Scholar 

  • Falcon J, Voisin P, Guerlotté J, Collin JP (1986) Photoreceptors in the teleost pineal organ. Daily fluctuations of indole metabolism. Ann Endocrinol 47:65–66

    Google Scholar 

  • Falcon J, Guerlotté JF, Voisin P, Collin JP (1987) Rhythmic melatonin biosynthesis in a photoreceptive pineal organ: a study in the pike. Neuroendocrinology 45:479–486

    Google Scholar 

  • Fredholm BB, Sollevi A (1986) Cardiovascular effects of adenosine. Clin Physiol 6:1–21

    Google Scholar 

  • Fukui H, Shichi H (1981) 5′-nucleotidases of retinal rod membranes. Arch Biochem Biophys 212:78–87

    Google Scholar 

  • Fukui H, Shichi H (1982) Soluble 5′-nucleotidase: purification and reversible binding to photoreceptor membranes. Biochemistry 21:3677–3681

    Google Scholar 

  • Gern WA, Karn CM (1983) Evolution of melatonin's functions and effects. Pineal Res Rev 1:49–90

    Google Scholar 

  • Harb J, Meflah K, Bernard S (1985) Structural differences between plasma-membrane 5′-nucleotidase in different cell types as evidenced by antibodies. Biochem J 232:859–862

    Google Scholar 

  • Higley HR, McNulty JA, Rowden G (1984) Glial fibrillary acidic protein and S-100 protein in pineal supportive cells: an electron microscopic study. Brain Res 304:117–120

    Google Scholar 

  • Jarviss SM, Ng AS (1985) Identification of the adenosine uptake sites in guinea pig brain. J Neurochem 44:183–188

    Google Scholar 

  • Kavaliers M (1979) The pineal organ and circadian organization of teleost fish. Rev Can Biol 38:281–292

    Google Scholar 

  • Klein DC, Auerbach DA, Namboodiri MAA, Wheler GHT (1981) Indole metabolism in the mammalian pineal gland. In: Reiter RJ (ed) The pineal gland, Vol. 1: Anatomy and biochemistry. CRC Press, Boca Raton, pp 199–227

    Google Scholar 

  • Kreutzberg GW, Barron KD (1978) 5′-nucleotidase of microglial cells in the facial nucleus during axonal reaction. J Neurocytol 7:601–610

    Google Scholar 

  • Kreutzberg GW, Hussain ST (1982) Cytochemical heterogeneity of the glial plasma membrane: 5′-nucleotidase in retinal Müller cells. J Neurocytol 11:53–64

    Google Scholar 

  • Kreutzberg GW, Hussain ST (1984) Cytochemical localization of 5′-nucleotidase activity in retinal photoreceptor cells. Neuro science 11:857–866

    Google Scholar 

  • Kreutzberg GW, Barron KD, Schubert P (1978) Cytochemical localization of 5′-nucleotidase in glial plasma membranes. BrainRes 158:247–257

    Google Scholar 

  • Kreutzberg GW, Heymann D, Reddington M (1986) 5′-Nucleotidase in the nervous system. In: Kreutzberg GW et al. (s) Cellular biology of ectoenzymes. Springer, Berlin Heidelberg New York, pp 147–164

    Google Scholar 

  • Meissl H, Dodt E (1981) Comparative physiology of pineal photoreceptor organs. In: Oksche A, Pévet P (eds) The Pineal Organ: Photobiology-Biochronometry-Endocrinology. Elsevier/NorthHolland Biomedical Press, Amsterdam, pp 61–80

    Google Scholar 

  • O'Brien PJ, Klein DC (1986) Pineal and retinal relationships. Academic Press, New York, pp 1–442

    Google Scholar 

  • Oksche A, Korf H-W, Rodriguez EM (1987) Pinealocytes as photoneuroendocrine units of neuronal origin: concepts and evidence. In: Reiter RJ, Fraschini F (eds) John Libbey & Co, London-Paris, pp 1–18

  • Phillis JW, Wu PH (1981) The role of adenosine and its nucleotides in central synaptic transmission. Prog Neurobiol 16:187–239

    Google Scholar 

  • Ralph CL (1983) Evolution of pineal control of endocrine function in lower vertebrates. Am Zool 23:597–605

    Google Scholar 

  • Robinson JM, Karnovsky MJ (1983) Ultrastructural localization of 5′-nucleotidase in guinea pig neutrophils based upon the use of cerium as capturing agent. J Histochem Cytochem 31:1190–1196

    Google Scholar 

  • Schubert P, Lee K, Kreutzberg GW (1982) Neuronal release of adenosine derivatives and modulation of signal processing in the CNS. Prog Brain Res 55:225–237

    Google Scholar 

  • Stanley KK, Edwards MR, Luzio JP (1980) Subcellular distribution and movement of 5′-nucleotidase in rat cells. Biochem J 186:59–69

    Google Scholar 

  • Ueno S, Bambauer HJ, Umar H, Ueck M (1984) A new histo and cytochemical method for demonstration of cyclic 3′–5′-nucleotide phosphodiesterase activity in retinal rod photoreceptor cells of the rat. Histochemistry 81:445–451

    Google Scholar 

  • Underwood H (1985) Pineal melatonin rhythms in the lizard Anolis carolinensis: effects of light and temperature cycles. J Comp Physiol A 157:57–65

    Google Scholar 

  • Voisin P, Martin C, Collin JP (1987) α 2-Adrenergic regulation of arylalkylamine N-acetyltransferase in organ cultured chick pineal gland: characterization with agonists and modulation of experimentally stimulated enzyme activity. J Neurochem (in press)

  • Wainwright SD, Wainwright LK (1984) Relationship between cycles in level of serotonin N-acetyltransferase activity and cyclic GMP content of cultured chick pineal glands. J Neurochem 43:358–363

    Google Scholar 

  • Wessberg P, Hedner J, Hedner T, Persson B, Jonason J (1985) Adenosine mechanisms in the regulation of breathing in the rat. Eur J Pharmacol 106:59–67

    Google Scholar 

  • Widnell CC, Schneider YJ, Pierre B, Baugduin P, Trouet A (1982) Evidence for a continual exchange of 5′-nucleotidase between the cell surface and cytoplasmic membranes in cultured rat fibroblasts. Cell 28:61–70

    Google Scholar 

  • Yamashina S, Katsumata O, Wada I, Kalo K (1986) Electron microscopic localization of 5′-nucleotidase in rat salivary glands. Comparative enzymeand immunohistochemical studies. Histochemistry 84:231–236

    Google Scholar 

  • Yu LW, Fager RS (1983) Localization and properties of bovine photoreceptor 5′-nucleotidase. Am J Physiol 244:C89-C99

    Google Scholar 

Download references

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Authors and Affiliations

  1. Laboratoire de Biologie Cellulaire, U.A. CNRS 290 et S.U.M.E.B., Université de Poitiers, Poitiers, France

    Jacky Falcon, Colette Besse, Jérôme Guerlotté & Jean-Pierre Collin

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  1. Jacky Falcon
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  2. Colette Besse
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  3. Jérôme Guerlotté
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  4. Jean-Pierre Collin
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Falcon, J., Besse, C., Guerlotté, J. et al. 5′-Nucleotidase activity in the pineal organ of the pike. Cell Tissue Res. 251, 495–502 (1988). https://doi.org/10.1007/BF00215859

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  • DOI: https://doi.org/10.1007/BF00215859

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