Skip to main content
SpringerLink
Log in

Pools of serotonin in the pineal gland of the mouse: The mammalian pinealocyte as a component of the diffuse neuroendocrine system

  • Published:
Cell and Tissue Research Aims and scope

Summary

In the pineal gland of the mouse the distribution of serotonin (5-HT) and its eventual relationships to a protein secretion were examined by means of fluorescence histochemical (Falck-Hillarp) and ultracytochemical (chromaffin and argentaffin) methods.

  1. (1)

    Yellow formaldehyde-induced fluorophores, characteristic of high concentrations of 5-HT, were found in pinealocytes, interstitial cells and sympathetic adrenergic nerve endings. The 5-HT content was studied according to the circadian variations and different drug treatments.

  2. (2)

    By use of ultracytochemical methods in untreated control mice precipitates indicative of 5-HT were found over dense-core vesicles (DCV; mean diameter: 100 nm) of the pinealocytes and the vesicular compartment of the sympathetic nerve fibers. After reserpine and p-CPA treatments, the reactivity of the DCV disappeared, but the protein secretion accumulated within the DCV was still present. After nialamide treatment the precipitates in the DCV increased and, similar to control mice, masked the protein secretion.

Taking into account the specificity and sensitivity of these three complementary methods, previous biochemical data in mammals and ultracytochemical data in submammalian vertebrates, synthesis, storage, catabolism and release of 5-HT in the mouse and hamster pineals are discussed at the cellular level. Different pools of 5-HT are present: agranular and granular in pinealocytes and sympathetic nerve endings; agranular in interstitial cells. In the mouse, only a small portion of the total 5-HT content appears to be secondarily taken up by the DCV. Within the DCV, 5-HT is possibly bound to a protein secretion of unknown significance (peptidergic neurohormone?). In the pinealocytes, which are sensitive to a large variety of inputs, processes of indole and protein secretion are found. These cells apparently are the recepto-secretory elements of the mammalian pineal gland. They can thus be classified as a member of the diffuse neuroendocrine system of the paraneuron group.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

References

  • Benson B, Krasovich M (1977) Circadian rhythm in the number of granulated vesicles in the pinealocytes of mice. Effects of sympathectomy and melatonin treatment. Cell Tissue Res 184:499–506

    Google Scholar 

  • Bertler Å, Falck B, Owman Ch (1962) Cellular localization of 5-hydroxytryptamine in the rat pineal gland. Kungl Fysiogr Sällsk Lund Förh 33:13–16

    Google Scholar 

  • Bertler Å, Falck B, Owman Ch (1964) Studies on 5-hydroxytryptamine stores in pineal gland of rat. Acta Physiol Scand Suppl 239, 63:1–18

    Google Scholar 

  • Björklund A, Owman Ch, West KA (1972) Peripheral sympathetic innervation and serotonin cells in the habenular region of the rat brain. Z Zellforsch 127:570–579

    Google Scholar 

  • Björklund A, Falck B, Lindvall O (1975) Microspectrofluorometric analysis of cellular monoamines after formaldehyde or glyoxylic acid condensation. In: Bradley PB (ed), Methods in Brain Research. Wiley J, London, pp 249–294

    Google Scholar 

  • Collin JP (1969) Contribution à l'étude de l'organe pinéal. De l'épiphyse sensorielle à la glande pinéale: modalités de transformation et implications fonctionnelles. Ann Stat Biol Besse-en-Chandesse, Suppl 1:1–359

    Google Scholar 

  • Collin JP (1971) Differentiation and regression of the cells of the sensory line in the epiphysis cerebri. In: Wolstenholme GEW, Knight J (eds) The pineal gland, Ciba Foundation Symposium 1970, Churchill JA, London, pp 79–125

    Google Scholar 

  • Collin JP (1977) La rudimentation des photorécepteurs dans l'organe pinéal des Vertébrés. In: Raynaud A (ed) Mécanismes de la rudimentation des organes chez les embryons de Vertébrés, Coll Int CNRS, 1976, Editions CNRS, Paris, Vol 266, pp 393–407

    Google Scholar 

  • Collin JP (1979) Recent advances in pineal cytochemistry. Evidence of the production of indoleamines and proteinaceous substances by rudimentary photoreceptor cells and pinealocytes of Amniota. In: Kappers J Ariëns, Pévet P (eds), Progress in Brain Research. The pineal gland of vertebrates including man. Elsevier/North-Holland, Amsterdam, Vol 52, pp 271–296

    Google Scholar 

  • Collin JP, Kappers J Ariëns (1968) Electron microscopic study of pineal innervation in lacertilians. Brain Res 11:85–106

    Google Scholar 

  • Collin JP, Meiniel A (1971) L'organe pinéal. Etudes combinées ultrastructurales, cytochimiques (monoamines) et expérimentales chez Testudo mauritanica. Grains denses des cellules de la lignée “sensorielle” chez les Vertébrés. Arch Anat Microsc Morphol Exp 60:269–304

    Google Scholar 

  • Collin JP, Oksche A (1981) Structure-function relationships in the nonmammalian pineal organ. In: Reiter RJ (ed), The pineal gland: anatomy and biochemistry. CRC Press, West Palm Beach (USA) (in press)

    Google Scholar 

  • Collin JP, Juillard MT, Falcon J (1977) Localization of 5-hydroxytryptamine and protein(s) in the secretion granules of the rudimentary photoreceptor cells in the pineal of Lacerta. J Neurocytol 6:541–554

    Google Scholar 

  • Collin JP, Juillard MT, Brisson P (1978) Ultracytochemistry and pharmacology of the specific secretory granules (SG) in the pineal organ of some reptiles, birds and mammals. In: Nir I, Reiter RJ, Wurtman RJ (eds) Journal of Neural Transmission, The pineal gland. Springer-Verlag, Wien-New York, Suppl 13, p 359

    Google Scholar 

  • Corrodi H, Jonsson G (1967) The formaldehyde fluorescence method for the histochemical demonstration of biogenic monoamines. A review of the methodology. J Histochem Cytochem 15:65–78

    Google Scholar 

  • Dogterom J, Snijdewint FGM, Pévet P, Swaab DF (1980) Studies on the presence of vasopressin, oxytocin and vasotocin in the pineal gland, subcommissural organ and fetal pituitary gland: failure to demonstrate vasotocin in mammals. J Endocrinol 84:115–123

    Google Scholar 

  • Ebels I, Benson B (1978) A survey of the evidence that unidentified pineal substances affect the reproductive system in mammals. In: Reiter RJ, Hubinont PO (eds) Progress in reproductive biology. The Pineal and Reproduction. Karger S, Basel München, Vol 4, pp 51–89

    Google Scholar 

  • Falck B, Owman Ch (1968) 5-hydroxytryptamine and related amines in endocrine cell systems. In: Advances in pharmacology, Academic Press, New York-London, Vol 6, pp 211–231

    Google Scholar 

  • Falck B, Owman Ch, Rosengren E (1966) Changes in rat pineal stores of 5-hydroxytryptamine after inhibition of its synthesis or break-down. Acta Physiol Scand 67:300–305

    Google Scholar 

  • Falcon J, Juillard MT, Collin JP (1980a) L'organe pinéal du Brochet (Esox lucius, L). IV. Sérotonine endogéne et activité monoamine oxydasique; étude histochimique, ultracytochimique et pharmacologique. Reprod Nutr Dévelop 20:139–154

    Google Scholar 

  • Falcon J, Juillard MT, Collin JP (1980b) L'organe pinéal du Brochet (Esox lucius, L). V. Etude radioautographique de l'incorporation in vivo et in vitro de précurseurs indoliques. Reprod Nutr Develop 20:(in press)

  • Fujita T (1977) Concept of paraneurons. Arch Histol Jpn, Suppl 477, 40:1–12

    Google Scholar 

  • Fujita T, Kobayashi S (1979) Current views on the paraneurone concept. Tins 2:27–30

    Google Scholar 

  • Gómez Dumm CLA, Iturizza FC (1979) On the presence of conspicuous electron dense bodies in the pinealocytes of the pig. Cell Tissue Res 201:507–510

    Google Scholar 

  • Håkanson R, Owman Ch (1966) Pineal dopa decarboxylase and monoamine oxidase activities as related to the monoamine stores. J Neurochem 13:597–605

    Google Scholar 

  • Hartwig HG, Brisson P, Lyncker I, Collin JP (1980) Aminergic systems in pulmonate gastropod molluscs. III. Microspectrofluorometric characterization of the monoamines in the reproductive system. Cell Tissue Res 210:223–234

    Google Scholar 

  • Hori S, Kuroda Y, Saito K, Ohotani S (1976) Subcellular localization of tryptophan-5-mono-oxygenase in bovine pineal glands and raphe nuclei. J Neurochem 27:911–914

    Google Scholar 

  • Ito T, Matsushima S (1967) A quantitative morphological study of the postnatal development of the pineal body of the mouse. Anat Rec 159:447–452

    Google Scholar 

  • Ito T, Matsushima S (1968) Electron microscopic observations on the mouse pineal with particular emphasis on its secretory nature. Arch Histol Jpn 30:1–15

    Google Scholar 

  • Jaim-Etcheverry JG, Zieher LM (1968) Cytochemistry of 5-hydroxytryptamine at the electron microscope level. II. Localization in the autonomic nerves of the rat pineal gland. Z Zellforsch 86:393–400

    Google Scholar 

  • Juillard MT (1979a) The proteinaceous content and possible physiological significance of dense-cored vesicles in hamster and mouse pinealocytes. Ann Biol anim Bioch Biophys 19:413–428

    Google Scholar 

  • Juillard MT (1979b) Ultrastructural localization of MAO activity in the pineal organ of sauropsida. A preliminary study. In: Kappers J Ariëns, Pévet P (eds) Progress in Brain Research, The pineal gland of vertebrates including man. Elsevier/North Holland, Amsterdam, Vol 52, pp 297–301

    Google Scholar 

  • Juillard MT, Collin JP (1976) L'organe pinéal aviaire: étude ultracytochimique et pharmacologique d'un “pool” granulaire de 5-hydroxytryptamine chez la Perruche (Melopsittacus undulatus, Shaw). J Microsc Biol Cell 26:133–138

    Google Scholar 

  • Juillard MT, Collin JP (1979) Membranous sites of oxidative deamination: a comparison between ultracytochemical and radioautographic studies in the pineal organ of the wall lizard and the parakeet. Biol Cell 36:29–35

    Google Scholar 

  • Juillard MT, Hartwig HG, Collin JP (1977) The avian pineal organ. Distribution of endogenous monoamines; a fluorescence microscopic, microspectrofluorimetric and pharmacological study in the parakeet. J Neural Transm 40:269–287

    Google Scholar 

  • Kappers J Ariëns (1969) The mammalian pineal organ. J Neuro-Visc Rel, Suppl 9:140–184

    Google Scholar 

  • Kappers J Ariëns (1976) The mammalian pineal gland, a survey. Acta Neurochir 34:109–149

    Google Scholar 

  • Kappers J Ariëns (1978) Localization of indoleamine and protein synthesis in the mammalian pineal gland (Chairman's introduction). In: Nir I, Reiter RJ, Wurtman RJ (eds) Journal of Neural Transmission. The pineal gland. Springer Verlag, Wien-New York, Suppl 13, pp 13–24

    Google Scholar 

  • Kappers J Ariëns (1979) Short history of pineal discovery and research. In: Kappers J Ariëns, Pévet P (eds) Progress in Brain Research. The pineal gland of vertebrates including man. Elsevier/North-Holland, Amsterdam, Vol 52, pp 3–22

    Google Scholar 

  • Karasek M, Mark K (1978) Influence of gonadotropic hormones on the ultrastructure of rat pinealocytes. Cell Tissue Res 188:133–141

    Google Scholar 

  • Koe BK, Weissman A (1966) p-Chlorophenylalanine: a specific depletor of brain serotonin. J Pharmacol Exp Ther 154:499–516

    Google Scholar 

  • Krasovich M, Benson B (1979) Effects of reserpine and p-chlorophenylalanine on the circadian rhythm of granulated vesicles in the pinealocytes of mice. Cell Tissue Res 203:457–467

    Google Scholar 

  • Lu KS, Lin HS (1979) Cytochemical studies on cytoplasmic granular elements in the hamster pineal gland. Histochemistry 61:177–187

    Google Scholar 

  • Machado CRS, Wragg LE, Machado ABM (1968) A histochemical study of sympathetic innervation and 5-hydroxytryptamine in the developing pineal body of the rat. Brain Res 8:310–318

    Google Scholar 

  • Matsushima S, Reiter RJ (1975) Comparative ultrastructural studies of the pineal gland of rodents. In: Hess M (ed) Ultrastructure of endocrine and reproductive organs. Wiley J, New York, pp 335–356

    Google Scholar 

  • Matsushima S, Morisawa Y (1978) Effects of acute cold exposure on the ultrastructure of the mouse pinealocyte. Cell Tissue Res 195:461–469

    Google Scholar 

  • Matsushima S, Kachi T, Mukai S, Morisawa Y (1977) Functional relationships between sympathetic nerves and pinealocytes in the mouse pineal: quantative electron microscopic observations. Arch Histol Jpn Suppl 40:279–291

    Google Scholar 

  • Møller M, van Deurs B, Westergaard E (1978) Vascular permeability to proteins and peptides in the mouse pineal gland. Cell Tissue Res 195:1–15

    Google Scholar 

  • Müller J, Da Lage C (1977) Ultracytochemical demonstration of monoamine oxidase activity in nervous and non-nervous tissues of the rat. J Histochem Cytochem 25:337–348

    Google Scholar 

  • Nielsen JT, Møller M (1978) Innervation of the pineal gland in the mongolian gerbil (Meriones unguiculatus). A fluorescence microscopical study. Cell Tissue Res 187:235–250

    Google Scholar 

  • Oksche A (1971) Sensory and glandular elements of the pineal organ. In: Wolstenholme GEW, Knight J (eds) The Pineal Gland. A Ciba Foundation Symposium 1970. Churchill JA, London, pp 127–146

    Google Scholar 

  • Orts RJ, Liao TH, Sartin JL, Bruot BC (1980) Isolation, purification and amino acid sequence of a tripeptide from bovine pineal tissue displaying antigonadotropic properties. Biochem Biophys Acta 628:201–209

    Google Scholar 

  • Owman Ch (1964) New aspects of the mammalian pineal gland. Acta Physiol Scand 63, Suppl 240: 1–40

    Google Scholar 

  • Owman Ch (1965) Localization of neuronal and parenchymal monoamines under normal and experimental conditions in the mammalian pineal gland. In: Kappers J Ariëns, Schadé JP (eds) Progress in Brain Research. Structure and function of the epiphysis cerebri. Elsevier, Amsterdam, Vol 10:pp 423–453

    Google Scholar 

  • Owman Ch (1968) On the significance of the 5-hydroxytryptamine stores in pineal gland. In: Advances in pharmacology. Academic Press, New York London, Vol. 6, pp 167–169

    Google Scholar 

  • Pavel S (1978) Arginine vasotocin as a pineal hormone. In: Nir I, Reiter RJ, Wurtman RJ (eds) Journal of Neural Transmission. The pineal gland. Springer-Verlag, Wien New York, Suppl 13, pp 135–155

    Google Scholar 

  • Pearse AGE, Takor Takor T (1979) Embryology of the diffuse neuroendocrine system and its relationship to the common peptides. Fed Proc 38:2288–2294

    Google Scholar 

  • Pellegrino de Iraldi A (1969) Granulated vesicles in the pineal gland of the mouse. Z Zellforsch 101:408–418

    Google Scholar 

  • Pévet P (1979) Secretory processes in the mammalian pinealocytes under natural and experimental conditions. In: Kappers J Ariëns, Pévet P (eds) Progress in Brain Research. The pineal gland of vertebrates including man. Elsevier/North Holland, Amsterdam, Vol 52, pp 149–194

    Google Scholar 

  • Pévet P, Karasek M (1977) Are the pineal active compounds of mammals proteinaceous in nature? An ultrastructural contribution. Acta Med Pol 18:351–353

    Google Scholar 

  • Pévet P, Buijs RM, Dogterom J, Vivien-Roels B, Holder FC, Guerné JM, Reinharz A, Swaab DF, Ebels I, Neacsu C (1980a) Peptides in the mammalian pineal gland. VI. Internat Congress Endocr, Melbourne-Thredbo, February 17–20 (in press)

  • Pévet P, Ebels I, Swaab DF, Mud MT, Arimura A (1980b) Presence of AVT-, α-MSH-, LHRH- and somatostatin-like compounds in the rat pineal gland and their relationship with the UMO5R pineal fraction. Cell Tissue Res 206:341–353

    Google Scholar 

  • Pévet P, Reinharz AC, Dogterom J (1980c) Neurophysins, vasopressin and oxytocin in the bovine pineal gland. Neurose Lett 16:301–306

    Google Scholar 

  • Quay WB (1974) Pineal chemistry. Thomas CC, Springfield (USA)

    Google Scholar 

  • Reiter RJ, Lukaszyk AJ, Vaughan MK, Blask DE (1976) New horizons of pineal research. Am Zool 16:93–101

    Google Scholar 

  • Sheridan MN, Sladek JR Jr (1975) Histofluorescence and ultrastructural analysis of hamster and monkey pineal. Cell Tissue Res 164:145–152

    Google Scholar 

  • Shibuya H, Toru M, Watanabe S (1978) A circadian rhythm of tryptophan hydroxylase in rat pineals. Brain Res 138:364–368

    Google Scholar 

  • Tilders FJH, Ploem JS, Smelik PG (1974) Quantitative microfluorimetric studies on formaldehydeinduced fluorescence of 5-hydroxytryptamine in the pineal gland of the rat. J Histochem Cytochem 22:967–975

    Google Scholar 

  • Ueck M (1977) The pinealocyte. A paraneuron? A review. Arch Histol Jpn, Suppl 1977, 40:261–278

    Google Scholar 

  • Ueck M, Wake K (1979) The pinealocyte. A paraneuron. In: Kapers J Ariëns, Pévet P (eds) Progress in Brain Research. The pineal gland of vertebrates including man. Elsevier/North-Holland, Vol 52, pp 141–147

  • Upson RH, Benson B (1977) Effects of binding on the ultrastructure of mouse pinealocytes with particular emphasis on the dense-cored vesicles. Cell Tissue Res 183:491–498

    Google Scholar 

  • Upson RH, Benson B, Satterfield V (1976) Quantitation of ultrastructural changes in the mouse pineal in response to continuous illumination. Anat Rec 184:311–324

    Google Scholar 

  • Veen Th van, Brackman M, Moghimzadeh E (1978) Post-natal development of the pineal organ in the hamsters Phodopus sungorus and Mesocricetus auratus. A fluorescence microscopic and microspectrofluorometric investigation. Cell Tissue Res 189:241–250

    Google Scholar 

  • Wurtman RJ, Axelrod J, Kelly DE (1968) The pineal. Academic Press, New York London

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Zoologie et Biologie Cellulaire et LA-CNRS N∘ 290, Poitiers, France

    Marie-Thérèse Juillard & Jean-Pierre Collin

Authors
  1. Marie-Thérèse Juillard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Pierre Collin
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Dedicated in gratitude and friendship to Professor J. Ariëns Kappers on the occasion of his 70th birthday

This work was supported by INSERM (contract n∘ 791539 4). The authors acknowledge the technical assistance of G. Baudu, F. Chevalier, and C. Jougla for the photographic work and D. Decourt for typing the manuscript

Rights and permissions

Reprints and permissions

About this article

Cite this article

Juillard, MT., Collin, JP. Pools of serotonin in the pineal gland of the mouse: The mammalian pinealocyte as a component of the diffuse neuroendocrine system. Cell Tissue Res. 213, 273–291 (1980). https://doi.org/10.1007/BF00234787

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00234787

Key words

Search

Navigation