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Pinealocytes immunoreactive with antisera against secretory glycoproteins of the subcommissural organ: A comparative study

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Summary

By means of light-microscopic immunocyto-chemistry two polyclonal antibodies (AFRU, ASO; see p. 470) directed against secretory glycoproteins of the subcom-missural organ were shown to cross-react with cells in the pineal organ of lamprey larvae, coho salmon, a toad, two species of lizards, domestic fowl, albino rat and bovine (taxonomic details, see below). The AFRU-immunoreactive cells were identified as pinealocytes of the receptor line (pineal photoreceptors, modified photoreceptors or classical pinealocytes, respectively) either due to their characteristic structural features or by combining AFRU-immunoreaction with S-antigen and opsin immunocytochemistry in the same or adjacent sections. Depending on the species, AFRU- or ASO-immunoreactions were found in the entire perikaryon, inner segments, perinuclear area, and in basal processes facing capillaries or the basal lamina. In most cases, only certain populations of pinealocytes were immunolabeled; these cells were arranged in a peculiar topographical pattern. In lamprey larvae, immunoreactive pinealocytes were observed only in the pineal organ, but not in the parapineal organ. In coho salmon, the immunoreaction occurred in S-antigen-positive pinealocytes of the pineal end-vesicle, but was absent from S-antigen-immunoreactive pinealocytes of the stalk region. In the rat, AFRU-immunoreaction was restricted to S-antigen-immunoreactive pinealocytes found in the deep portion of the pineal organ and the habenular region. These findings support the concept that several types of pinealocytes exist, which differ in their molecular, biochemical and functional features. They also indicate the possibility that the AFRU- and ASO-immunoreactive material found in certain pinealocytes might represent a proteinaceous or peptidic compound, which is synthesized and released from a specialized type of pinealocyte in a hormone-like fashion. This cell type may share functional characteristics with peptidergic neurons or paraneurons.

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References

  • Baker JR (1946) Cytological technique; the principles underlying routine methods. John Wiley and Sons, New York

    Google Scholar 

  • Chan-Palay V, Jonsson G, Palay SL (1978) Serotonin and substance P coexist in neurons of the rat's central nervous system. Proc Natl Acad Sci USA 75:1582–1586

    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. Prog Brain Res 52:271–296

    Google Scholar 

  • Collin JP (1981) New data and vistas on the mechanisms of secretion of proteins and indoles in the mammalian pinealocyte and its phylogenetic precursors; the pinealin hypothesis and preliminary comments on membrane traffic. In: Oksche A, Pévet P (eds) The pineal organ: photobiology — biochronometry — endocrinology. Elsevier, Amsterdam, pp 187–210

    Google Scholar 

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

    Google Scholar 

  • Ebels I (1979) A chemical study of some biologically active pineal fractions. Prog Brain Res 52:309–321

    Google Scholar 

  • Ekström P, Foster RG, Korf HW, Schalken JJ (1987) Antibodies against retinal photoreceptor-specific proteins reveal axonal projections from the photosensory pineal organ in teleosts. J Comp Neurol 265:25–33

    Google Scholar 

  • Falcon J (1979) Unusual distribution of neurons in the pike pineal organ. Prog Brain Res 52:89–91

    Google Scholar 

  • Foster RG, Korf HW, Schalken JJ (1987) Immunocytochemical markers revealing retinal and pineal but not hypothalamic photoreceptor systems in the Japanese quail. Cell Tissue Res 248:161–167

    Google Scholar 

  • Gonzalez CB, Rodríguez EM (1980) Ultrastructure and immunocytochemistry of neurons in the supraoptic and paraventricular nuclei of the lizard Liolaemus cyanogaster. Evidence for the intracisternal location of the precursor of neurophysin. Cell Tissue Res 207:463–477

    Google Scholar 

  • Hewing M, Bergmann M (1985) Differential permeability of pineal capillaries to lanthanum ion in rat (Rattus norvegicus), gerbil (Meriones unguiculatus) and golden hamster (Mesocricetus auratus). Cell Tissue Res 241:149–154

    Google Scholar 

  • Hökfelt T, Johansson O, Goldstein M (1984) Chemical anatomy of the brain. Science 225:1326–1334

    Google Scholar 

  • Iwanaga T, Yui R, Kuramoto H, Fujita T (1987) The paraneuron concept and its implication in neurobiology. In: Scharrer B, Korf HW, Hartwig HG (eds) Functional morphology of neuroendocrine systems. Evolutionary and environmental aspects. Springer, Berlin Heidelberg New York, pp 139–148

    Google Scholar 

  • Korf HW (1986) Zur Frage photoneuroendokriner Zellen und Systeme: Vergleichende Untersuchungen am Pinealkomplex. Habilitationsschrift, Fachbereich Humanmedizin, Giessen

    Google Scholar 

  • Korf HW, Ekström P (1987) Photoreceptor differentiation and neuronal organization of the pineal organ. In: Trentini GP, Gaetani C de, Pévet P (eds) Fundamentals and clinics in pineal research. Raven Press, New York, pp 35–47

    Google Scholar 

  • Korf HW, Møller M (1985) The central innervation of the mammalian pineal organ. In: Mess B, Rúzsás C, Tima L, Pévet P (eds) Current state of pineal research. Akadémiai Kiadó, Budapest, pp 47–69

    Google Scholar 

  • Korf HW, Oksche A (1986) The pineal organ. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology. Fundamentals and biomedical implications. Vol. 1. Morphological considerations. Academic Press, Orlando, pp 105–145

    Google Scholar 

  • Korf HW, Møller M, Gery I, Zigler JS, Klein DC (1985a) Immunocytochemical demonstration of retinal S-antigen in the pineal organ of four mammalian species. Cell Tissue Res 239:81–85

    Google Scholar 

  • Korf HW, Foster RG, Ekström P, Schalken JJ (1985b) Opsin-like immunoreaction in the retinae and pineal organs of four mammalian species. Cell Tissue Res 242:645–648

    Google Scholar 

  • Korf HW, Oksche A, Ekström P, van Veen T, Zigler JS, Gery I, Stein P, Klein DC (1986a) S-antigen immunocytochemistry. In: O'Brien P, Klein DC (eds) Pineal and retinal relationships. Academic Press, Orlando, pp 343–355

    Google Scholar 

  • Korf HW, Oksche A, Ekström P, Gery I, Zigler JS, Klein DC (1986b) Pinealocyte projections into the mammalian brain revealed with S-antigen antiserum. Science 231:735–737

    Google Scholar 

  • Korf HW, Panzica GC, Viglietti-Panzica C, Oksche A (1988) Pattern of peptidergic neurons in the avian brain: clusters — local circuitries — projections. Bas Appl Histochem 31:55–75

    Google Scholar 

  • Meiniel R, Molat JL, Meiniel A (1986) Concanavalin A-binding glycoproteins in the subcommissural and the pineal organ of the sheep (Ovis aries). Cell Tissue Res 245:605–613

    Google Scholar 

  • Meiniel R, Duchier N, Meiniel A (1987) Glycoprotein synthesis in the diencephalic roof. A histochemical and cytochemical study using lectins and specific antibodies. In: Trentini GP, Gaetani C de, Pévet P (eds) Fundamentals and clinics in pineal reserach. Raven Press, New York, pp 49–52

    Google Scholar 

  • Oksche A (1971) Sensory and glandular elements of the pineal organ. In: Wolstenholme GEW, Knight J (eds) The pineal gland. Churchill-Livingstone, London, pp 127–146

    Google Scholar 

  • Oksche A (1987) Neuronal characteristics of pinealocytes: reflections — concepts — prospects. In: Trentini GP, Gaetani C de, Pévet P (eds) Fundamentals and clinics in pineal research. Raven Press, New York, pp 3–10

    Google Scholar 

  • Oksche A, Hartwig HG (1979) Pineal sense organs — components of photoneuroendocrine systems. Prog Brain Res 52:113–130

    Google Scholar 

  • Oksche A, Korf HW, Rodríguez EM (1987) Pinealocytes as photoneuroendocrine units of neuronal origin: concepts and evidence. In: Reiter RJ, Fraschini F (eds) Advances in pineal research, Vol. 2. John Libbey, London, pp 1–18

    Google Scholar 

  • Pévet P (1977) The pineal gland of the mole (Talpa europaea L.). IV. Effect of pronase on material present in cisternae of the granular endoplasmic reticulum of pinealocytes. Cell Tissue Res 182:215–219

    Google Scholar 

  • Pévet P (1979) Secretory processes in the mammalian pinealocyte under natural and experimental conditions. Prog Brain Res 52:149–192

    Google Scholar 

  • Pévet P (1981) Peptides in the pineal gland of vertebrates. Ultrastructural, histochemical, immunocytochemical and radioimmunological aspects. In: Oksche A, Pévet P (eds) The pineal organ: photobiology — biochronometry — endocrinology. Elsevier, Amsterdam, pp 211–235

    Google Scholar 

  • Quay WB (1965) Histological structure and cytology of the pineal organ in birds and mammals. Prog Brain Res 10:49–84

    Google Scholar 

  • Quay WB (1974) Pineal chemistry in cellular and physiological mechanisms. Thomas, Springfield

    Google Scholar 

  • Quay WB (1986) Indole biochemistry in pineal and retinal mechanisms. In: O'Brien P, Klein DC (eds) Pineal and retinal relationships. Academic Press, Orlando, pp 107–118

    Google Scholar 

  • Rodríguez EM, Oksche A, Hein S, Rodríguez S, Yulis R (1984a) Comparative immunocytochemical study of the subcommissural organ. Cell Tissue Res 237:427–441

    Google Scholar 

  • Rodríguez EM, Oksche A, Hein S, Rodríguez S, Yulis R (1984b) Spatial and structural interrelationships between secretory cells of the subcommissural organ and blood vessels. An immunocytochemical study. Cell Tissue Res 237:443–449

    Google Scholar 

  • Rodríguez EM, Yulis R, Peruzzo B, Alvial G, Andrade R (1984c) Standardization of various applications of methacrylate embedding and silver methenamine for light and electron microscopy immunocytochemistry. Histochemistry 81:253–263

    Google Scholar 

  • Rodríguez EM, Hein S, Rodríguez S, Herrera H, Peruzzo B, Nualart F, Oksche A (1987) Analysis of secretory products of the subcommissural organ. In: Scharrer B, Korf HW, Hartwig HG (eds) Functional morphology of neuroendocrine systems. Evolutionary and environmental aspects. Springer, Berlin, pp 189–201

    Google Scholar 

  • Scharrer B (1978) Peptidergic neurons: facts and trends. Gen Comp Endocrinol 34:52–60

    Google Scholar 

  • Scharrer E (1964) Photo-neuro-endocrine systems: general concepts. Ann N Y Acad Sci 117:13–22

    Google Scholar 

  • Steinbusch HWM (1984) Serotonin-immunoreactive neurons and their projections in the CNS. In: Björklund A, Hökfelt T, Kuhar MJ (eds) Handbook of chemical neuroanatomy, Vol. 3. Classical transmitters and transmitter receptors in the CNS, part II. Elsevier, Amsterdam, pp 68–125

    Google Scholar 

  • Sternberger LA, Hardy PH, Cuculis JJ, Meyer HG (1970) The unlabeled antibody enzyme method of immunohistochemistry. Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem 18:315–333

    Google Scholar 

  • Sheridan MN, Reiter RJ (1970) Observations on the pineal system in the hamster. I. Relations of the superficial and deep pineal to the epithalamus. J Morphol 131:153–162

    Google Scholar 

  • Sutherland RJ (1982) The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 6:1–13

    Google Scholar 

  • Ueck M, Wake K (1977) The pinealocyte — a paraneuron? Arch Histol Jpn 40 [Suppl]: 261–278

    Google Scholar 

  • Ueck M, Wake K (1979) The pinealocyte: a paraneuron. Prog Brain Res 52:141–147

    Google Scholar 

  • Veen T van, Elofsson R, Hartwig HG, Gery I, Mochizuki M, Klein DC (1986) Retinal S-antigen: immunocytochemical and immunochemical studies on the distribution in animal photoreceptors and pineal organs. Exp Biol 45:15–25

    Google Scholar 

  • Vigh B, Vigh-Teichmann I (1981) Light- and electron microscopic demonstration of immunoreactive opsin in the pinealocytes of various vertebrates. Cell Tissue Res 221:451–463

    Google Scholar 

  • Vigh-Teichmann I, Vigh B (1983) The system of cerebrospinal fluid-contacting neurons. Arch Histol Jpn 46:427–468

    Google Scholar 

  • Vollrath L (1979) Comparative morphology of the vertebrate pineal complex. Prog Brain Res 52:25–38

    Google Scholar 

  • Vollrath L, Schröder H (1987) Neuronal properties of mammalian pinealocytes? In: Trentini GP, Gaetani C de, Pévet P (eds) Fundamentals and clinics in pineal research. Raven Press, New York, pp 13–23

    Google Scholar 

  • Wiklund L (1974) Development of serotonin-containing cells and the sympathetic innervation of the habenular region in the rat brain. Cell Tissue Res 155:231–243

    Google Scholar 

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Supported by Grant I 38259 from the Stiftung Volkswagenwerk, Federal Republic of Germany, to E.M.R. and A.O.; Grant S-85-39 from the Direccion de Investigaciones, Universidad Austral de Chile, to E.M.R.; Grant 187 from FONDECYT, Chile, to C.R.Y.; and Grant Ko 758/3-1 from the Deutsche Forschungsgemeinschaft, Federal Republic of Germany, to H.W.K.

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Rodríguez, E.M., Korf, HW., Oksche, A. et al. Pinealocytes immunoreactive with antisera against secretory glycoproteins of the subcommissural organ: A comparative study. Cell Tissue Res. 254, 469–480 (1988). https://doi.org/10.1007/BF00226496

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