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Developmental expression of glial markers in ependymocytes of the rat subcommissural organ: role of the environment

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Summary

The rat subcommissural organ (SCO), principally composed of modified ependymocytes (a type of glial cell), is a suitable model for the in vivo study of glial differentiation. An immunohistochemical study of the ontogenesis of rat SCO-ependymocytes from embryonic day 13 to postnatal day 10 shows that these cells express transitory glial fibrillary acidic protein (GFAP) from embryonic day 19 until postnatal day 3. However, S100 protein (S100) is never expressed in the SCO-cells, contrasting with the ventricle-lining cells of the third ventricle, which contain S100 as early as embryonic day 17. Environmental factors could be responsible for the repression of GFAP and S100 in adult rats, because GFAP and S100 are observed in ependymocytes of SCO 3 months after being grafted from newborn rat into the fourth ventricle of an adult rat. Neuronal factors might be involved in the control of the expression of S100, since after the destruction of serotonin innervation by neurotoxin at birth, S100 can be observed in some SCO-ependymocytes of adult rats. On the other hand, GFAP expression is apparently not affected by serotomin denervation, suggesting the existence of several factors involved in the differentiation of SCO-cells.

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References

  • Allore R, O'Hanlon D, Price R, Neilson K, Willard HF, Cox DR, Marks A, Dunn RJ (1988) Gene encoding the β subunit of S100 protein is on chromosome 21: implications for Down syndrome. Science 239: 1311–1313

    Google Scholar 

  • Bignami A, Raju T, Dahl D (1982) Localisation of vimentin, the nonspecific intermediate filament protein in embryonal glia and in early differentiating neurons. In vivo and in vitro immunofluorescence study of the rat embryo with vimentin and neurofilament antisera. Dev Biol 91: 286–295

    Google Scholar 

  • Biosca A, Azcoitia I (1989) Evidence for basal secretion in the subcommissural organ of the chicken (Gallus gallus). J Hirnforsch 30: 273–279

    Google Scholar 

  • Bruni JE, Del Bigio MR, Clattenburg RE (1985) Ependyma: normal and pathological. A review of the literature. Brain Res Rev 9: 1–19

    Google Scholar 

  • Cash CD, Vayer P, Mandel P, Maitre P (1985) Tryptophan-5-hydroxylase: rapid purification from whole rat brain and production of specific antiserum. Eur J Biochem 149: 239–245

    Google Scholar 

  • Choi BH, Kim RC, Lapham LW (1983) Do radial glia give rise to both astroglial and oligodendroglial cells? Dev Brain Res 8: 119–130

    Google Scholar 

  • Chouaf L, Didier-Bazes M, Aguera M, Tardy M, Sallanon M, Kitahama K, Belin MF (1989) Comparative marker analysis of the ependymocytes of the subcommissural organ in four different mammalian species. Cell Tissue Res 257: 255–262

    Google Scholar 

  • Dahl D, Rueger DC, Bignami A (1981) Vimentin, the 57000 molecular weight protein of fibroblast filaments, is the major cytoskeletal component in immature glia. Eur J Cell Biol 24: 191–196

    Google Scholar 

  • Das GD (1979) Gliogenesis and ependymogenesis during embryonic development of the rat. J Neurol Sci 43: 193–204

    Google Scholar 

  • Didier M, Harandi M, Aguera M, Bancel B, Tardy M, Fages C, Calas A, Stagaard M, Møllgaard K, Belin MF (1986) Differential immunocytochemical staining for glial fibrillary acidic (GFA) protein, S100 protein and glutamine synthetase in the rat subcommissural organ and nonspecialized ventricular ependyma and adjacent neuropil. Cell Tissue Res 245: 243–251

    Google Scholar 

  • Didier-Bazes M, Aguera M, Chouaf L, Harandi M, Calas A, Meiniel A, Belin MF (1989) Neuronal control of [3H] GABA uptake in the ependymocytes of the subcommissural organ: an in vivo model of neuron-glia interaction. Brain Res 489: 137–145

    Google Scholar 

  • Didier-Bazes M, Chouaf L, Hardin H, Aguera M, Belin MF (1991) Developmental neuron-glia interaction: role of the serotonin innervation upon the onset of GABA uptake into the ependymocytes of the rat subcommissural organ. Der Brain Res (in press)

  • Diederen JHB, Vullings HGB, Legerstee-Oosteveen GG (1987) Autoradiographic study of the production of secretory material by the subcommissural organ of frogs (Rana temporaria) after injection of several radioactive precursors, with special reference to the glycosylation and turnover rate of the secretory material. Cell Tissue Res 248: 215–222

    Google Scholar 

  • Donato R (1988) Calcium-independent, pH regulated effects of S-100 proteins on assembly-disassembly of brain microtubule protein in vitro. J Biol Chem 263: 106–110

    Google Scholar 

  • Dupoucy P, Benjelloun S, Gomes D (1985) Immunohistochemical demonstration of an organized cytoarchitecture of the radial glia in the CNS of the embryonic mouse. Dev Neurosci 7: 81–93

    Google Scholar 

  • Eng L, Shiurba R (1988) Glial fibrillary acidic protein: a review of structure, function and clinical application. In: Morangos PJ, Campbell IC, Cohen RM (eds) Neuronal and glial protein. Academic Press, New York, pp 339–359

    Google Scholar 

  • Gamrani H, Belin MF, Aguera M, Calas A, Pujol JF (1981) Radioautographic evidence for an innervation of the subcommissural organ by GABA-containing nerve fibers. J Neurocytol 10: 411–424

    Google Scholar 

  • Hatten ME (1985) Neuronal inhibition of astroglial morphology and proliferation in vitro. J Cell Biol 100: 384–396

    Google Scholar 

  • Hatten ME (1987) Neuronal inhibition of astroglial cell proliferation is membrane mediated. J Cell Biol 104: 1353–1360

    Google Scholar 

  • Hess J, Sterba G (1973) Studies concerning the function of the complex subcommissural organ-liquor fibre: the binding ability of the liquor fibre to pyrocatechin derivatives and its functional aspects. Brain Res 58: 303–312

    Google Scholar 

  • Hofer HO (1985) Observations on organized areas of the endoplasmic reticulum, mitochondria and ribosomes in ependymal cells of the subcommissural organ of Cebus, Saimiri and Callicebus (Platyrrhina, Primates). Gegenbaurs Morphol Jahrbl 131: 757–776

    Google Scholar 

  • Holton B, Weston JA (1982) Analysis of glial cell differentiation in peripheral nervous tissue. II. Neurons promote S-100 synthesis by purified glial precursor cell populations. Dev Biol 89: 72–81

    Google Scholar 

  • Joosten EAJ, Gribnau AAM (1989) Astrocytes and guidance of outgrowing corticospinal tract axons in the rat. An immunocytochemical study using anti-vimentin and anti-glial fibrillary acidic protein. Neuroscience 31: 439–452

    Google Scholar 

  • Karoumi A, Meiniel R, Croisille Y, Belin MF, Meiniel A (1990a) Glycoprotein synthesis in the subcommisural organ of the chick embryo. I. An ontogenetical study using specific antibodies. J Neural Transm 79: 141–153

    Google Scholar 

  • Karoumi A, Croisille Y, Croisille F, Meiniel R, Belin MF, Meiniel A (1990b) Glycoprotein synthesis in the subcommissural organ of the chick embryo. II. An immunochemical study. J Neural Transm 80: 203–212

    Google Scholar 

  • Kimble JE, Møllgaard K (1973) Evidence for basal secretion in the subcommissural organ of the adult rabbit. Z Zellforsch 142: 223–239

    Google Scholar 

  • Le Prince G, Copin MC, Hardin H, Belin MF, Bouilloux JP, Tardy M (1990) Neuron-glia interactions: effect of serotonin on the astroglial expression of GFAP and of its encoding message. Dev Brain Res 51: 295–298

    Google Scholar 

  • Lösecke W, Naumann W, Sterba G (1984) Preparation and discharge of secretion in the subcommisural organ of the rat. An electron-microscopic immunocytochemical study. Cell Tissue Res 235: 201–206

    Google Scholar 

  • Matsuura T, Sano Y (1987) Immunohistochemical demonstration of serotoninergic and peptidergic nerve fibers in the subcommissural organ of the dog. Cell Tissue Res 248: 287–295

    Google Scholar 

  • Meiniel R, Meiniel A (1985) Analysis of the secretion of the subcommissural organs of several vertebrate species by use of fluorescent lectins. Cell Tissue Res 239: 359–364

    Google Scholar 

  • Nanopoulos D, Belin MF, Didier M, Aguera M, Partisani M, Maitre M, Pujol JF (1983) Immunohistochemical evidence for neuronal and non neuronal synthesis of GABA in the rat subcommissural organ. Neurochem Int 5: 785–791

    Google Scholar 

  • Naruse I, Kato K, Asano T, Suzuki F, Kameyama Y (1990) Developmental brain abnormalities accompanied with the retarded production of S-100 β protein in genetic polydactyly mice. Dev Brain Res 51: 253–258

    Google Scholar 

  • Oksche A (1969) The subcommissural organ. J Neuro-Visc Relax Suppl 9: 111–139

    Google Scholar 

  • Pixley SRK, De Vellis J (1984) Transition between immature radial glia and mature astrocytes studies with a monoclonal antibody to vimentin. Dev Brain Res 15: 201–209

    Google Scholar 

  • Rakic P, Sidman RL (1968) Subcommissural organ and adjacent ependyma: autoradiographic study of their origin in the mouse brain. Am J Anat 122: 317–336

    Google Scholar 

  • Redecker P (1989) Immunohistochemical localisation of glial fibrillary acidic protein (GFAP) and vimentin in the subcommissural organ of the Mongolian gerbil (Meriones unguiculatus). Cell Tissue Res 255: 595–600

    Google Scholar 

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

    Google Scholar 

  • Rodríguez EM, Herrera H, Peruzzo B, Rodríguez S, Hein S, Oksche A (1986) Light and electron-microscopic immunocytochemistry and lectin histochemistry of the subcommissural organ: evidence for processing of the secretory material. Cell Tissue Res 243: 545–559

    Google Scholar 

  • Rodríguez EM, Rodríguez S, Schoebitz K, Yulis CR, Hoffmann P, Manns V, Oksche A (1989) Light- and electron-microscopic investigation of the rat subcommissural organ grafted under the kidney capsule, with particular reference to immunocytochemistry and lectin histochemistry. Cell Tissue Res 258: 499–514

    Google Scholar 

  • Rodríguez S, Rodríguez EM, Jara P, Peruzzo B, Oksche A (1990) Single injection into the cerebrospinal fluid of antibodies against the secretory material of the subcommissural organ reversibly blocks formation of Reissner's fiber: immunocytochemical investigations in the rat. Exp Brain Res 81: 113–124

    Google Scholar 

  • Roessmann U, Velasco ME, Sindely SD, Gambetti P (1980) Glial fibrillary acidic protein (GFAP) in ependymal cells during development. An immunocytochemical study. Brain Res 200: 1321

    Google Scholar 

  • Sakumoto T, Sakaï K, Salvert D, Sasaki H, Kimura H, Maeda T, Jouvet M (1984) Possible role of serotonin in the secretory activity of the subcommissural organ of the cat. Neurosci Res 1: 191–197

    Google Scholar 

  • Schnitzer J, Franke WW, Schachner M (1981) Immunocytochemical demonstration of vimentin in astrocytes and ependymal cells of developing and adult mouse nervous system. J Cell Biol 90: 435–447

    Google Scholar 

  • Schoebitz K, Garrido O, Heinrichs M, Speer L, Rodríguez EM (1986) Ontogenetical development of the chick and duck subcommissural organ. An immunocytochemical study. Histochemistry 84: 31–40

    Google Scholar 

  • Simonian A, Baudier J, Haglid KG (1989) Modulation of ATPase activities in the central nervous system by the S-100 proteins. Neurochem Res 14: 761–764

    Google Scholar 

  • Sterba G, Klein I, Naumann W, Petter H (1981) Immunocytochemical investigation of the subcommissural organ in the rat. Cell Tissue Res 218: 659–662

    Google Scholar 

  • Sterba G, Lösecke W, Kiessig C (1987) The secretion of the subcommissural organ. Wiss 2 Karl Marx Uni Leipzig Math Naturwis 36, 2: 9–16

    Google Scholar 

  • Tardy M, Rolland B, Fages C, Caldani M (1984) Astroglia cells: glucocorticoid target cells in the brain. Clin Neuropharmacol 7-4: 296–302

    Google Scholar 

  • Weissmann D, Belin MF, Aguera M, Meunier C, Maitre M, Cash CD, Ehret M, Mandel P, Pujol JF (1987) Immunocytochemistry of tryptophan hydroxylase in the rat brain. Neurosci 23: 291–304

    Google Scholar 

  • Wiklund L, Lundberg JJ, Møllgaard K (1977) Species differences in serotoninergic innervation and secretory activity of the rat, gerbil, mouse and rabbit subcommissural organ. Acta Physiol Scand [Suppl] 452: 27–30

    Google Scholar 

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Authors and Affiliations

  1. INSERM CJF 90-10, CNRS US 1195, Laboratoire Anatomie Pathologique, Faculté A. Carrel, F-69372, Lyon Cedex 08, France

    L. Chouaf, M. Didier-Bazes, H. Hardin, M. Aguera, M. Fevre-Montange, B. Voutsinos & M. F. Belin

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  1. L. Chouaf
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  2. M. Didier-Bazes
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  3. H. Hardin
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  4. M. Aguera
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  5. M. Fevre-Montange
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  6. B. Voutsinos
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  7. M. F. Belin
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Chouaf, L., Didier-Bazes, M., Hardin, H. et al. Developmental expression of glial markers in ependymocytes of the rat subcommissural organ: role of the environment. Cell Tissue Res 266, 553–561 (1991). https://doi.org/10.1007/BF00318597

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  • DOI: https://doi.org/10.1007/BF00318597

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