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Neuroendocrinology pp 289–303Cite as

Specific Glycoproteins of the Subcommissural Organ/Reissner’s Fiber Complex: Molecular and Functional Evidence of Their Involvement in Developmental Events

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Abstract

The subcommissural organ (SCO) is a phylogenetically old structure of the vertebrate brain made up of ependymal cells which secrete glycoproteins basally towards the leptomeningeal spaces and apically into the ventricular cavity. The latter mode of secretion forms a particular structure called Reissner’s fiber (RF). The functional significance of the SCO/RF complex is still discussed, in spite of a wide range of experimental data. Here we present new molecular and biological data favoring a putative morphogenetic activity of the SCO/RF complex. The glycoproteins secreted by the SCO exhibit sequence homologies with proteins expressed in the developing nervous system, including thrombospondins 1 and 2, semaphorins F and G and F-spondin. These glycoproteins were called SCO-spondin because of their high expression in the SCO and the presence of conserved domains (thrombospondin type 1 repeats). Molecules exhibiting such domains have been shown to interfere with cell adhesivity and neuritic outgrowth. Besides the molecular features, we analyzed the biological effect of RF and solubilized material from RF on neuronal cells in primary cell cultures. In these in vitro systems, RF markedly enhanced cell survival and interfered with cell aggregation and neuritic outgrowth. Thus, both molecular and functional data give new insights into a putative morphogenetic activity of the SCO/RF complex.

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References

  • Adams JC, Tucker RP, Lawler J (1995) The thrombospondin gene family. In: Landes RG (ed) Molecular biology intelligence unit. Springer, Berlin, Heidelberg, New York, pp 1–188

    Google Scholar 

  • Adams RH, Betz H, Puschel AW (1996) A novel class of murine semaphorins with homology to thrombospondin is differentially expressed during early embryogenesis. Mech Dev 57: 33–45

    Article  PubMed  CAS  Google Scholar 

  • Bofnstein P, Sage H (1994) Thrombospondins. Methods Enzymol 245: 62–85

    Article  Google Scholar 

  • Chiquet-Ehrismann R (1991) Anti-adhesive molecules of the extracellular matrix. Curr Opin Cell Biol 3: 800–804

    Article  PubMed  CAS  Google Scholar 

  • Creveaux I, Meiniel R, Gobron S, Dastugue B, Meiniel A (1997) Specific glycoproteins of the bovine SCO: Identification and characterization of corresponding cDNAs. (submitted)

    Google Scholar 

  • DeFreitas MF, Yoshida CK, Frazier WA, Mendrick DL, Kypta RM, Reichardt LF (1995) Identification of integrin αβp1 as a neuronal thrombospondin receptor mediating neuritic outgrowth. Neuron 15: 333–343

    Article  PubMed  CAS  Google Scholar 

  • Del Bigio MR (1995) The ependyma: a protective barrier between brain and cerebrospinal fluid. Glia 14: 1–13

    Article  PubMed  CAS  Google Scholar 

  • Didier M, Harandi M, Aguera M, Bancel B, Tardy M, Fages C, Calas A, Stagaard M, M MØllgard K, Belin MF (1986) Differential immunocytochemical staining for glial fibrillary acidic (GFA) protein, S-100 protein and glutamine synthetase in the rat subcommissural organ, non specialized ventricular ependyma and adjacent neuropil. Cell Tissue Res 245: 343–351

    Article  PubMed  CAS  Google Scholar 

  • Didier-Bazes M, Chouaf L, Lepetit P, Aguera M, Belin MF (1993) The subcommissural organ of the rat: an in vivo model of neuron-glia interactions. In: Oksche A, Rodriguez EM, Fernandez-Llebrez P (eds) The subcommissural organ: an ependymal brain gland. Springer, Berlin, Heidelberg, New York, pp 161–168

    Google Scholar 

  • Didier R, Meiniel A, Meiniel R (1992) Monoclonal antibodies as probes for the analysis of the secretory ependymal differentiation in the subcommissural organ of the chick embryo. Dev Neurosci 14: 44–52

    Article  PubMed  CAS  Google Scholar 

  • Edelman GM, Cunnigham BA, Thiery JP (1990) Morphoregulatory molecules. Wiley, New York, pp 1–648

    Google Scholar 

  • Faissner A, Kruse J (1990) Jl/Tenascin is a repulsive substrate for central nervous system neurons. Neuron 5: 627–637

    Article  PubMed  CAS  Google Scholar 

  • Feige JJ, Quirin N, Souchelnitskiy S (1996) TGFβ, un peptide biologique sous contrôle: forms latentes et mécanismes d’activation. Médecine/Sciences 12: 929–939

    Google Scholar 

  • Frazier WA (1991) Thrombospondins. Curr Opin Cell Biol 3: 792–799

    Article  PubMed  CAS  Google Scholar 

  • Gobron S, Monnerie H, Meiniel R, Creveaux I, Lehmann W, Lamalle D, Dastugue B, Meiniel A (1996) SCO-spondin: a new member of the thrombospondin family secreted by the subcommissural organ is a candidate in the modulation of neuronal aggregation. J Cell Sci 109: 1053–1061

    PubMed  CAS  Google Scholar 

  • Hecht PM, Anderson KV (1992) Extracellular proteases and embryonic pattern formation. Trends Cell Biol 2: 197–202

    Article  PubMed  CAS  Google Scholar 

  • Hedgecock EM, Culotti JG, Hall DH (1990) The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 2: 61–85

    Article  Google Scholar 

  • Hong Ch C, Hashimoto C (1995) An unusual mosaic protein with a protease domain, encoded by the nudel gene, is involved in defining embryonic dorsoventral polarity in Drosophila. Cell 82: 785–794

    Article  Google Scholar 

  • Iwashita Y, Kawaguchi S, Murata M (1994) Restoration of function by replacement of spinal cord segments in the rat. Nature 367: 167–170

    Article  PubMed  CAS  Google Scholar 

  • Jouet M, Rosenthal A, Mc Farlane J, Kenwrick S A (1993) Missense mutation confirms the LI defect in X-linked hydrocephalus (HSAS). Nature Genet 4: 331

    Article  PubMed  CAS  Google Scholar 

  • Karoumi A (1990) Mise en évidence et caractérisation par des méthodes immunologiques de sécrétions glycoprotéiques au niveau du diencéphale dorsal. Thèse d’Université, Clermont-Ferrand II

    Google Scholar 

  • Kennedy TE, Serafini T, de la Torre JR, Tessier-Lavigne M (1994) Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78: 425–435

    Article  PubMed  CAS  Google Scholar 

  • Keynes R, Cook G (1990) Cell-cell repulsion: clues from the growth cone? Cell 62: 609–610

    Article  PubMed  CAS  Google Scholar 

  • Klar A, Baldassare M, Jessell TM (1992) F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 69: 95–110

    Article  PubMed  CAS  Google Scholar 

  • Korzh VP (1994) Genetic control of early neuronal development in vertebrates. Curr Opin Neurobiol 4: 21–28

    Article  PubMed  CAS  Google Scholar 

  • Krumlauf R (1994) Hox genes in vertebrate development. Cell 78: 191–201

    Article  PubMed  CAS  Google Scholar 

  • Lawler J, Hynes RO (1986) The structure of human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins. J Cell Biol 103: 1635–1648

    Article  PubMed  CAS  Google Scholar 

  • Lochter A, Taylor J, Braunewell K-H, Holm J, Schachner M (1995) Control of neuronal morphology in vitro: interplay between adhesive substrate forces and molecular instruction. J Neurosci Res 42: 145–158

    Article  PubMed  CAS  Google Scholar 

  • Lôsecke W, Naumann W, Sterba G (1984) Preparation and discharge of secretion in the subcommissural organ of the rat. Electron-microscopic immunochemical study. Cell Tissue Res 235: 201–206

    Article  PubMed  Google Scholar 

  • Lôsecke W, Naumann W, Sterba G (1986) Immuno-electron-microscopic analysis of the basal route of secretion in the subcommissural organ of the rabbit. Cell Tissue Res 244: 449–456

    Article  PubMed  Google Scholar 

  • McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68: 283–302

    Article  PubMed  CAS  Google Scholar 

  • Meiniel A, Molat JL, Meiniel R (1988) Complex-type glycoproteins synthesized in the subcommissural organ of mammals. Light and electron microscopic investigations by use of lectins. Cell Tissue Res 253: 383–395

    Article  PubMed  CAS  Google Scholar 

  • Meiniel A, Meiniel R, Didier R, Creveaux I, Gobron S, Monnerie H, Dastugue B (1996) The subcommissural organ and Reissner’s fiber complex. An enigma in the central nervous system? Prog Histochem Cytochem 30: 1–66

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Meiniel R, Duchier-Liris N, Molat JL, Meiniel A (1991) The complex-type glycoprotein secreted by the bovine subcommissural organ: an immunological study using C1B8A8 monoclonal antibody. Cell Tissue Res 266: 483–490

    Article  PubMed  CAS  Google Scholar 

  • Meiniel R, Creveaux I, Dastugue B, Meiniel A (1995) Specific transcripts analysed by in situ hybridization in the subcommissural organ of bovine embryos. Cell Tissue Res 279: 101–107

    Article  PubMed  CAS  Google Scholar 

  • Miyazaki T, Maruyama M, Yamada G, Hatakeyama M, Taniguchi T (1991) The integrity of the conserved ‘WS motif common to IL-2 and other cytokine receptors is essential for ligand binding and signal transduction. EMBO J 10: 3191–3197

    PubMed  CAS  Google Scholar 

  • Monnerie H, Boespflug-Tanguy O, Dastugue B, Meiniel, A (1995) Reissner’s fiber supports the survival of chick cortical neurons in primary mixed cultures. Cell Tissue Res 282: 81–91

    PubMed  CAS  Google Scholar 

  • Monnerie H, Boespflug-Tanguy O, Dastugue B, Meiniel A (1996) Soluble material from Reissner’s fiber displays anti-aggregative activity in primary cultures of chick cortical neurons. Dev Brain Res 96: 120–129

    Article  CAS  Google Scholar 

  • Monnerie H, Dastugue B, Meiniel A (1997) Reissner’s fibre promotes aggregation and neuritic outgrowth of chick cortical neuronal cells in culture. Cell Tissue Res 287: 285–295

    Article  PubMed  CAS  Google Scholar 

  • Oksche A, Rodriguez EM, Fernández-Llebrez P (1993) In: Oksche A, Rodriguez EM, Fernández-Llebrez P (eds) The subcommissural organ: An ependymal brain gland. Springer, Berlin, Heidelberg, New York, pp 1–333

    Google Scholar 

  • Olsson R (1993) Reissner’s fiber mechanisms: some common denominators. In: Oksche A, Rodriguez EM, Fernández-Llebrez P (eds) The subcommissural organ: an ependymal brain gland. Springer, Berlin, Heidelberg, New York, pp 33–39

    Google Scholar 

  • Olsson R, Yulis R, Rodriguez EM (1994) The infundibular organ of the lancelet (Branchiostomalanceolatum, Acrania): an immunocytochemical study. Cell Tissue Res 277: 107–114

    Article  Google Scholar 

  • O’Shea KS, Liu L-H.J, Dixit VM (1991) Thrombospondin and a 140 kd fragment promote adhesion and neurite outgrowth from embryonic central and peripheral neurons and from PC12 cells. Neuron 7: 231–237

    Article  PubMed  Google Scholar 

  • Osterhout DJ, Frazier WA, Higgins D (1992) Thrombospondin promotes process outgrowth in neurons from the peripheral and central nervous systems. Dev Biol 150: 256–265

    Article  PubMed  CAS  Google Scholar 

  • Prater CA, Plotkin J, Jaye D, Frazier WA (1991) The properdin-like type I repeats of human thrombospondin contain a cell attachment site. J Cell Biol 112: 1031–1040

    Article  PubMed  CAS  Google Scholar 

  • Reissner E (1860) Beiträge zur Kenntnis vom Bau des Rückenmarks von Petromyzon fluviatilis L. Arch Anat Physiol 77: 545–588

    Google Scholar 

  • Rich KA, George IV FW, Law JL and Martin WJ (1990) Cell-adhesion motif in region II of malarial circumsporozoite protein. Science 249: 1574–1577

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rodriguez EM, Herrera H, Peruzzo B, Rodriguez 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

    Article  PubMed  CAS  Google Scholar 

  • Sage EH, Bornstein P (1991) Extracellular proteins that modulate cell-matrix interactions. J Biol Chem 266: 14831–14834.

    PubMed  CAS  Google Scholar 

  • Sarnat HB (1992) Role of human fetal ependyma. Pediatr Neurol 8: 163–178

    Article  PubMed  CAS  Google Scholar 

  • Schachner M (1994) Neurai recognition molecules in diseases and regeneration. Curr Opin Neurobiol 4: 726–734

    Article  PubMed  CAS  Google Scholar 

  • Schnell L, Schneider R, Kolbeck R, Barde YA, Schwab ME (1994) Neurotrophin-3 enhances sprouting of corticospinal tract during development and after spinal cord lesion. Nature 367: 170–173.

    Article  PubMed  CAS  Google Scholar 

  • Schoebitz K, Rodriguez EM, Garrido O, Del Brio-Leon MA (1993) Ontogenetic development of the subcommissural organ with reference to the flexural organ. In: Oksche A, Rodriguez EM, Fernández-Llebrez P (eds) The subcommissural organ: an ependymal brain gland. Springer, Berlin, Heidelberg, New York, pp 41–49

    Google Scholar 

  • Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M (1994) The netrins define a family of axon outgrowth promoting proteins with homology to C. elegans UNC-6. Cell 78: 409–424

    Article  PubMed  CAS  Google Scholar 

  • Snider WD (1994) Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77: 627–638

    Article  PubMed  Google Scholar 

  • Sterba G, Fredriksson G, Olsson R (1983) Immunocytochemical investigations of the infundibular organ in amphioxus (Branchiostoma lanceolatum Cephalochordata). Acta Zool (Stockh) 64: 149–153

    Article  Google Scholar 

  • Sterba G, Kießig C, Naumann W, Petter H, Kleim I (1982) The secretion of the subcommissural organ. A comparative immunocytochemical investigation. Cell Tissue Res 226: 427–439

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Studnicka FK (1900) Untersuchungen über den Bau des Ependyms der nervösen Centraiorgane. Anat Hefte 15: 303–430

    Article  Google Scholar 

  • Stutinski F (1950) Colloi’de, corps de Herring et substance Gomori positive de la neurohypophyse. C R Soc Biol 144: 1357–1360

    Google Scholar 

  • Takeuchi IK, Kimura R, Matsuda M, Shoji R (1987) Absence of subcommissural organ in the cerebral aqueduct of congenital hydrocephalus spontaneously occurring in MT/Hokldr mice. Acta Neuropathol 73: 320–322

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi IK, Kimura R, Shoji R (1988) Dysplasia of subcommissural organ in congenital hydrocephalus spontaneously occurring in Cws/Idr rats. Experientia 44: 338–340

    Article  PubMed  CAS  Google Scholar 

  • Tucker RP (1993) The in situ localization of tenascin splice variants and thrombospondin 2 mRNA in the avian embryo. Development 117: 347–358.

    PubMed  CAS  Google Scholar 

  • Van Camp G, Vits L, Coucke P, Lyonnet S, Schrander-Stumpel C, Darby J, Holden J, Munnich A, Willems J (1993) A duplication in the LI CAM gene associated with X-linked hydrocephalus. Nat Genet 4: 421–425

    Article  PubMed  CAS  Google Scholar 

  • Wislocki GB, Leduc EH (1952) The cytology and histochemistry of the subcommissural organ and Reissner’s fiber in the rodents. J Comp Neurol 97: 515–544

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Faculté de Médecine, INSERM U384 et Laboratoire de Biochimie médicale, 28 Place Henri Dunant, 63001, Clermont-Ferrand cédex, France

    A. Meiniel

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  1. A. Meiniel
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  1. Dr. Senckenbergische Anatomie, Klinikum der J.W. Goethe-Universität, Theodor-Stern-Kai 7, D-60590, Frankfurt/Main, Germany

    Horst-Werner Korf

  2. Medizinische Klinik I, Klinikum der J.W. Goethe-Universität, Theodor-Stern-Kai 7, D-60590, Frankfurt/Main, Germany

    Klaus-Henning Usadel

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Meiniel, A. (1997). Specific Glycoproteins of the Subcommissural Organ/Reissner’s Fiber Complex: Molecular and Functional Evidence of Their Involvement in Developmental Events. In: Korf, HW., Usadel, KH. (eds) Neuroendocrinology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-60915-2_21

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  • DOI: https://doi.org/10.1007/978-3-642-60915-2_21

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