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Cell and Tissue Research

, Volume 273, Issue 3, pp 417–425 | Cite as

Ultrastructural localization of ependymins in the endomeninx of the brain of the rainbow trout: possible association with collagen fibrils of the extracellular matrix

  • Heinz Schwarz
  • Angelika Müller-Schmid
  • Werner Hoffmann
Article

Abstract

In the rainbow trout, ependymins represent the predominant protein constituents of the cerebrospinal fluid (CSF) and perimeningeal fluid (PMF). Synthesis of these glycoproteins occurs exclusively in the endomeninx. Generally, ependymins share characteristics with proteins mediating cell-contact phenomena. Here, we show that the endomeninx of the rainbow trout is composed of three different layers, viz. an outer layer, an arachnoid-like intermediate barrier layer and an inner layer. This structure is in agreement with a meningeal barrier concept separating the PMF from the CSF. Furthermore, by immuno-electron microscopy, we have localized the majority of intracellular ependymins to the rough endoplasmic reticulum of fibroblast-like cells of the inner layer and to cells to the intermediate barrier layer. This pattern is compatible with the observed distribution of ependymins in both the PMF and CSF. In addition to their intracellular localization, an extracellular association of ependymins with bundles of collagen fibrils is demonstrated; this is particularly pronounced around all blood vessels of the brain.

Key words

Cerebrospinal fluid Regeneration Ependymins Extracellular matrix Collagen Meninges Immuno-electron microscopy Oncorhynchus mykiss (Teleostei) 

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References

  1. Achtstätter T, Fouquet B, Rungger-Brändle E, Franke WE (1989) Cytokeratin filaments and desmosomes in the epitheloid cells of the perineurial and arachnoidal sheats of some vertebrate species. Differentiation 40:129–149Google Scholar
  2. Albrecht U, Seulberger H, Schwarz H, Risau W (1990) Correlation of blood-brain barrier function and HT7 protein distribution in chick brain circumventricular organs. Brain Res 535:49–61Google Scholar
  3. Azzi G, Jouis V, Godeau G, Groult N, Robert AM (1989) Immunolocalisation of extracellular matrix macromolecules in the rat spinal cord. Matrix 9:479–485Google Scholar
  4. Bundgaard M, Cserr HF (1991) Barrier membranes at the outer surface of the brain of an elasmobranch, Raja erinacea. Cell Tissue Res 265:113–120Google Scholar
  5. Carlemalm E, Garavito RM, Villiger W (1982) Resin development for electron microscopy and analysis of embedding at low temperature. J Microsc 126:123–143Google Scholar
  6. Cserr HF, Bundgaard M (1984) Blood-brain interfaces in vertebrates: a comparative approach. Am J Physiol 246:R277-R288Google Scholar
  7. Cserr HF, Ostrach LH (1974) On the presence of subarachnoid fluid in the mudpuppy, Necturus maculosus. Comp Biochem Physiol [A] 48:145–151Google Scholar
  8. Gelderen C van (1925) Über die Entwicklung der Hirnhäute bei Teleostiern. Anat Anz 60:48–57Google Scholar
  9. Ghitescu L, Galis Z, Simionescu M, Simionescu N (1988) Differentiated uptake and transcytosis of albumin in successive vascular segments. J Submicrosc Cytol Pathol 20:657–669Google Scholar
  10. Gude S, Burmeister J, Pehlemann FW, Sievers J (1987) Meningealzellen bilden Bestandteile der Interstitialmatrix und der Basalmembran. Anat Anz 163:154Google Scholar
  11. Hartmann D, Sievers J, Pehlemann FW, Berry M (1992) Destruction of meningeal cells over the cerebral hemisphere of newborn hamsters prevents the formation of the infrapyramidal blade of the dentate gyrus. J Comp Neurol 320:33–61Google Scholar
  12. Hoffmann W (1992) Goldfish ependymins: cerebrospinal fluid proteins of meningeal origin. Prog Brain Res 91:13–17Google Scholar
  13. Hoffmann W, Königstorfer A, Sterrer S (1992) Biosynthesis and expression of goldfish ependymins: potential candidates in neural plasticity and regeneration? In: Nona S, Cronly-Dillon JR, Ferguson M, Stafford C (eds) Development and regeneration of the nervous system. Chapman and Hall, London, pp 255–265Google Scholar
  14. Ichimura T, Fraser PA, Cserr HF (1991) Distribution of extracellular tracers in perivascular spaces of the rat brain. Brain Res 545:103–113Google Scholar
  15. Klatzo I, Steinwall O (1965) Observation on cerebrospinal fluid pathways and behaviour of the blood-brain barrier in sharks. Acta Neuropathol 5:161–175Google Scholar
  16. Königstorfer A, Sterrer S, Hoffman W (1990) Ependymins are expressed in the meninx of goldfish brain. Cell Tissue Res 261:59–64Google Scholar
  17. Lakos SF, Thormodsson F, Grafstein B (1989) Immunostaining of goldfish brain with antiserum to extracellular glycoproteins of the optic tectum. Anat Rec 223:64AGoogle Scholar
  18. Matthiessen HP, Schmalenbach C, Müller HW (1991) Identification of meningeal cell released neurite promoting activities for embryonic hippocampal neurons. J Neurochem 56:759–768Google Scholar
  19. Momose Y, Kohno K, Ito R (1988) Ultrastructural study on the meninx of the goldfish brain. J Comp Neurol 270:327–336Google Scholar
  20. Müller-Schmid A, Rinder H, Lottspeich F, Gertzen E-M, Hoffmann W (1992) Ependymins from the cerebrospinal fluid of salmonid fish: gene structure and molecular characterization. Gene 118:189–196Google Scholar
  21. Müller-Schmid A, Ganß B, Gorr T, Hoffmann W (1993) Molecular analysis of ependymins from the cerebrospinal fluid of the orders Clupeiformes and Salmoniformes: no indication for the extistence of an euteleost infradivision. J Mol Evol 36:578–585Google Scholar
  22. Nakao T (1979) Electron microscopic studies on the lamprey meninges. J Comp Neurol 183:429–454Google Scholar
  23. Ng HK, Wong ATC (1991) Immunohistochemical expression of extracellular matrix proteins in meningiomas. Lab Invest 64:102AGoogle Scholar
  24. Paulsson M (1992) Basement membrane proteins: structure, assembly, and cellular interactions. Crit Rev Biochem Mol Biol 27:93–127Google Scholar
  25. Rasmussen L, Rasmussen R (1967) Comparative protein and enzyme profiles of the cerebrospinal fluid, extradural fluid, nervous tissue, and sera of elasmobranchs. In: Gilbert PW, Mattewson RF, Rall DP (eds) Sharks, skates and rays. Johns Hopkins University Press, Baltimore, pp 361–379Google Scholar
  26. Rennels ML, Gregory TF, Blaumanis OR, Fujimoto K, Grady PA (1985) Evidence for a “paravascular” fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 326:47–63Google Scholar
  27. Rinder H, Bayer TA, Gertzen E-M, Hoffmann W (1992) Molecular analysis of the ependymin gene and functional test of its promoter region by transient expression in Branchydanio rerio. DNA Cell Biol 11:425–432Google Scholar
  28. Rutka JT, Giblin J, Dougherty DV, McCulloch JR, DeArmond SJ, Rosenblum ML (1986) An ultrastructural and immunochemical analysis of leptomeningeal and meningioma cultures. J Neuropathol Exp Neurol 45:285–303Google Scholar
  29. Sagemehl M (1884) Beiträge zur vergleichenden Anatomie der Fische. II. Einige Bemerkungen über die Gehirnhäute der Knochenfische. Morphol Jahrb 9:457–475Google Scholar
  30. Schachner M, Schoonmaker G, Hynes RO (1978) Cellular and subcellular localization of LETS protein in the nervous system. Brain Res 158:149–158Google Scholar
  31. Schmidt JT, Shashoua VE (1988) Antibodies to ependymin block the sharpening of the regenerating retinotectal projection in goldfish. Brain Res 446:269–284Google Scholar
  32. Schmidt R, Lapp H (1987) Regional distribution of ependymins in goldfish brain measured by radioimmunoassay. Neurochem Int 10:383–390Google Scholar
  33. Schmidt R, Makiola E (1991) Calcium and zinc ion binding properties of goldfish brain ependymin. Neuro Chem (Life Sci Adv) 10:161–171Google Scholar
  34. Schmidt R, Rother S, Schlingensiepen K-H, Brysch W (1992) Neuronal plasticity depending on a glycoprotein synthesized in goldfish leptomeninx. Prog Brain Res 91:7–12Google Scholar
  35. Schwarz H, Hohenberg H, Humbel BM (1992) Freeze substitution in virus research. In: Hyatt AD, Eaton BT (eds) Immuno-gold electron microscopy in viral diagnosis and research. CRC, Boca Raton, pp 349–376Google Scholar
  36. Shashoua VE (1977) Ependymin β: a brain protein metabolically linked with behavioral plasticity in the goldfish. In: Roberts S, Lajtha A, Gispen WH (eds) Mechanisms, regulation and special functions of protein synthesis in the brain. Elsevier, Amsterdam, pp 331–342Google Scholar
  37. Shashoua VE (1981) Extracellular fluid proteins of goldfish brain: studies of concentration and labeling patterns. Neurochem Res 6:1129–1147Google Scholar
  38. Shashoua VE (1985) The role of brain extracellular proteins in neuroplasticity and learning. Cell Mol Neurobiol 5:183–207Google Scholar
  39. Shashoua VE (1991) Ependymin, a brain extracellular glycoprotein, and CNS plasticity. Ann NY Acad Sci 627:94–114Google Scholar
  40. Sievers J, Pehlemann FW, Berry M (1986) Influences of meningeal cells on brain development. Naturwissenschaften 73:188–194Google Scholar
  41. Sievers J, Hartmann D, Gude S, Pehlemann FW, Berry M (1987) Influences of meningeal cells on the development of the brain. In: Wolff JR, Sievers J, Berry M (eds) Mesenchymal-epithelial interactions in neural development. NATO ASI series, vol H5. Springer, Berlin Heidelberg New York, pp 171–188Google Scholar
  42. Sterrer S, Königstorfer A, Hoffmann W (1990) Biosynthesis and expression of ependymin homologous sequences in zebrafish brain. Neuroscience 37:277–284Google Scholar
  43. Stewart GR, Pearlman (1987) Fibronectin-like immunoreactivity in the developing cerebral cortex. J Neurosci 7:3325–3333Google Scholar
  44. Thormodsson F, Antonian E, Grafstein B (1992) Extracellular proteins of goldfish optic tectum are labeled by intraocular injection of 3H-proline. Exp Neurol 117:260–268Google Scholar
  45. Yamada KM, Olden K (1978) Fibronectins-adhesive glycoproteins of cell surface and blood. Nature 275:179–184Google Scholar
  46. Zubrod CG, Rall DP (1959) Distribution of drugs between blood and cerebrospinal fluid in the various vertebrate classes. J Pharmacol 125:194–197Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Heinz Schwarz
    • 1
  • Angelika Müller-Schmid
    • 2
  • Werner Hoffmann
    • 2
  1. 1.Max-Planck-Institut für EntwicklungsbiologieTübingenGermany
  2. 2.Max-Planck-Institut für Psychiatrie, Abteilung NeurochemieMartinsriedGermany

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