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Cranial meninges of goldfish: age-related changes in morphology of meningeal cells and accumulation of surfactant-like multilamellar bodies

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Abstract

In the optic tectum of goldfish, the outer, middle and inner layers of the endomeninx were evident in animals ranging in age from 1 month to several years. The outer layer in young animals consisted of closely overlapping cells with intertwined processes, whereas in the older animals it contained large extracellular spaces. The intermediate layer cells were always arranged in a single continuous layer, but in young animals they overlapped extensively with one another toward their edges whereas in the oldest animals they became extremely flat and non-overlapping. The inner layer included an outer tier of cells with their bases adhering to the intermediate layer, and an inner tier of cells detached from both the intermediate layer and the basal lamina overlying the brain parenchyma. Inner layer cells contained many large vacuoles that were in continuity with the extracellular space. With age, the extracellular space and the vacuolar system expanded, and the inner layer evolved into a meshwork of attenuated cytoplasmic processes embedded in the granular extracellular matrix. Another age-related feature was the accumulation adjacent to the basal lamina of uniform disc-shaped membranous structures, resembling multilamellar bodies of lung surfactant. These “disc bodies” were apparently generated by the coalescence of vesicles formed at the surface of the inner layer cells, possibly as a by-product of protein secretion by these cells.

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References

  • Achúcarro N (1915) De l'évolution de la névroglie, et spécialement de ses relations avec l'appareil vasculaire. Trab Lab Invest Biol 13:169–212

    Google Scholar 

  • Bernstein JJ, Streicher E (1965) The blood-brain barrier of fish. Exp Neurol 11:464–473

    Google Scholar 

  • Bundgaard M, Cserr HF (1991) Barrier membranes at the outer surface of the brain of an elasmobranch,Raja erinacea. Cell Tissue Res 265:113–120

    Google Scholar 

  • Frederickson RG (1991) The subdural space interpreted as a cellular layer of meninges. Anat Rec 230:38–51

    Google Scholar 

  • Gelderen C van (1925) Über die Entwicklung der Hirnhäute bei Teleostiern. Anat Anz 60:48–57

    Google Scholar 

  • Golde LMG van, Batenburg JJ, Robertson B (1994) The pulmonary surfactant system. News Physiol Sci 9:13–20

    Google Scholar 

  • Haagsman HP, Golde LMG van (1991) Synthesis and assembly of lung surfactant. Ann Rev Physiol 53:441–464

    Google Scholar 

  • Haines DE (1991) On the question of a subdural space. Anat Rec 230:3–21

    Google Scholar 

  • Hoffmann W (1992) Goldfish ependymins: cerebrospinal fluid proteins of meningeal origin. Prog Brain Res 91:13–17

    Google Scholar 

  • 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 J, Stafford C (eds) Development and Regeneration of the Nervous System. Chapman & Hall, London, pp 255–265

    Google Scholar 

  • Kao Y-C, Lichtenberger LM (1990) A method to preserve extracellular surfactant-like phospholipids on the luminal surface of rodent gastric mucosa. J Histochem Cytochem 38:427–431

    Google Scholar 

  • Lakos SF, Thormodsson FR, Grafstein B (1989) Immunostaining of goldfish brain with antiserum to extracellular glycoproteins of the optic tectum. Anat Rec 221:64a

    Google Scholar 

  • Lakos SF, Thormodsson FR, Grafstein B (1994) Immunolocalization of exoglycoproteins (“ependymis”) in the goldfish brain. Neurochem Res 19:1281–1292

    Google Scholar 

  • Momose Y, Kohno K, Ito R (1988) Ultrastructural study on the meninx of the goldfish brain. J Comp Neurol 270:327–336

    Google Scholar 

  • Morse DE, Low FN (1972) The fine structure of the pia mater of the rat. Am J Anat 133:349–368

    Google Scholar 

  • 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 11:189–196

    Google Scholar 

  • Oda Y, Nakanishi I (1984) Ultrastructure of the mouse leptomeninx. J Comp Neurol 225:448–457

    Google Scholar 

  • Peters A, Palay SL, Webster H de F (1991) The Fine Structure of the Nervous System. Neurons and their supporting cells. Third edn. Oxford, New York

  • Ramsey HJ (1965) Fine structure of the surface of the cerebral cortex of human brain. J Cell Biol 26:323–333

    Google Scholar 

  • Raviola G (1982) Schwalbe line's cells: a new cell type in the trabecular meshwork ofMacaca mulatta. Invest Ophthal Vis Sci 22:45–56

    Google Scholar 

  • 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 inBrachydanio rerio. DNA Cell Biol 11:425–432

    Google Scholar 

  • Schachenmayr F, Friede RL (1978) The origin of subdural neomembranes. I. Fine structure of the dura-arachnoid interface in man. Am J Pathol 92:53–68

    Google Scholar 

  • Schmidt R (1989) Glycoproteins involved in long-lasting plasticity in the teleost brain. In: Rahmann H (ed) Fundamentals of memory formation: neuronal plasticity and brain function (Prog Zool, vol 37). Gustav Fischer, Stuttgart, pp 327–339

    Google Scholar 

  • Schmidt R, Rother S, Schlingensiepen K-H, Brysch W (1991) Neuronal plasticity depending on a glycoprotein synthesized in goldfish leptomeninx. Prog Brain Res 91:7–12

    Google Scholar 

  • Schwarz H, Müller-Schmid A, Hoffmann W (1993) Ultrastructural localization of ependymins in the endomeninx of the brain of the rainbow trout: possible association with collagen fibrils of the extracellular matrix. Cell Tissue Res 273:417–425

    Google Scholar 

  • Shashoua VE (1976) Brain metabolism and the acquisition of new behaviors. I. Evidence for specific changes in the pattern of protein synthesis. Brain Res 111:347–364

    Google Scholar 

  • Shashoua VE (1981) Extracellular fluid proteins of goldfish brain: studies of concentration and labeling patterns. Neurochem Res 6:1129–1147

    Google Scholar 

  • Stein JM, Luzio JP (1991) Ectocytosis caused by sublytic autologous complement attact on human neutrophils. The sorting of endogenous plasma-membrane proteins and lipids into shed vesicles. Biochem J 274:381–386

    Google Scholar 

  • Stevenson JA, Yoon M-G (1982) Morphology of radial glia, ependymal cells, and periventricular neurons in the optic tectum of goldfish (Carassius auratus). J Comp Neurol 205:128–138

    Google Scholar 

  • Svane-Knudsen V, Rasmussen G, Clausen PP (1990) Surfactantlike lamellar bodies in the mucosa of the human nose. Acta Otolaryngol 109:307–313

    Google Scholar 

  • Thormodsson F, Antonian E, Grafstein B (1988) Extracellular glycoproteins of the goldfish optic tectum are labelled by intraocular injection3H-proline. Soc Neurosci Abstr 14:805

    Google Scholar 

  • thormodsson F, Lakos SF, Grafstein B (1989) Characterization and immunolocalization of soluble extracellular glycoproteins in goldfish brain. Soc Neurosci Abstr 15:880

    Google Scholar 

  • Thormodsson FR, Antonian E, Grafstein B (1992a) Extracellular proteins of goldfish optic tectum labelled by intraocular injection of3H-proline. Exp Neurol 117:260–268

    Google Scholar 

  • Thormodsson FR, Parker TS, Grafstein B (1992b) Immunochemical studies of extracellular glycoproteins (X-GPs) of goldfish brain. Exp Neurol 118:275–283

    Google Scholar 

  • Weakley BS (1972) A Beginner's Handbook in Biological Electron Microscopy. Williams & Wilkins, Baltimore, pp 117–118

    Google Scholar 

  • Yamashima T, Yamashita J, Takahashi T (1990) Pulmonary surfactant-like multilamellar bodies in human arachnoid villi. J Hirnforsch 31:795–802

    Google Scholar 

  • Zhang ET, Inman CB, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123

    Google Scholar 

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Wang, J., Murray, M. & Grafstein, B. Cranial meninges of goldfish: age-related changes in morphology of meningeal cells and accumulation of surfactant-like multilamellar bodies. Cell Tissue Res. 281, 349–358 (1995). https://doi.org/10.1007/BF00583403

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  • DOI: https://doi.org/10.1007/BF00583403

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