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Chondroitin sulphate proteoglycan and embryonic brain enlargement in the chick

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Abstract

Previous studies of the early development of the neural tube have shown the existence of an intraneural fluid, which causes a positive pressure inside this primordium, and seems to play a key role in the early development of the central nervous system. In the present study we investigated the composition and synthesis of this intraneural fluid. By using a sequential method, which includes fixation with glutaraldehyde plus cetylpyridinium chloride, opening the neural cavity after critical point drying and scanning electron microscopy analysis, we found a water-soluble extracellular matrix that filled up the brain vesicles of chick embryos at the earliest stages of the neural tube. An ultrastructural study of the neural epithelium during these stages revealed the existence of a secretion process in the neural cells toward the apical side, the future neural cavity. An immunocytochemical study to asses the nature of the secreted material has shown that the intraneural matrix contains chondroitin sulphate proteoglycan, which appeared homogenously distributed throughout the neural cavity. Our findings demonstrate that the intraneural liquid is a fluid of complex composition and includes chondroitin sulphate proteoglycan as an osmotically active molecule. This suggests a morphogenetic role for the proteoglycan during early brain enlargement. The neural ectoderm is a polarized epithelium from early developmental stages and secretes the intraneural matrix.

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References

  • Avnur Z, Geiger B (1984) Immunocytochemical localization of native chondroitin sulfate in tissues and cultured cells using specific monoclonal antibody. Cell 38:811–822

    Google Scholar 

  • Barbosa E, Giraldez F, Represa JJ (1985) Transepithelial potential and resistance in the otic vesicle of the chick embryo. J Physiol 365:53

    Google Scholar 

  • Bard JBL, Abbott AS (1979) Matrices containing glycosaminoglycans in the developing anterior chambers of chick and Xenopus embryonic eyes. Dev Biol 68:472–486

    Google Scholar 

  • Compert WD, Laurent TC (1978) Physiological function of connective tissue polysaccharides. Physiol Rev 58:255–315

    Google Scholar 

  • Compert WD, Zamparo O (1990) Hydrodynamic properties of connective-tissue polysaccharides. Biochem J 269:561–564

    Google Scholar 

  • Coulombre AJ (1956) The role of intraocular pressure in the development of the chicken eye. I. Control of eye size. J Exp Zool 133:221–223

    Google Scholar 

  • Desmond ME, Jacobsen AG (1977) Embryonic brain enlargement requires cerebrospinal fluid pressure. Dev Biol 57:188–198

    Google Scholar 

  • Giraldez F, Represa JJ, Borondo L, Barbosa E (1987) Polarization and density of Na-pumps in the inner ear of chick embryo during early stages of development. Development 100:271–278

    Google Scholar 

  • Haddon CM, Lewis JH (1991) Hyaluronan as a propellant for epithelial movement: the development of semicircular canals in the inner ear of Xenopus. Development 112:541–550

    Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–82

    Google Scholar 

  • Hascall VC, Heinegard DK, Wight TN (1991) Proteoglycans: metabolism and pathology. In: Hay ED (ed) Cell biology of extracellular matrix. Plenum Press, New York, 149–176

    Google Scholar 

  • Herzog V, Farquhar MG (1977) Luminal membrane retrieved after exocytosis reaches most Golgi cisternae in secretory cells. Proc Natl Acad Sci USA 74:5073–5077

    Google Scholar 

  • Hilfer SR, Yang J-JW (1980) Accumulation of CPC-precipitable material at apical cell surfaces during formation of the optic cup. Anat Rec 197:423–433

    Google Scholar 

  • Jelinek R, Pexieder T (1968) The pressure on encephalic fluid in chick embryos between the 2nd and 6th day of incubation. Physiol Bohemo 17:297–305

    Google Scholar 

  • Jelinek R, Pexieder T (1970) Pressure of the CFS and morphogenesis of the CNS. I. Chick embryo. Fol Morphol XVIII:102–110

    Google Scholar 

  • Mak LL (1978) Ultrastructural studies of amphibian neural fold fusion. Dev Biol 65:435–446

    Google Scholar 

  • Markwald RR, Fifzharris TP, Bank H, Bernanke DH (1978) Structural analyses of the matrical organization of glycosaminoglycans in developing endocardial cushions. Dev Biol 62:292–316

    Google Scholar 

  • Morris GM, Solursh M (1978) Regional differences in mesenchymal cell morphology and glycosaminoglycans in early neural fold stage rat embryos. J Embryo Exp Morphol 46:37–52

    Google Scholar 

  • Pexieder T, Jelinek R (1970) Pressure of the CSF and the morphogenesis of the CNS. II. Pressure necessary for normal development of brain vesicles. Fol Morphol XVII:181–192

    Google Scholar 

  • Represa JJ, Barbosa E, Giraldez F (1986) Electrical properties of the otic vesicle epithelium in the chick embryo. J Embryol Exp Morphol 97:125–139

    Google Scholar 

  • Reynolds T (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212

    Google Scholar 

  • Schoenwolf GC, Desmond ME (1984) Neural tube occlusion precedes rapid brain enlargement. J Exp Zool 230:405–407

    Google Scholar 

  • Schoenwolf GC, Smith JL (1990) Mechanism of neurulation: traditional viewpoint and recent advances. Development 109:243–270

    Google Scholar 

  • Scott JE (1955) The solubility of cetylpyridinium complexes of biological polyanoins in solution of salts. Biochem Biophys Acta 18:428–429

    Google Scholar 

  • Singley CT, Solursh M (1980) The use of tannic acid for the ultrastructural visualization of hyaluronic acid. Histochemistry 65:93–102

    Google Scholar 

  • Sinning AR, Olson MD (1988) Surface coat material associated with the developing otic placode/vesicle in the chick. Anat Rec 220:198–207

    Google Scholar 

  • Smits-Van Prooije AE, Poelman RE, Gesink AF, Van Groeningen MJ, Vermeij-Keers C (1986) The cell surface coat in neurulating mouse and rat embryos, studied with lectins. Anat Embryol 175:111–117

    Google Scholar 

  • Snider MD, Rogers OC (1986). Membrane traffic in animal cells: cellular glycoproteins to the site of Golgi manoside. I J Cell Biol 103:265–275

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31

    Google Scholar 

  • Waterman RE (1980) Preparation of embryonic tissues for SEM. Scanning Electron Microsc 20:21–44

    Google Scholar 

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Gato, A., Moro, J.A., Alonso, M.I. et al. Chondroitin sulphate proteoglycan and embryonic brain enlargement in the chick. Anat Embryol 188, 101–106 (1993). https://doi.org/10.1007/BF00191455

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