Summary
The fibrillar and mucoid extracellular matrix of the posterior chamber and vitreous base was studied in the mouse by electron microscopy using fixation and staining methods that demonstrated complex carbohydrates. These methods, including block-staining with Alcian Blue, allowed globular and filamentous hyaluronic acid, finely filamentous oligosaccharides, laminated glycolipids or lipophilic glycoproteins and stellate proteoglycan monomers to be identified tentatively. There was much less globular hyaluronic acid along the basement membrane of the peripheral retina and ciliary body than has been observed in the posterior fundus. A finely filamentous network on the basement membrane interconnected with a similar network covering individual collagen fibrils, zonules and meridional fibrillar laminae as well as with a branching fibrillar network that was seen in the posterior chamber and vitreous base. This interconnected system of fibrillar proteins and complex carbohydrates was also connected to the anterior hyaloid membrane. The infoldings of the ciliary epithelium contained stellage densities with characteristics of proteoglycan monomers similar to those reported in the matrix of cartilage. The complex carbohydrates of the posterior chamber and vitreous base are of several types known to affect protein function, provide water binding and assist in mechanical stability.
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Ananthanarayanan, S. &Nimni, M. E. (1975) Collagen of rat skin and bovine articular cartilage: their hydrodynamic properties during interactions with proteoglycans. InExtracellular Matrix Influences on Gene Expression (edited bySlavkin, H. C. andGreulich, R. C.), pp. 311–20. New York. Academic Press.
Aplin, J. D., &Hughes, R. C. (1982) Complex carbohydrates of the extracellular matrix. Structures, interactions and biological roles.Biochim. biophys. Acta 694, 375–418.
Arakawa, T. &Timasheff, S. N. (1982) Stabilization of protein structure by sugars.Biochemistry 21, 6536–44.
Atkins, E. D. T., Phelps, C. F. &Sheehan, J. K. (1972). The conformation of the mucopolysaccharides. Hyaluronates.Biochem. J. 128, 1255–63.
Balazs, E. A. (1961) Molecular morphology of the vitreous body. InThe Structure of the Eye (edited bySmelser, G. K.), vol. 1, pp. 293–310. New York: Academic Press.
Baldwin, A. L. &Winlove, C. P. (1984) Effects of perfusate composition on binding of Ruthernium red and gold colloid to glycocalyx of rabbit aortic endothelium.J. Histochem. Cytochem. 32, 259–66.
Beckmann, H.-J. &Dierichs, R. (1982) Lipid extracting properties of 2,2-dimethoxypropane as revealed by electron microscopy and thin layer chromatography.Histochemistry 76, 407–12.
Bettelheim, F. A. &Wang, T. J. Y. (1976) Dynamic viscoelastic properties of bovine vitreous.Expl Eye Res. 23, 435–41.
Chakrabarti, B. &Hultsch, E. (1976) Owl monkey vitreous: a novel model for hyaluronic acid structural studies.Biochem. biophys Res. Commun. 71, 1189–93.
Christner, J. E., Brown, M. L. &Dziewiatkowski, D. D. (1977) Interaction of cartilage proteoglycans with hyaluronic acid. The role of the hyaluronic acid carboxyl groups.Biochem. J. 167, 711–6.
Davanger, M. &Ringvold, A. (1977) The ciliary body and the suspension of the lens in a monkey (Cercopithecus aethiops). A scanning electron microscopic study.Acta Ophthal. 55, 965–75.
Davanger, M. &Pedersen, O. Ö (1978) The ciliary body and the suspension of the lens in rabbits. A scanning electron microscopy study.Acta Ophthal. 56, 127–38.
Eisner, G. (1973)Biomicroscopy of the Peripheral Fundus. An Atlas and Textbook. New York: Springer-Verlag.
Eisner, G. (1982) Clinical anatomy, of the vitreous. InOcular Anatomy, Embryology, and Teratology (edited byJakobiec F. A.), pp. 391–424. Philadelphia: Harper and Row.
Endo, T., Inoue, K., Nojima, S., Sekiya, T. Ohki, K. &Nozawa, Y. (1983) Electron microscopic study on the structures formed by mixtures containing synthetic glyceroglycolipids.J. Biochem. Tokyo 93, 1–6.
Fessler, J. H. &Fessler, L. I. (1966) Electron microscopic visualization of the polysaccharide hyaluronic acid.Proc. Acad. Sci. USA. 56, 141–7.
Fine, B. S. &Tousimis, A. J. (1961) The structure of the vitreous body and the suspensory ligaments of the lens.Archs Ophthal. NY 65, 95–110.
Gartner, J. (1970a) The fine structure of the zonular fibre of the rat. Development and aging changes.Z. Anat. EntwGesch. 130, 129–52.
Gärtner J. (1970b) Electron microscopic observations on the cilio-zonular border area of the human eye with particular reference to the aging changes.Z. Anat. EntwGesch. 131, 263–73.
Gärtner, J. (1971) The fine structure of the vitreous base of the human eye and pathogenesis of pars planitis.Am. J. Ophthal. 71, 1317–27.
Gärtner, J. (1974) Extracellular fibril formation by neuroglial cells at the vitreoretinal junction of the human eye.Albrecht v. Graefes Arch. Ophthal. 191, 77–84.
Glant, T. &Léval, G. (1983) Localization of antigenic components in proteoglycan aggregate of bovine nasal cartilage.Histochemistry 77, 217–32.
Hadler, N. M., Dourmashkin, R. R., Nermut, M. V. &Williams, L. D. (1982) Ultrastructure of a hyaluronic acid matrix.Proc. natl Acad. Sci. USA 79, 307–9.
Hascall, G. K. (1980) Cartilage proteoglycans: comparison of sectioned and spread whole molecules.J. Ultrastruct. Res. 70, 369–75.
Hascall, V. C. &Hascall, G. K. (1981) Proteoglycans. InCell Biology of Extracellular Matrix (edited byHay, E. D.), pp. 39–63. New York: Plenum Press.
Hay, E. D. (1978) Fine structure of embryonic matrices and their relation to the cell surface in ruthenium red-fixed tissues.Growth 42, 399–423.
Hodson, S. &Meenan, A. (1969) The distribution of acidic mucopolysaccharides in corneal stroma.Experientia 25, 1305.
Hogan, M. J., Alvarado, J. A. &Weddell, J. E. (1971) Vitreous. InHistology of the Human Eye: An Atlas and Textbook, pp. 607–37. Philadelphia: W. B. Saunders Co.
Kalina, M. &Pease, D. C. (1977) The preservation of ultrastructure in saturated phosphatidyl cholines by tannic acid in model systems and type II pneumocytes.J. Cell Biol. 74, 726–41.
Kanwar, Y. S. &Rosenzweig, L. J. (1982) Clogging of the glomerular basement membrane.J. Cell Biol. 93, 489–94.
Kefalides, N. A., Alper, R. &Clark, C. C. (1979) Biochemistry and metabolism of basement membranes.Int. Rev. Cytol. 61, 167–228.
Kelly, J. W., Bloom, G. D. &Scott, J. E. (1963) Quaternary ammonium compounds in connective tissue histochemistry: I. Selective unblocking.J. Histochem. Cytochem. 11, 791–8.
Kempson, G. E., Muir, H., Swanson, S. A. V., &Freeman, M. A. R. (1970) Correlations between stiffness and the chemical constituents of cartilage on the human femoral head.Biochim. biophys. Acta 215, 70–7.
Laurie, G. W., Leblond, C. P., &Martin, G. R. (1982) Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement membranes.J. Cell Biol. 95, 340–4.
Lilia, S. &Barrach, H.-J. (1981) An electron microscopical study of the influence of different glycosaminoglycans on the fibrillogenesis of collagen type I and II in vitro.Virchows Arch./[path. Anat.] 390, 325–38.
Luft, J. H. (1971) Ruthenium red and violet. II. Fine structural localization in animal tissues.Anat. Rec. 171, 369–415.
Markwald, R. R., Fitzharris, T. P. &Bernanke, D. H. (1979) Morphologic recognition of complex carbohydrates in embryonic cardiac extracellular matrix.J. Histochem. Cytochem. 27, 1171–3.
Matsumoto, B., Blanks, J. C. &Ryan, S. J. (1984) Topographic variations in the rabbit and primate internal limiting membrane.Invest. Ophthal. Visual Sci. 25, 71–82.
Meyer, F. A. (1983) Macromolecular basis of globular protein exclusion and of swelling pressure in loose connective tissue (umbilical cord).Biochim. biophys. Acta 755, 388–99.
Mollenhauer, H. H. &Morré, D. J. (1983) Laminated figures of the intercisternal regions of dictyosome-like structures from guinea-pig spermatocytes fixed with glutaraldehyde-tannic acid.Cell Tissue Res. 234, 633–9.
Muller, L. L. &Jacks, T. J. (1975) Rapid chemical dehydration of samples for electron microscopic examinations.J. Histochem. Cytochem. 23, 107–10.
Ober, M. &Rohen, J. W. (1979) Regional differences in the fine structure of the ciliary epithelium related to accommodation.Invest. Ophthal. Visual Sci. 18, 655–64.
Olden, K., Parent, J. B. &White, S. L. (1982a) Carbohydrate moieties of glycoproteins. A re-evaluation of their function.Biochim. biophys. Acta 650, 209–32.
Olden, K., Bernard, B. A., White, S. L. &Parent, J. B. (1982b) Function of the carbohydrate moieties of glycoproteins.J. cell. Biochem. 18, 313–35.
Poole, A. R., Pidoux, I., Reiner, A. &Rosenberg, L. (1982). An immunoelectron microscope study of the organization of proteoglycan monomer, link protein, and collagen in the matrix of articular cartilage.J. Cell Biol. 93, 921–37.
Quintarelli, G., Vocaturo, A., Rodén, L., Bellocci, M. &Vassallo, L. M. (1978) Role of hyaluronic acid in thein vivo aggregation of cartilage proteoglycans.Connect. Tissue Res. 5, 237–48.
Raviola, G. (1971) The fine structure of the ciliary zonule and ciliary epithelium. With special regard to the organization and insertion of the zonular fibrils.Invest. Ophthal. 10, 851–69.
Rees, D. A. (1975) Stereochemistry and binding behaviour of carbohydrate chains. InBiochemistry Series One (edited byWhelan, W. J.),Biochemistry of Carbohydrates, vol. 5, pp. 1–42. Woburn: Butterworth.
Reeser, F. H. &Aaberg, T. M. (1979) Vitreous humor. InPhysiology of the Human Eye and Visual System (edited byRecords, R. E.), pp. 261–95. Philadelphia: Harper and Row.
Rentsch, F. J. (1976) The fine structure of the normal and pathological vitreous body as revealed by ruthenium-red. InThe Structure of the Eye (edited byYamada, E. andMishima, S.), vol. 3, pp. 19–37. Tokyo: Japanese Journal of Ophthalmology.
Rhodes, R. H. (1982) An ultrastructural study of the complex carbohydrates of the mouse posterior vitreoretinal juncture.Invest. Ophthal. Visual Sci. 22, 460–77.
Rhodes, R. H. (1983a) An ultrastructural study of histochemical staining of complex carbohydrates in the mouse posterior vitreous body.Histochemistry 78, 125–43.
Rhodes, R. H. (1983b) A comparative study of vitreous-body and zonular glycoconjugates that bind to the lectin fromUlex europaeus.Histochemistry 78, 349–60.
Roughley, P. J. (1975) Helix formation: its involvement in the formation of gel structures.Trans. ophthal. Soc. UK. 95, 369–71.
Ruggeri, A., Dell'orbo, C. &Quacci, D. (1975) Electron microscopic visualization of proteoglycans with Alcian Blue.Histochem. J. 7, 187–97.
Schofield, B. H., Williams, B. R. &Doty, S. B. (1975) Alcian Blue staining of cartilage for electron microscopy. Application of the critical electrolyte concentration principle.Histochem. J. 7, 139–49.
Scott, J. E. &Dorling, J. (1965) Differential staining of acid glycosaminoglycans (mucopolysaccharides) by Alcian Blue in salt solutions.Histochemie 5, 221–33.
Snowden, J. M. (1982) The stabilization of in vivo assembled collagen fibrils by proteoglycans/glycos-aminoglycans.Biochim. biophys. Acta. 703, 21–5.
Stamper, R. L. (1979) Aqueous humor: secretion and dynamics. InPhysiology of the Human Eye and Visual System (edited byRecords, R. E.), pp. 156–82. Philadelphia: Harper and Row.
Streeten, B. W. (1982) Zonular apparatus. InOcular Anatomy, Embryology, and Teratology (edited byJakobiec, F. A.), pp. 331–53. Philadelphia: Harper and Row.
Streeten, B. W., Swann, D. A., Licari, P. A., Robinson, M. R., Gibson, S. A., Marsh, N. J., Vergnes, J.-P. &Freeman, I. L. (1983) The protein composition of the ocular zonules.Invest. Ophthal. Visual Sci. 24, 119–23.
Swann, D. A. (1972) The structure and function of the vitreous. InRetina Congress (edited byPreutt, R. C. andRegan, C. D. J.), pp. 203–14. New York: Appleton-Century-Crofts.
Swann, D. A. &Constable, I. J. (1972) Vitreous structure. I. Distribution of hyaluronate and protein.Invest. Ophthal. 11, 159–63.
Takagi, M., Parmley, R. T., Toda, Y. &Austin, R. L. (1982) Ultrastructural cytochemistry and immunocytochemistry of sulfated glycosaminoglycans in epiphyseal cartilage.J. Histochem. Cytochem. 30, 1179–85.
Takei, Y. &Ozanics, V. (1975) Electron microscopic studies on the zonule. 1. Fine structure of normal and Ruthenium Red stained zonular fibrils in the rabbit and monkey.Jap. J. Ophthal. 19, 69–93.
Trimm, H. H. &Jennings, B. R. (1983) Study of hyaluronic acid flexibility by electric birefringence.Biochem. J. 213, 671–7.
Warwick, R. (1976) The vitreous. InEugene Wolff's Anatomy of the Eye and Orbit 7th edn, pp. 175–8. Philadelphia: W. B. Saunders Co.
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Rhodes, R.H. An ultrastructural study of complex carbohydrates in the posterior chamber and vitreous base of the mouse. Histochem J 17, 291–312 (1985). https://doi.org/10.1007/BF01004592
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DOI: https://doi.org/10.1007/BF01004592