Summary
A potential association between hyaluronan and unmyelinated nerve fibres in the PNS (rat skin and iris) and CNS (rat retinal inner plexiform and nerve fibre layers) was investigated at the ultrastructural level using two different hyaluronan-binding probes (link protein-gold and aggrecan-gold). Neuronal and glial cell plasma membranes, as well as the periaxonal space in between, were specifically labelled, suggesting that hyaluronan is secreted by these cells and utilized locally. Intracelluarly, weak labelling of mitochondrial profiles was observed.
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Alho, A. M. &Underhill, C. B. (1989) The hyaluronate receptor is preferentially expressed on proliferating epithelial cells.Journal of Cell Biology 108, 1557–65.
Asari, A., Miyauchi, S., Miyazaki, K., Hamai, A., Horie, K., Takahashi, T., Sekiguchi, T., Machida, A., Kohno, K. &Uchiyama, Y. (1992) Intra- and extracellular localization of hyaluronic acid and proteoglycan constituents (chondroitin sulfate, keratan sulfates and protein core) in articular cartilage of rabbit tibia.Journal of Histochemistry and Cytochemistry 40, 1693–703.
Asher, R. &Bignami, A. (1991) Localization of hyaluronate in primary glial cell cultures derived from newborn rat brain.Experimental Cell Research 195, 401–11.
Bignami, A. &Dahl, D. (1986) Brain-specific hyaluronate-binding protein: an immunohistological study with monoclonal antibodies of human and bovine central nervous system.Proceedings of the National Academy of Sciences (USA) 83, 3518–22.
Bignami, A., Hosley, M. &Dahl, D. (1993) Hyaluronic acid and hyaluronic acid-binding proteins in brain extracellular matrix.Anatomy and Embryology 188, 419–33.
Castejón, H. V. (1970) Histochemical demonstration of acid glycosaminoglycans in the nerve cell cytoplasm of mouse central nervous system.Acta Histochemica 35, 161–72.
Castejón, O. J. &Castejón, H. V. (1987) Electron microscopy and glycosaminoglycan histochemistry of cerebellar stellate neurons.Scanning Microscopy 1, 681–93.
Delpech, B. &Halavent, C. (1981) Characterization and purification from human brain of a hyaluronic acid-binding glycoprotein, hyaluronectin.Journal of Neurochemistry 36, 855–9.
Delpech, B., Delpech, A., Brückner, G., Girard, N. &Maingonnat, C. (1989) Hyaluronan and hyaluronectin in the nervous system. Inthe Biology of Hyaluronan (edited byEvered, D. &Whelan, J.) pp. 208–32. Chichester: John Wiley & Sons.
Eggli, P. S. &Graber, W. (1995) Association of hyaluronan with rat vascular endothelial and smooth muscle cells.Journal of Histochemistry and Cytochemistry 43, 689–97.
Eggli, P. S., Lucocq, J., Ott, P., Graber, W. &Van Der Zypen, E. (1992) Ultrastructural localization of hyaluronan in the myelin sheaths of the rat central and rat and human peripheral nervous systems using hyaluronan-binding protein-gold and link protein-gold.Neuroscience 48, 737–44.
Furukawa, K. &Terayama, H. (1977) Isolation and identification of glycosaminoglycans associated with purified nuclei from rat liver.Biochimica and Biophysica Acta 499, 278–89.
Fuxe, K., Tinner, B., Chadi, G., Härfstrand, A. &Agnati, L. F. (1994) Evidence for a regional distribution of hyaluronic acid in the rat brain using a highly specific hyaluronic acid recognizing protein.Neuroscience Letters 169, 25–30.
Gong, H., Underhill, C. B. &Freddo, T. F. (1994) Hyaluronan in the bovine ocular anterior segment, with emphasis on the outflow pathways.Investigative Ophthalmology and Visual Science 35, 4328–32.
Green, S. J., Tarone, G. &Underhill, C. B. (1988) Distribution of hyaluronate receptors in the adult lung.Journal of Cell Science 89, 145–56.
Hellström, S., Tengblad, A., Johansson, C., Hedlund, U. &Axelsson, E. (1990) An improved technique for hyaluronan histochemistry using microwave irradiation.Histochemical Journal 22, 677–82.
Hunter, G. K., Wong, K. S. &Kim, J. J. (1988) Binding of calcium to glycosaminoglycans: an equilibrium dialysis study.Archives of Biochemistry and Biophysics 260, 161–7.
Jaworski, D. M., Kelly, G. M. &Hockfield, S. (1994) BEHAB, a new member of the proteoglycan tandem repeat family of hyaluronan-binding proteins that is restricted to the brain.Journal of Cell Biology 125, 495–509.
Johnson-Green, P. C., Dow, K. E. &Riopelle, R. J. (1991) Characterization of glycosaminoglycans produced by primary astrocytesin vitro.Glia 4, 314–21.
Laurent, T. C. &Fraser, J. R. E. (1992) Hyaluronan.FASEB Journal 6, 2397–404.
Malathy, K. &Kurup, P. A. (1972) Metabolism of glycosaminoglycans in alloxan diabetic rats. I. Changes in tissue glycosaminoglycans.Diabetes 21, 1162–7.
Margolis, R. U. &Margolis, R. K. (1974) Distribution and metabolism of mucopolysaccharides and glycoproteins in neuronal perikarya, astrocytes, and oligodendroglia.Biochemistry 13, 2849–52.
Margolis, R. U., Margolis, R. K., Chang, L. B. &Preti, C. (1975) Glycosaminoglycans of brain during development.Biochemistry 14, 85–8.
Margolis, R. K., Crockett, C. P., Kiang, W. L. &Margolis, R. U. (1976) Glycosaminoglycans and glycoproteins associated with rat brain nuclei.Biochimica and Biophysica Acta 451, 465–9.
Picker, L. J., Nakache, M. &Butcher, E. C. (1989) Monoclonal antibodies to human lymphocyte homing receptors define a novel class of adhesion molecules on diverse cell types.Journal of Cell Biology 109, 927–37.
Prehm, P. &Mausolf, A. (1986) Isolation of streptococcal hyaluronate synthase.Biochemical Journal 235, 887–9.
Ripellino, J. A., Klinger, M. M., Margolis, R. U. &Margolis, R. K. (1985) The hyaluronic acid binding region as a specific probe for the localization of hyaluronic acid in tissue sections.Journal of Histochemistry and Cytochemistry 33, 1060–6.
Ripellino, J. A., Bailo, M., Margolis, R. U. &Margolis, R. K. (1988) Light and electron microscopic studies on the localization of hyaluronic acid in developing rat cerebellum.Journal of Cell Biology 106, 845–55.
Rodríguez, J. P. &Minguell, J. J. (1989) Synthesis of proteoglycans and hyaluronic acid by long-term cultures of testicular cells from immature and pubertal rats.Cell Biochemistry and Function 7, 293–300.
Sunderland, C. A., Bulmer, J. N., Lunscombe, M., Redman, C. W. G. &Stirrat, G. M. (1981) Immunological and biochemical evidence for a role for hyaluronic acid in the growth and development of the placenta.Journal of Reproductive Immunology 8, 197–212.
Tammi, R., Rönkkö, S., Ågren, U. M. &Tammi, M. (1994) Distribution of hyaluronan in bull reproductive organs.Journal of Histochemistry and Cytochemistry 42, 1479–86.
Tengblad, A. (1979) Affinity chromatography on immobilized hyaluronate and its application to the isolation of hyaluronate binding proteins from cartilage.Biochimica et Biophysica Acta 578, 281–9.
Terpe, H. J., Stark, H., Prehm, P. &Günthert, U. (1994) CD44 variant isoforms are preferentially expressed in basal epithelia of non-malignant human fetal and adult tissues.Histochemistry 101, 79–89.
Toole, B. P. (1973) Hyaluronate and hyaluronidase in morphogenesis and differentiation.American Zoologist 13, 1061–5.
Tona, A. &Bignami, A. (1993) Effect of hyaluronidase on brain extracellular matrixin vivo and optic nerve regeneration.Journal of Neuroscience Research 36, 191–9.
Tona, A., Perides, G., Rahemtulla, F. &Dahl, D. (1993) Extracellular matrix in regenerating rat sciatic nerve: a comparative study on the localization of laminin, hyaluronic acid, and chondroitin sulfate proteoglycans, including versican.Journal of Histochemistry and Cytochemistry 41, 593–9.
Vogel, H., Butcher, E. C. &Picker, L. J. (1992) H-CAM expression in the human nervous system: evidence for a role in diverse glial interactions.Journal of Neurocytology 21, 363–73.
Yasuhara, O., Akiyama, H., Mcgeer, E. G. &Mcgeer, P. L. (1994) Immunohistochemical localization of hyaluronic acid in rat and human brain.Brain Research 635, 269–82.
Young, I. J. &Abood, L. G. (1960) Histological demonstration of hyaluronic acid in the central nervous system.Journal of Neurochemistry 6, 89–94.
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Eggli, P.S., Graber, W. Ultrastructural association of hyaluronan with rat unmyelinated nerve fibres. J Neurocytol 25, 79–87 (1996). https://doi.org/10.1007/BF02284787
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DOI: https://doi.org/10.1007/BF02284787