Skip to main content
Log in

Nervous tissue proteoglycans

  • Multi-author Reviews
  • Proteoglycans
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

The structure, biosynthesis, localization, and possible functional roles of nervous tissue glycosaminoglycans and proteoglycans were last reviewed several years ago70,74. Since that time, there has been an exponential increase in publications on the neurobiology of proteoglycans. This review will therefore focus on reports which have appeared in the period after 1988, and especially on those concerning the properties of individual characterized nervous tissue proteoglycans. Related areas such as the regulation of glycosaminoglycan biosynthesis and the roles of cell surface proteoglycans in adhesion and growth control are covered in other contributions to this special topic issue.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Akeson, R., and Warren, S. L., PC12 adhesion and neurite formation on selected substrates are inhibited by some glycosaminoglycans a fibronectin-derived tetrapeptide. Expl Cell Res.162 (1986) 347–362.

    Article  CAS  Google Scholar 

  2. Andres, J. L., Stanley, S., Cheifetz, S., and Massagué, J., Membrane-anchored and soluble forms of betaglycan, a polymorphic proteoglycan that binds transforming growth factor-β. J. Cell Biol.109 (1989) 3137–3145.

    Article  CAS  PubMed  Google Scholar 

  3. Aquino, D. A., Margolis, R. U., and Margolis, R. K., Immunocytochemical localization of a chondroitin sulfate proteoglycan in nervous tissue. I. Adult brain, retina, and peripheral nerve. J. Cell Biol.99 (1984) 1117–1129.

    Article  CAS  PubMed  Google Scholar 

  4. Aquino, D. A., Margolis, R. U., and Margolis, R. K., Immunocytochemical localization of a chondroitin sulfate proteoglycan in nervous tissue. II. Studies in developing brain. J. Cell Biol.99 (1984) 1130–1139.

    Article  CAS  PubMed  Google Scholar 

  5. Ard, M. D., and Bunge, R. P., Heparan sulfate proteoglycan and laminin immunoreactivity on cultured astrocytes: Relationship to differentiation and neurite growth. J. Neurosci.8 (1988) 2844–2858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Asher, R., Perides, G., Vanderhaeghen, J.-J., and Bignami, A., Extracellular matrix of central nervous system white matter: Demonstration of an hyaluronate-protein complex. J. Neurosci. Res.28 (1991) 410–421.

    Article  CAS  PubMed  Google Scholar 

  7. Bahr, B. A., Noremberg, K., Rogers, G. A., Hicks, B. W., and Parsons, S. M., Linkage of the acetylcholine transportervesamicol receptor to proteoglycan in synaptic vesicles. Biochemistry31 (1992) 5778–5784.

    Article  CAS  PubMed  Google Scholar 

  8. Banerjee, S. D., and Toole, B. P., Monoclonal antibody to chick embryo hyaluronan-binding protein: Changes in distribution of binding protein during early brain development. Devl Biol.146 (1991) 186–197.

    Article  CAS  Google Scholar 

  9. Bertolotto, A., Rocca, G., Canavese, G., Migheli, A., and Schiffer, D., Chondroitin sulfate proteoglycan surrounds a subset of human and rat CNS neurons. J. Neurosci. Res.29 (1991) 225–234.

    Article  CAS  PubMed  Google Scholar 

  10. Bignami, A., and Asher, R., Some observations on the localization of hyaluronic acid in adult, newborn and embryonal rat brain. Int. J. devl Neurosci.10 (1992) 45–57.

    Article  CAS  Google Scholar 

  11. Brittis, P. A., Canning, D. R., and Silver, J., Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science255 (1992) 733–736.

    Article  CAS  PubMed  Google Scholar 

  12. Burg, M., and Cole, G. J., A neural keratan sulfate proteoglycan, claustrin, is recognized by antibodies to MAP1B. Soc. Neurosci. Abstracts18 (1992) 236.

    Google Scholar 

  13. Carbonetto, S., Gruver, M. M., and Turner, D. C., Nerve fiber growth in culture on fibronectin, collagen, and glycosaminoglycan substrates. J. Neurosci.3 (1983) 2324–2335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Carey, D. J., and Evans, D. M., Membrane anchoring of heparan sulfate proteoglycans by phosphatidylinositol and kinetics of synthesis of peripheral and detergent-solubilized proteoglycans in Schwann cells. J. Cell Biol.108 (1989) 1891–1897.

    Article  CAS  PubMed  Google Scholar 

  15. Carey, D. J., and Stahl, R. C., Identification of a lipidanchored heparan sulfate proteoglycan in Schwann cells. J. Cell Biol.111 (1990) 2053–2062.

    Article  CAS  PubMed  Google Scholar 

  16. Carey, D. J., Crumbling, D. M., Stahl, R. C., and Evans, D. M., Association of cell surface heparan sulfate proteoglycans of Schwann cells with extracellular matrix proteins. J. biol. Chem.265 (1990) 20627–20633.

    Article  CAS  PubMed  Google Scholar 

  17. Carey, D. J., Evans, D. M., Stahl, R. C., Asundi, V. K., Conner, K. J., Garbes, P., and Cizmeci-Smith, G., Molecular cloning and characterization ofN-syndecan, a novel transmembrane heparan sulfate proteoglycan. J. Cell Biol.117 (1992) 191–201.

    Article  CAS  PubMed  Google Scholar 

  18. Carlson, S. S., Synaptic vesicle glycoproteins and proteoglycans, in: Neurobiology of Glycoconjugates, pp. 309–336. Eds R. U. Margolis and R. K. Margolis. Plenum Press, New York 1989.

    Chapter  Google Scholar 

  19. Cole, G. J., and McCabe, C. F., Identification of a developmentally regulated keratan sulfate proteoglycan that inhibits cell adhesion and neurite outgrowth. Neuron7 (1991) 1007–1018.

    Article  CAS  PubMed  Google Scholar 

  20. Damon, D. H., D'Amore, P. A., and Wagner, J. A., Sulfated glycosaminoglycans modify growth factor-induced neurite outgrowth in PC12 cells. J. cell. Physiol.135 (1988) 293–300.

    Article  CAS  PubMed  Google Scholar 

  21. David, G., Lories, V., Decock, B., Marynen, P., Cassiman, J.-J., and Van den Berghe, H., Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts. J. Cell Biol.111 (1990) 3165–3176.

    Article  CAS  PubMed  Google Scholar 

  22. DeCoster, M. A., and DeVries, G. H., Evidence that the axolemmal mitogen for cultured Schwann cells is a positively charged, heparan sulfate proteoglycan-bound, heparin-displaceable molecule. J. Neurosci. Res.22 (1989) 283–288.

    Article  CAS  PubMed  Google Scholar 

  23. Delpech, B., Maingonnat, C., Delpech, A., Maes, P., Girard, N., and Bertrand, P., Characterization of a hyaluronic acidbinding protein from sheep brain. Comparison with human brain hyaluronectin. Int. J. Biochem.23 (1991) 329–377.

    Article  CAS  PubMed  Google Scholar 

  24. Dow, K. E., Riopelle, R. J., and Kisilevsky, R., Domains of neuronal heparan sulphate proteoglycans involved in neurite growth on laminin. Cell Tissue Res.265 (1991) 345–351.

    Article  CAS  PubMed  Google Scholar 

  25. Fichard, A., Verna, J.-M., Olivares, J., and Saxod, R., Involvement of a chondroitin sulfate proteoglycan in the avoidance of chick epidermis by dorsal root ganglia fibers: A study using β-d-xyloside. Devl Biol.148 (1991) 1–9.

    Article  CAS  Google Scholar 

  26. Flaccus, A., Janetzko, A., Tekotte, H., Margolis, R. K., and Margolis, R. U., Immunocytochemical localization of chondroitin and chondroitin 4- and 6-sulfates in developing rat cerebellum. J. Neurochem.56 (1991) 1608–1615.

    Article  CAS  PubMed  Google Scholar 

  27. Fryer, H. J. L., Kelly, G. M., Molinaro, L., and Hockfield, S., The high molecular weight Cat-301 chondroitin sulfate proteoglycan from brain is related to the large aggregating proteoglycan from cartilage, aggrecan. J. biol. Chem.267 (1992) 9874–9883.

    Article  CAS  PubMed  Google Scholar 

  28. Fujita, S. C., Tada, Y., Murakami, F., Hayashi, M., and Matsumura, M., Glycosaminoglycan-related epitopes surrounding different subsets of mammalian central neurons. Neurosci. Res.7 (1989) 117–130.

    Article  CAS  PubMed  Google Scholar 

  29. Gallo, V., Bertolotto, A., and Levi, G., The proteoglycan chondroitin sulfate is present in a subpopulation of cultured astrocytes and in their precursors. Devl Biol.123 (1987) 282–285.

    Article  CAS  Google Scholar 

  30. Gallo, V., and Bertolotto, A., Extracellular matrix of cultured glial cells: Selective expression of chondroitin 4-sulfate by type-2 astrocytes and their progenitors. Expl Cell Res.187 (1990) 211–223.

    Article  CAS  Google Scholar 

  31. Geissler, D., Martinek, A., Margolis, R. U., Margolis, R. K., Skrivanek, J. A., Ledeen, R. W., König, P., and Winkler, H., Composition and biogenesis of complex carbohydrates of adrenal chromaffin granules. Neuroscience2 (1977) 685–693.

    Article  CAS  PubMed  Google Scholar 

  32. Girard, N., Courel, M. N., Delpech, A., Bruckner, G., and Delpech, B., Staining of hyaluronan in rat cerebellum with a hyaluronectin-antihyaluronectin immune complex. Histochem. J.24 (1992) 21–24.

    Article  CAS  PubMed  Google Scholar 

  33. Gowda, D. C., Goossen, B., Margolis, R. K., and Margolis, R. U., Chondroitin sulfate and heparan sulfate proteoglycans of PC12 pheochromocytoma cells. J. biol. Chem.264 (1989) 11436–11443.

    Article  CAS  PubMed  Google Scholar 

  34. Gowda, D. C., Margolis, R. U., and Margolis, R. K., Presence of the HNK-1 epitope on poly(N-acetyllactosaminyl) oligosaccharides and identification of multiple core proteins in the chondroitin sulfate proteoglycans of brain. Biochemistry28 (1989) 4468–4474.

    Article  CAS  PubMed  Google Scholar 

  35. Gowda, D. C., Hogue-Angeletti, R., Margolis, R. K., and Margolis, R. U., Chromaffin granule and PC12 cell chondroitin sulfate proteoglycans and their relation to chromogranin A. Archs Biochem. Biophys.281 (1990) 219–224.

    Article  CAS  Google Scholar 

  36. Grumet, M., Cell adhesion molecules and their subgroups in the nervous system. Curr. Opin. Neurobiol.1 (1991) 370–376.

    Article  CAS  PubMed  Google Scholar 

  37. Grumet, M., Flaccus, A., and Margolis, R. U., Functional characterization of chondroitin sulfate proteoglycans of brain: Interactions with neurons and neural cell adhesion molecules. J. Cell Biol.120 (1993) 815–824.

    Article  CAS  PubMed  Google Scholar 

  38. Guimarães, A., Zaremba, S., and Hockfield, S., Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301. J. Neurosci.10 (1990) 3014–3024.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Hageman, G. S., Kirchoff-Rempe, M. A., Lewis, G. P., Fisher, S. K., and Anderson, D. H., Sequestration of basic fibroblast growth factor in the primate retinal interphotoreceptor matrix. Proc. natl Acad. Sci. USA88 (1991) 6706–6710.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Haugen, P. K., Letourneau, P. C., Drake, S. L., Furcht, L. T., and McCarthy, J. B., A cell-surface heparan sulfate proteoglycan mediates neural cell adhesion and spreading on a defined sequence from the C-terminal cell and heparin binding domain of fibronectin, FN-C/H II. J. Neurosci.12 (1992) 2597–2608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Herndon, M. E., and Lander, A. D., A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system. Neuron4 (1990) 949–961.

    Article  CAS  PubMed  Google Scholar 

  42. Hockfield, S., and Sur, M., Monoclonal antibody Cat-301 identifies Y-cells in the dorsal lateral geniculate nucleus of the cat. J. comp. Neurol.300 (1990) 320–330.

    Article  CAS  PubMed  Google Scholar 

  43. Hoffman, S., and Edelman, G. M., A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin. Proc. natl Acad. Sci. USA84 (1987) 2533–2537.

    Article  Google Scholar 

  44. Hoffman, S., Crossin, K. L., and Edelman, G. M., Molecular forms, binding functions, and developmental expression patterns of cytotactin and cytotactin-binding proteoglycan, an interactive pair of extracellular matrix molecules. J. Cell Biol.106 (1988) 519–532.

    Article  CAS  PubMed  Google Scholar 

  45. Horner, A. A., Heterogeneous distribution of antithrombin-binding sites in rat brain heparan sulphate proteoglycans. Biochem. J.280 (1991) 393–397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Iijima, N., Oohira, A., Mori, T., Kitabatake, K., and Kohsaka, S., Core protein of chondroitin sulfate proteoglycan promotes neurite outgrowth from cultured neocortical neurons. J. Neurochem.56 (1991) 706–708.

    Article  CAS  PubMed  Google Scholar 

  47. Iwata, M., and Carlson, S. S., A large chondroitin sulfate basement membrane-associated proteoglycan exists as a disulfide-stabilized complex of several proteins. J. biol. Chem.266 (1991) 323–333.

    Article  CAS  PubMed  Google Scholar 

  48. Iwata, M., and Carlson, S. S., A large chondroitin sulfate proteoglycan has the characteristics of a general extracellular matrix component of adult brain. J. Neurosci.13 (1993) 195–207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Iwata, M., Wight, T. N., and Carlson, S. S., pgT1, A large chondroitin sulfate proteoglycan from adult rat brain, binds to hyaluronic acid. Soc. Neurosci. Abstr.18 (1992) 1326.

    Google Scholar 

  50. Johnson-Green, P. C., Dow, K. E., and Riopelle, R. J., Characterization of glycosaminoglycans produced by primary astrocytes in vitro. Glia4 (1991) 314–321.

    Article  CAS  PubMed  Google Scholar 

  51. Kalb, R. G., and Hockfield, S., Large diameter primary afferent input is required for expression of the Cat-301 proteoglycan on the surface of motor neurons. Neuroscience34 (1990) 391–401.

    Article  CAS  PubMed  Google Scholar 

  52. Kalb, R. G., and Hockfield, S., Induction of a neuronal proteoglycan by the NMDA receptor in the developing spinal cord. Science250 (1990) 294–296.

    Article  CAS  PubMed  Google Scholar 

  53. Karthikeyan, L., Maurel, P., Rauch, U., Margolis, R. K., and Margolis, R. U., Cloning of a major heparan sulfate proteoglycan from brain and identification as the rat form of glypican. Biochem. Biophys. Res. Commun.188 (1992) 395–401.

    Article  CAS  PubMed  Google Scholar 

  54. Kato, M., Koike, Y., Suzuki, S., and Kimata, K., Basement membrane proteoglycan in various tissues: Characterization using monoclonal antibodies to the Engelbreth-Holm-Swarm mouse tumor low density heparan sulfate proteoglycan. J. Cell Biol.106 (1988) 2203–2210.

    Article  CAS  PubMed  Google Scholar 

  55. Kiang, W.-L., Krusius, T., Finne, J., Margolis, R. U., and Margolis, R. K., Glycoproteins and proteoglycans of the chromaffin granule matrix. J. biol. Chem.257 (1982) 1651–1659.

    Article  CAS  PubMed  Google Scholar 

  56. Klinger, M. M., Margolis, R. U., and Margolis, R. K., Isolation and characterization of the heparan sulfate proteoglycans of brain. Use of affinity chromatography on lipoprotein lipase-agarose. J. biol. Chem.260 (1985) 4082–4090.

    Article  CAS  PubMed  Google Scholar 

  57. Krueger, R. C. Jr., Hennig, A. K., and Schwartz, N. B., Two immunologically and developmentally distinct chondroitin sulfate proteoglycans in embryonic chick brain. J. biol. Chem.267 (1992) 12149–12161.

    Article  CAS  PubMed  Google Scholar 

  58. Krusius, T., Finne, J., Margolis, R. K., and Margolis, R. U., Identification of anO-glycosidic mannose-linked sialylated tetrasaccharide and keratan sulfate oligosaccharides in the chondroitin sulfate proteoglycan of brain. J. biol. Chem.261 (1986) 8237–8242.

    Article  CAS  PubMed  Google Scholar 

  59. Krusius, T., Reinhold, V. N., Margolis, R. K., and Margolis, R. U., Structural studies on sialylated and sulfatedO-glycosidic mannose-linked oligosaccharides in the chondroitin sulfate proteoglycan of brain. Biochem. J.245 (1987) 229–234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lafont, F., Rouget, M., Triller, A., Prochiantz, A., and Rousselet, A., In vitro control of neuronal polarity by glycosaminoglycans. Development114 (1992) 17–29.

    Article  CAS  PubMed  Google Scholar 

  61. LeBaron, R. G., Zimmermann, D. R., and Ruoslahti, E., Hyaluronate binding properties of versican. J. biol. Chem.267 (1992) 10003–10010.

    Article  CAS  PubMed  Google Scholar 

  62. Levine, J. M., and Card, J. P., Light and electron microscopic localization of a cell surface antigen (NG2) in rat cerebellum: Association with smooth protoplasmic astrocytes. J. Neurosci.7 (1987) 2711–2720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Levine, J. M., and Stallcup, W. B., Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. J. Neurosci.7 (1987) 2721–2731.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Li, Y.-S., Milner, P. G., Chauhan, A. K., Watson, M. A., Hoffman, R. M., Kodner, C. M., Milbrandt, J., and Deuel, T. F., Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity. Science250 (1990) 1690–1694.

    Article  CAS  PubMed  Google Scholar 

  65. Lin, W.-L., Immunogold localization of basal laminar heparan sulfate proteoglycan in rat brain and retinal capillaries. Brain Res. Bull.24 (1990) 533–536.

    Article  CAS  PubMed  Google Scholar 

  66. Lisanti, M. P., Rodriguez-Boulan, E., and Saltiel, A. R., Emerging functional roles for the glycosyl-phosphatidylinositol membrane protein anchor. J. Membrane Biol.117 (1990) 1–10.

    Article  CAS  Google Scholar 

  67. Lories, V., Cassiman, J.-J., Van den Berghe, H., and David, G., Differential expression of cell surface heparan sulfate proteoglycans in human mammary epithelial cells and lung fibroblasts. J. biol. Chem.267 (1992) 1116–1122.

    Article  CAS  PubMed  Google Scholar 

  68. Low, M. G., and Saltiel, A. R., Structural and functional roles of glycosyl-phosphatidylinositol in membranes. Science239 (1988) 268–275.

    Article  CAS  PubMed  Google Scholar 

  69. Maeda, N., Matsui, F., and Oohira, A., A chondroitin sulfate proteoglycan that is developmentally regulated in the cerebellar mossy fiber system. Devl Biol.151 (1992) 564–574.

    Article  CAS  Google Scholar 

  70. Margolis, R. K., Discussion, in: The Biology of Hyaluronan, pp. 221–222. Eds. D. Evered and J. Whelan. Wiley, Chichester 1989.

    Google Scholar 

  71. Margolis, R. K., and Margolis, R. U., Structure and localization of glycoproteins and proteoglycans. in: Neurobiology of Glycoconjugates, pp. 85–126. Eds R. U. Margolis and R. K. Margolis. Plenum Publishing Corp., New York 1989.

    Chapter  Google Scholar 

  72. Margolis, R. K., Salton, S. R. J., and Margolis, R. U., Effects of nerve growth factor-induced differentiation on the heparan sulfate of PC12 pheochromocytoma cells and comparison with developing brain. Archs Biochem. Biophys.257 (1987) 107–114.

    Article  CAS  Google Scholar 

  73. Margolis, R. K., Goossen, B., Tekotte, H., Hilgenberg, L., and Margolis, R. U., Effects of β-xylosides on proteoglycan biosynthesis and morphology of PC12 pheochromocytoma cells and primary cultures of rat cerebellum. J. Cell Sci.99 (1991) 237–246.

    Article  CAS  PubMed  Google Scholar 

  74. Margolis, R. U., and Margolis, R. K., Distribution and metabolism of mucopolysaccharides and glycoproteins in neuronal perikaria, astrocytes, and oligodendroglia. Biochemistry13 (1974) 2849–2852.

    Article  CAS  PubMed  Google Scholar 

  75. Margolis, R. U., and Margolis, R. K. (Eds), Neurobiology of Glycoconjugates. Plenum Publishing Corp., New York 1989.

    Google Scholar 

  76. Margolis, R. U., Ledeen, R. W., Sbaschnig-Agler, M., Byrne, M. C., Klein, R. L., Douglas, B. H., and Margolis, R. K., Complex carbohydrate composition of large dense-cored vesicles from sympathetic nerve. J. Neurochem.49 (1987) 1839–1844.

    Article  CAS  PubMed  Google Scholar 

  77. Margolis, R. U., and Margolis, R. K., Properties of nervous tissue proteoglycans relevant to studies on Alzheimer's disease. Neurobiol. Aging10 (1989) 500–502.

    Article  CAS  PubMed  Google Scholar 

  78. Marks, M. S., Chi-Rosso, G., and Toole, B. P., Hyaluronate-binding proteins of murine brain. J. Neurochem.54 (1990) 171–180.

    Article  CAS  PubMed  Google Scholar 

  79. Marynen, P., Zhang, J., Cassiman, J.-J., Van den Berghe, H., and David, G., Partial primary structure of the 48- and 90-kilodalton core proteins of cell surface-associated heparan sulfate proteoglycans of lung fibroblasts. J. biol. Chem.264 (1989) 7017–7024.

    Article  CAS  PubMed  Google Scholar 

  80. McKeon, R. J., Schreiber, R. C., Rudge, J. S., and Silver, J., Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J. Neurosci.11 (1991) 3398–3411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Merenmies, J., and Rauvala, H., Molecular cloning of the 18-kDa growth-associated protein of developing brain. J. biol. Chem.265 (1990) 16721–16724.

    Article  CAS  PubMed  Google Scholar 

  82. Merenmies, J., Pihlaskari, R., Laitinen, J., Wartiovaara, J., and Rauvala, H., 30-kDa heparin-binding protein of brain (amphoterin) involved in neurite outgrowth. Amino acid sequence and localization in the filopodia of the advancing plasma membrane. J. biol. Chem.266 (1991) 16722–16729.

    Article  CAS  PubMed  Google Scholar 

  83. Miller, B., Sheppard, A. M., and Pearlman, A. L., Expression of two chondroitin sulfate proteoglycan core proteins in the subplate pathway of early cortical afferents. Soc. Neurosci. Abstr.18 (1992) 778.

    Google Scholar 

  84. Murillo-Lopez, F., Politi, L., Adler, R., and Tyl Hewitt, A., Proteoglycan synthesis in cultures of murine retinal neurons and photoreceptors. Cell. molec. Neurobiol.11 (1991) 579–591.

    Article  CAS  PubMed  Google Scholar 

  85. Nishiyama, A., Dahlin K. J., and Stallcup, W. B., The expression of NG2 proteoglycan in the developing rat limb. Development111 (1991) 933–944.

    Article  CAS  PubMed  Google Scholar 

  86. Nishiyama, A., Dahlin, K. J., Prince, J. T., Johnstone, S. R., and Stallcup, W. B., The primary structure of NG2, a novel membrane-spanning proteoglycan. J. Cell Biol.114 (1991) 359–371.

    Article  CAS  PubMed  Google Scholar 

  87. Norling, B., Glimelius, B., and Wasteson, Å., A chondroitin sulphate proteoglycan from human cultured glial and glioma cells. Structural and functional properties. Biochem. J.221 (1984) 845–853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Oakley, R. A., and Tosney, K. W., Peanut agglutinin and chondroitin-6-sulfate are molecular markers for tissues that act as barriers to axon advance in the avian embryo. Devl Biol.147 (1991) 187–206.

    Article  CAS  Google Scholar 

  89. Oohira, A., Matsui, F., Matsuda, M., Takida, Y., and Kuboki, Y., Occurrence of three distinct molecular species of chondroitin sulfate proteoglycan in the developing rat brain. J. biol. Chem.263 (1988) 10240–10246.

    Article  CAS  PubMed  Google Scholar 

  90. Oohira, A., Matsui, F., and Katoh-Semba, R. Inhibitory effects of brain chondroitin sulfate proteoglycans on neurite outgrowth from PC12D cells. J. Neurosci.11 (1991) 822–827.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Perides, G., Lane, W. S., Andrews D., Dahl, D., and Bignani, A., Isolation and partial characterization of a glial hyaluropate-binding protein. J. biol. Chem.264 (1989) 5981–5987.

    Article  CAS  PubMed  Google Scholar 

  92. Perides, G., Biviano, F., and Bignami, A., Interaction of a brain extracellular matrix protein with hyaluronic acid. Biochim. biophys. Acta1075 (1991) 248–258.

    Article  CAS  PubMed  Google Scholar 

  93. Perides, G., Rahemtulla, F., Lane, W. S., Asher, R. A., and Bignami, A., Isolation of a large aggregating proteoglycan from human brain. J. biol. Chem.267 (1992) 23883–23887.

    Article  CAS  PubMed  Google Scholar 

  94. Perkins, S. J., Nealis, A. S., Dudhia, J., and Hardingham, T. E., Immunoglobulin fold and tandem repeat structures in proteoglycan N-terminal domains and link protein. J. molec. Biol.206 (1989) 737–753.

    Article  CAS  PubMed  Google Scholar 

  95. Perris, R. and Johansson, S., Inhibition of neural crest cell migration by aggregating chondroitin sulfate proteoglycans is mediated by their hyaluronan-binding region. Devl Biol.137 (1990) 1–12.

    Article  CAS  Google Scholar 

  96. Perris, R., Krotoski, D., Lallier, T., Domingo, C., Sorrell, J. M., and Bronner-Fraser, M., Spatial and temporal changes in the distribution of proteoglycans during avian neural crest development. Development111 (1991) 583–599.

    Article  CAS  PubMed  Google Scholar 

  97. Pierce, A., Lyon, M., Hampson, I. N., Cowling, G. J., and Gallagher, J. T., Molecular cloning of the major cell surface heparan sulfate proteoglycan from rat liver. J. biol. Chem.267 (1992) 3894–3900.

    Article  CAS  PubMed  Google Scholar 

  98. Ratner, N., Hong, D., Lieberman, M. A., Bunge, R. P., and Glaser, L., The neuronal cell-surface molecule mitogenic for Schwann cells is a heparin-binding protein. Proc. natl Acad. Sci. USA85 (1988) 6992–6996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Rauch, U., Gao, P., Janetzko, A., Flaccus, A., Hilgenberg, L., Tekotte, H., Margolis, R. K., and Margolis, R. U., Isolation and characterization of developmentally-regulated chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of brain identified with monoclonal antibodies. J. biol. Chem.266 (1991) 14785–14801.

    Article  CAS  PubMed  Google Scholar 

  100. Rauch, U., Karthikeyan, L., Maurel, P., Margolis, R. U., and Margolis, R. K., Cloning and primary structure of neurocan, a developmentally regulated, aggregating chondroitin sulfate proteoglycan of brain. J. biol. Chem.267 (1992) 19536–19547.

    Article  CAS  PubMed  Google Scholar 

  101. Ripellino, J. A. and Margolis, R. U., Structural properties of the heparan sulfate proteoglycans of brain. J. Neurochem.52 (1989) 807–812.

    Article  CAS  PubMed  Google Scholar 

  102. Ripellino, J. A., Klinger, M. M., Margolis, R. U., and Margolis, R. K., The hyaluronic acid binding region as a specific probe for the localization of hyaluronic acid in tissue sections. Application to chick embryo and rat brain. J. Histochem. Cytochem.33 (1985) 1060–1066.

    Article  CAS  PubMed  Google Scholar 

  103. Ripellino, J. A., Bailo, M., Margolis, R. U., and Margolis, R. K., Light and electron microscopic studies on the localization of hyaluronic acid in developing rat cerebellum. J. Cell Biol.106 (1988) 845–855.

    Article  CAS  PubMed  Google Scholar 

  104. Ripellino, J. A., Margolis, R. U., and Margolis, R. K., Immunoelectron microscopic localization of hyaluronic acid-binding region and link protein epitopes in brain. J. Cell Biol.108 (1989) 1899–1907.

    Article  CAS  PubMed  Google Scholar 

  105. Rosa, P., Hille, A., Lee, R. W. H., Zanini, A., DeCamilli, P., and Huttner, W. B., Secretogranins I and II: Two tyrosine-sulfated secretory proteins common to a variety of cells secreting peptides by the regulated pathway. J. Cell Biol.101 (1985) 1999–2011.

    Article  CAS  PubMed  Google Scholar 

  106. Ruoslahti, E., and Yamaguchi, Y., Proteoglycans as modulators of growth factor activities. Cell64 (1991) 867–869.

    Article  CAS  PubMed  Google Scholar 

  107. Sahin, M. and Hockfield, S., Molecular identification of the Lugaro cell in the cat cerebellar cortex. J. comp. Neurol.301 (1990) 575–584.

    Article  CAS  PubMed  Google Scholar 

  108. Schubert, D., Schroeder, R., LaCorbiere, M., Saitoh, T., and Cole, G., Amyloid β protein precursor is possibly a heparan sulfate proteoglycan core protein. Science241 (1988) 223–226.

    Article  CAS  PubMed  Google Scholar 

  109. Schulz, M., Raju, T., Ralston, G., and Bennett, M. R., A retinal ganglion cell neurotrophic factor purified from superior colliculus. J. Neurochem.55 (1990) 832–841.

    Article  CAS  PubMed  Google Scholar 

  110. Schwartz, N. B. and Smalheiser, N. R., Biosynthesis of glycosaminoglycans and proteoglycans, in: Neurobiology of Glycoconjugates, pp. 151–186. Eds R. U. Margolis and R. K. Margolis. Plenum Publishing Corp., New York, 1989.

    Chapter  Google Scholar 

  111. Scanton, T. W., Iwata, M., and Carlson, S. S. A keratan sulfate membrane proteoglycan of synaptic vesicles. J. Neurochem. (1993), in press.

  112. Sheppard, A. M., Hamilton, S. K., and Pearlman, A. L., Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J. Neurosci.11 (1991) 3928–3942.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Shioi, J., Anderson, J. P., Ripellino, J. A., and Robakis, N. K., Chondroitin sulfate proteoglycan form of the Alzheimer's β-amyloid precursor. J. biol. Chem.267 (1992) 13819–13822.

    Article  CAS  PubMed  Google Scholar 

  114. Snow, D. M., and Letourneau, P. C., Neurite outgrowth on a step gradient of chondroitin sulfate proteoglycan. J. Neurobiol.23 (1992) 322–336.

    Article  CAS  PubMed  Google Scholar 

  115. Snow, D. M., Lemmon, V., Carrino, D. A., Caplan, A. I., and Silver, J., Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Expl Neurol.109 (1990) 111–130.

    Article  CAS  Google Scholar 

  116. Snow, D. M., Steindler, D. A., and Silver, J., Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: A possible role for a proteoglycan in the development of an axon barrier. Devl Biol.138 (1990) 359–376.

    Article  CAS  Google Scholar 

  117. Snow, D. M., Watanabe, M., Letourneau, P. C., and Silver, J., A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development113 (1991) 1473–1485.

    Article  CAS  PubMed  Google Scholar 

  118. Stallcup, W. B. and Beasley, L., Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J. Neurosci.7 (1987) 2737–2744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Stallcup, W. B., Dahlin, K., and Healy, P., Interaction of the NG2 chondroitin sulfate proteoglycan with type VI collagen. J. Cell Biol.111 (1990) 3177–3188.

    Article  CAS  PubMed  Google Scholar 

  120. Streit, A., Faissner, A., Gehrig, B., and Schachner, M., Isolation and biochemical characterization of a neural proteoglycan expressing the L5 carbohydrate epitope. J. Neurochem.55 (1990) 1494–1506.

    Article  CAS  PubMed  Google Scholar 

  121. Tan, S. S., Crossin, K. L., Hoffman, S., and Edelman, G. M., Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution. Proc. natl Acad. Sci. USA84 (1987) 7977–7981.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Toole, B. P., Hyaluronate and hyaluronate-binding proteins of brain, in: Neurobiology of Glycoconjugates, pp. 411–420. Eds R. U. Margolis and R. K. Margolis. Plenum Publishing Corp., New York 1989.

    Chapter  Google Scholar 

  123. Verna, J.-M., Fichard, A., and Saxod, R., Influence of glycosaminoglycans on neurite morphology and outgrowth patterns in vitro. Int. J. devl. Neurosci.7 (1989) 389–399.

    Article  CAS  Google Scholar 

  124. Wang, L., and Denburg, J. L., A role for proteoglycans in the guidance of a subset of pioneer axons in cultured embryos of the cockroach. Neuron8 (1992) 701–714.

    Article  CAS  PubMed  Google Scholar 

  125. Watanabe, E., Fujita, S. C., Murakami, F., Hayashi, M., and Matsumura, M., A monoclonal antibody identifies a novel epitope surrounding a subpopulation of the mammalian central neurons. Neuroscience29 (1989) 645–657.

    Article  CAS  PubMed  Google Scholar 

  126. Wohlfarter, T., Fischer-Colbrie, R., Hogue-Angeletti, R., Eiden, L. E., and Winkler, H., Processing of chromogranin A within chromaffin granules starts at C- and N-terminal cleavage sites. FEBS Lett.231 (1988) 67–70.

    Article  CAS  PubMed  Google Scholar 

  127. Yamaguchi, Y., Mann, D. M., and Ruoslahti, E., Negative regulation of transforming growth factor-β by the proteoglycan decorin. Nature346 (1990) 281–284.

    Article  CAS  PubMed  Google Scholar 

  128. Yanagishita, M., Glycosylphosphatidylinositol-anchored and core protein-intercalated heparan sulfate proteoglycans in rat ovarian granulosa cells have distinct secretory, endocytotic, and intracellular degradative pathways. J. biol. Chem.267 (1992) 9505–9511.

    Article  CAS  PubMed  Google Scholar 

  129. Yayon, A., Klagsbrun, M., Esko, J. D., Leder, P., and Ornitz, D. M., Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell64 (1991) 841–848.

    Article  CAS  PubMed  Google Scholar 

  130. Zaremba, S., Guimaraes, A., Kalb, R. G., and Hockfield, S., Characterization of activity-dependent, neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron2 (1989) 1207–1219.

    Article  CAS  PubMed  Google Scholar 

  131. Zimmermann, D. R., and Ruoslahti, E., Multiple domains of the large fibroblast proteoglycan, versican. EMBO J.8 (1989) 2975–2981.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Margolis, R.K., Margolis, R.U. Nervous tissue proteoglycans. Experientia 49, 429–446 (1993). https://doi.org/10.1007/BF01923587

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01923587

Key words

Navigation