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Domains of neuronal heparan sulphate proteoglycans involved in neurite growth on laminin

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Summary

A single neuronal cell assay of neurite growth was utilized to determine types and domains of neuronal proteoglycans involved in neurite growth on laminin. Perturbations of biosynthesis and processing, enzymatic digestion with specific lyases, and competition with glycosaminoglycan side chains produced complementary data consistent with a molecular model implicating glycosaminoglycan (GAG) residues of heparan sulphate proteoglycans (HSPGs) in neurite growth. The observations suggest that HSPGs promote neurite growth on laminin by bridging between binding domains for HSPGs on laminin and on the neuronal cell surface, and that the bridge is tethered at both ends by noncovalent interactions between the binding domains and GAG side chains. Sulphation of the GAGs of HSPGs appears to be critical to the tethering and/or neurite growth-promoting activity of neuronal HSPGs.

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References

  • Ard MD, Bunge RP (1988) Heparan sulphate proteoglycan and laminin immunoreactivity on cultured astrocytes: relationship to differentiation and neurite growth. J Neurosci 8:2844–2858

    PubMed  Google Scholar 

  • Begovac PC, Shur BD (1990) Cell surface galactosylatransferase mediates the initiation of neurite outgrowth from PC12 cells on laminin. J Cell Biol 110:461–470

    Article  PubMed  Google Scholar 

  • Bottenstein JE, Skaper SS, Varon SS, Sato GH (1980) Selective survival of neurons from chick embryo sensory ganglionic dissociates utilizing serum-free supplemented medium. Exp Cell Res 125:183–190

    PubMed  Google Scholar 

  • Bronner-Fraser M, Lallier T (1988) A monoclonal antibody against a laminin-heparan sulfate proteoglycan complex perturbs cranial neural crest migration in vivo. J Cell Biol 106:1321–1329

    Article  PubMed  Google Scholar 

  • Carey DJ, Rafferty CM, Todd MS (1987) Effects of inhibition of proteoglycan synthesis on the differentiation of cultured rat Schwann cells. J Cell Biol 105:1013–1021

    Article  PubMed  Google Scholar 

  • Clement B, Segui-Real B, Hassell JR, Martin GR, Yamada Y (1989) Identification of a cell surface-binding protein for the core protein of the basement membrane proteoglycan. J Biol Chem 264:12467–12471

    PubMed  Google Scholar 

  • Cole GJ, Akeson R (1989) Identification of a heparin binding domain of the neural cell adhesion molecule N-CAM using synthetic peptides. Neuron 2:1157–1165

    Article  PubMed  Google Scholar 

  • Cole GJ, Burg M (1989) Characterization of a heparan sulfate proteoglycan that copurifies with the neural cell adhesion molecule. Exp Cell Res 182:44–60

    PubMed  Google Scholar 

  • Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GM (1987) Neural cell adhesion molecule. Structure, immunoglobulin-like domains, cell surface modulation, and alterative RNA splicing. Science 236:799–806

    PubMed  Google Scholar 

  • David S (1988) Neurite outgrowth from mammalian CNS neurons on astrocytes in vitro may not be mediated primarily by laminin. J Neurocytol 17:131–144

    PubMed  Google Scholar 

  • Dean JW III, Chandrasekaran S, Tanzer ML (1990) A biological role of the carbohydrate moieties of laminin. J Biol Chem 265:12553–12562

    PubMed  Google Scholar 

  • Deuel TF (1987) Polypeptide growth factors: roles in normal and abnormal cell growth. Ann Rev Cell Biol 3:443–492

    PubMed  Google Scholar 

  • Dow KE, Mirski SEL, Roder JC, Riopelle RJ (1988) Neuronal proteoglycans: biosynthesis and functional interaction with neurons in vitro. J Neurosci 8:3278–3289

    PubMed  Google Scholar 

  • Dow KE, Riopelle RJ, Bols M, Ison ER, Plenkiewcz J, Szarek WA, Lyon A, Kisilevsky R (1990) Effects of a novel carbohydrate 4-deoxy-L-threo-pentose, on neuronal cell proteoglycan synthesis and function. Neurobiol Aging 11:307A

    Google Scholar 

  • Elbein AD, Pan YT, Solf R, Vosbeck K (1983) Effect of swainsonine, an inhibitor of glycoprotein processing, on cultured mammalian cells. J Cell Physiol 115:265–275

    PubMed  Google Scholar 

  • Engvall E, Davis GE, Dickerson K, Ruoslahti E, Varon S, Manthorpe M (1986) Mapping of domains in human laminin using monoclonal antibodies: localization of the neurite-promoting site. J Cell Biol 103:1457–1465

    Article  Google Scholar 

  • Fujiwara S, Shinkai H, Deutzmann R, Paulsson M, Timpl R (1988) Structure and distribution of N-linked oligosaccharide chains on various domains of mouse tumour laminin. Biochem J 252:453–461

    PubMed  Google Scholar 

  • Gallagher JT, Lyon M, Steward WP (1986) Structure and function of heparan sulphate proteoglycans. Biochem J, 236:313–325

    PubMed  Google Scholar 

  • Gowda DC, Goossen B, Margolis RK, Margolis RU (1989a) Chondroitin sulfate and heparan sulfate proteoglycans of PC12 pheochromocytoma cells. J Biol Chem 264:11436–11443

    PubMed  Google Scholar 

  • Gowda DC, Margolis RU, Margolis RK (1989b) Presence of the HNK-1 epitope on poly(N-acetyllactosaminyl) oligosaccharides and identification of multiple core proteins in the chondroitin sulfate proteoglycans of brain. Biochemistry 28:4468–4474

    PubMed  Google Scholar 

  • Hoffman S, Crossin KL, Edelman GM (1988) Molecular forms, binding functions, and developmental expression patterns of cytotactin and cytotactin-binding proteoglycan, an interactive pair of extracellular matrix molecules. J Cell Biol 106:519–532

    PubMed  Google Scholar 

  • Johnson-Green P, Dow KE, Riopelle RJ (1991) Characterization of glycosaminoglycan production by primary astrocytes in vitro. Glia (in press).

  • Kouzi-Koliakos K, Koliakos GG, Tsilibary EC, Furcht LT, Charonis AS (1989) Mapping of three major heparin-binding sites on laminin and identification of a novel heparin-binding site on the B1 chain. J Biol Chem 264:17971–17978

    PubMed  Google Scholar 

  • Lee YG, Radhakrishnamurthy B, Dalferes ER Jr, Berenson GS (1987) Fractionation of aorta glycosaminoglycans by high-performance liquid chromatography. J Chromatog 419:275–279

    Google Scholar 

  • Matthew WD, Greenspan RJ, Lander AD, Reichardt LF (1985) Immunopurification and characterization of a neuronal heparan sulfate proteoglycan. J Neurosci 5:1842–1850

    PubMed  Google Scholar 

  • McGarry RC, Riopelle RJ, Roder JC (1985) Accelerated regenerative neurite formation by a neuronal surface epitope reactive with the monoclonal antibody, Leu 7. Neurosci Lett 56:95–100

    Article  PubMed  Google Scholar 

  • Mobley WC, Schenker A, Shooter EM (1976) Characterization and isolation of proteolytically modified nerve growth factor. Biochemistry 15:5543–5551

    PubMed  Google Scholar 

  • Nybroe O, Moran N, Bock E (1989) Equilibrium binding analysis of neural cell adhesion molecule binding to heparin. J Neurochem 52:1947–1949

    PubMed  Google Scholar 

  • Pesheva P, Horwitz AF, Schachner M (1987) Neurosci Lett 83:303–306

    Article  PubMed  Google Scholar 

  • Probstmeier R, Kuhn K, Schachner M (1989) Binding properties of the neural cell adhesion molecule to different components of the extracellular matrix. J Neurochem 53:1794–1801

    PubMed  Google Scholar 

  • Rapraeger A, Jalkanen M, Endo E, Koda J, Bernfield M (1985) The cell surface proteoglycan from mouse mammary epithelial cells bears chondroitin sulfate and heparan sulfate glycosaminoglycans. J Biol Chem 260:11046–11052

    PubMed  Google Scholar 

  • Riopelle RJ, Cameron DA (1984) Neurite-promoting factors from embryonic neurons. Dev Brain Res 15:265–274

    Article  Google Scholar 

  • Riopelle RJ, Dow KE (1991a) Functional interactions of neuronal heparan sulphate proteoglycans with laminin. Brain Res 525:92–100

    Article  Google Scholar 

  • Riopelle RJ, Dow KE (1991) Neurite formation on laminin: effects of a galactosyltransferase on primary sensory neurons. Brain Res 541:265–272

    Article  PubMed  Google Scholar 

  • Riopelle RJ, McGarry RC, Roder JC (1986) Adhesion properties of a neuronal epitope recognized by the monoclonal antibody HNK-1 Brain Res 367:20–25

    Article  PubMed  Google Scholar 

  • Ruoslahti E (1988) Structure and biology of proteoglycans. Ann Rev Cell Biol 4:229–255

    PubMed  Google Scholar 

  • Saul R, Chambers JP, Molyneux RJ, Elbein AD (1983) Castanospermine, a tetrahydroxylated alkaloid that inhibitis β-glucosidase and β-glucocerebrosidase. Arch Biochem Biophys 221:593–597

    PubMed  Google Scholar 

  • Scott JE, Dorling J (1965) Differential staining of acid glycosaminoglycans (mucopolysaccharides) by alcian blue in salt solutions. Histochemie 5:221–233

    PubMed  Google Scholar 

  • Shing Y, Folkman J, Weisz PB, Joullie MM, Ewing WR (1990) Affinity of fibroblast growth factors for B-cyclodextrin tetradecasulfate. Anal Biochem 185:108–111

    PubMed  Google Scholar 

  • Shively JE, Conrad HE (1976) Formation of anhydrosugars in the chemical depolymerization of heparin. Biochemistry 15:3932–3942

    PubMed  Google Scholar 

  • Skubitz APN, McCarthy JB, Charonis AS, Furcht LT (1989) Novel synthetic heparin binding peptides of laminin and fibronectin which promote the adhesion of melanoma cells. Invas Metast 9:89–101

    Google Scholar 

  • Sutter A, Riopelle RJ, Harris-Warrick RM, Shooter EM (1979) The heterogeneity of nerve growth factor receptors. In: Bitensky M, Collier RJ, Steiner DF, Fox CF (eds) Progress in clinical and biological research 31: Transmembrane signalling. Liss, New York, pp 659–667

    Google Scholar 

  • Tomaselli KJ, Reichardt LF (1989) Integrins, cadherins, and cell adhesion molecules of the immunoglobulin superfamily: neuronal receptors that regulate axon growth and guidance. In: Landmesser LT (ed) The assembly of the nervous system. Liss, New York, pp 81–108

    Google Scholar 

  • Tulsiani DRP, Harris TM, Touster O (1982) Swainsonine inhibits the biosynthesis of complex glycoproteins by inhibition of golgi mannosidase II. J Biol Chem 257: 7936–7939

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Yanagishita M, Midura RJ, Hascall VC (1987) Proteoglycans: isolation and purification from tissue cultures. Meth Enzymol 138:279–289

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Pediatrics, Queen's University Kingston General Hospital, K7L 2V7, Kingston, Ontario, Canada

    K. E. Dow

  2. Department of Medicine, Queen's University Kingston General Hospital, K7L 2V7, Kingston, Ontario, Canada

    R. J. Riopelle

  3. Department of Pathology, Queen's University Kingston General Hospital, K7L 2V7, Kingston, Ontario, Canada

    R. Kisilevsky

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  1. K. E. Dow
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  2. R. J. Riopelle
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  3. R. Kisilevsky
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Dow, K.E., Riopelle, R.J. & Kisilevsky, R. Domains of neuronal heparan sulphate proteoglycans involved in neurite growth on laminin. Cell Tissue Res. 265, 345–351 (1991). https://doi.org/10.1007/BF00398082

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  • DOI: https://doi.org/10.1007/BF00398082

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