Skip to main content

Proteoglycans and Hyaluronan in Morphogenesis and Differentiation

  • Chapter
Cell Biology of Extracellular Matrix

Abstract

The objective of this chapter is to discuss the roles of hyaluronan (HA) and proteoglycans (PGs) in developmental processes and tissue remodeling. In the first section I have summarized recent progress on the molecular basis of HA and PG interactions with the surface of cells, since this is the most likely means whereby HA and PGs would influence cell behavior during development. This is followed by a review of cellular studies, mainly performed in vitro, that implicate HA and PGs in specific aspects of cell behavior that would be relevant to development in vivo. Finally, I have chosen three developmental systems to illustrate ways in which HA or PGs are involved in actual morphogenetic and differentiative processes.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Alho, A. M., and Underhill, C. B., 1989, The hyaluronate receptor is preferentially expressed on proliferating epithelial cells, J. Cell Biol. 108:1557–1565.

    Article  PubMed  CAS  Google Scholar 

  • Anderson, C. B., and Meier, S., 1982, Effect of hyaluronidase treatment on the distribution of cranial neural crest cells in the chick embryo, J. Exp. Zool. 221:329–335.

    Article  PubMed  CAS  Google Scholar 

  • Angello, J. C., and Hauschka, S. D., 1980, Hyaluronate—cell interaction: Effects of exogenous hyaluronate on muscle fibroblast cell surface composition, Exp. Cell Res. 125:389–400.

    Article  CAS  Google Scholar 

  • Aono, H., and Ide, H., 1988, A gradient of responsiveness to the growth-promoting activity of ZPA (zone of polarizing activity) in the chick limb bud, Dev. Biol. 128:136–141.

    CAS  Google Scholar 

  • Aruffo, A., Stamenkovic, I., Melnick, M., Underhill, C. B., and Seed, B., 1990, CD44 is the principal cell surface receptor for hyaluronate, Cell 61:1303–1313.

    Article  PubMed  CAS  Google Scholar 

  • Baird, A., and Ling, N., 1987, Fibroblast growth factors are present in the extracellular matrix produced by endothelial cells in vitro: Implications for a role of heparinase-like enzymes in the neovascular response, Biochem. Biophys. Res. Commun. 142:428–435.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Banerjee, S. D., Cohn, R. H., and Bernfield, M. R., 1977, Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology, J. Cell Biol. 73:445–463.

    Article  PubMed  CAS  Google Scholar 

  • Barnhart, B. J., Cox, S. H., and Kraemer, P. M., 1979, Detachment variants of Chinese hamster cells. Hyaluronic acid as a modulator of cell detachment, Exp. Cell Res. 119:327–332.

    Article  CAS  Google Scholar 

  • Bell, K. M., and McLachlan, J. C., 1985, Stimulation of division in mouse 3T3 cells by coculture with embryonic chick limb tissue, J. Embryo]. Exp. Morphol. 86:219–226.

    CAS  Google Scholar 

  • Benitz, W. E., Kelley, R. T., Anderson, C. M., Lorant, D. E., and Bernfield, M., 1990, Endothelial heparan sulfate proteoglycan. I. Inhibitory effects on smooth muscle cell proliferation, Am. J. Respir. Cell Mol. Biol. 2:13–24.

    CAS  Google Scholar 

  • Bernfield, M. R., and Banerjee, S. D., 1972, Acid mucopolysaccharide (glycosaminoglycan) at the epithelial—mesenchymal interface of mouse embryo salivary glands, J. Cell Biol. 52:664–673.

    Article  PubMed  CAS  Google Scholar 

  • Bernfield, M., and Sanderson, R. D., 1990, Syndecan, a developmentally regulated cell surface proteoglycan that binds extracellular matrix and growth factors, Philos. Trans. R. Soc. London 327:171–186.

    Article  CAS  Google Scholar 

  • Bernfield, M., Banerjee, S. D., Koda, J. E., and Rapraeger, A. C., 1984, Remodeling of the basement membrane as a mechanism of morphogenetic tissue interaction, in: The Role of Extracellular Matrix in Development (R. L. Trelstad, ed.), pp. 545–572, Liss, New York.

    Google Scholar 

  • Bertrand, P., and Delpech, B., 1985, Interaction of hyaluronectin with hyaluronic acid oligosaccharides, J. Neurochem. 45:434–439.

    Article  PubMed  CAS  Google Scholar 

  • Bilozur, M. E., and Biswas, C., 1990, Identification and characterization of heparan sulfate-binding proteins from human lung carcinoma cells, J. Biol. Chem. 265:19697–19703.

    CAS  Google Scholar 

  • Biswas, C., and Toole, B. P., 1987, Modulation of the extracellular matrix by tumor cell—fibroblast interactions, in: Cell Membranes (E. Elson, W. Frazier and L. Glaser, eds.), pp. 341–363, Plenum Press, New York.

    Chapter  Google Scholar 

  • Boyd, F. T., and Massague, J., 1989, Transforming growth factor-ß inhibition of epithelial cell proliferation linked to the expression of a 53-kDa membrane receptor, J. Biol. Chem. 264:2272–2278.

    PubMed  CAS  Google Scholar 

  • Brecht, M., Mayer, U., Schlosser, E., and Prehm, P., 1986, Increased hyaluronate synthesis is required for fibroblast detachment and mitosis, Biochem. J. 239:445–450.

    PubMed  CAS  Google Scholar 

  • Brennan, M. J., Oldberg, A., Hayman, E G, and Ruoslahti, E., 1983, Effect of a proteoglycan produced by rat tumor cells on their adhesion to fibronectin—collagen substrata, Cancer Res. 43:4302–4307.

    PubMed  CAS  Google Scholar 

  • Cardin, A. D., and Weintraub, H. J. R., 1989, Molecular modeling of protein—glycosaminoglycan interactions, Arteriosclerosis 9:21–32.

    Article  PubMed  CAS  Google Scholar 

  • Carey, D. J., and Stahl, R. C., 1990, Identification of a lipid-anchored heparan sulfate proteoglycan in Schwann cells, J. Cell Biol. 111:2053–2062.

    Article  PubMed  CAS  Google Scholar 

  • Castellot, J. J., Addonizio, M. L., Rosenberg, R., and Karnovsky, M. J., 1981, Cultured endothelial cells produce a heparinlike inhibitor of smooth muscle cell growth, J. Cell Biol. 90:372–379.

    Article  PubMed  CAS  Google Scholar 

  • Castellot, J. J., Wong, K., Herman, B., Hoover, R. L., Albertini, D. F., Wright, T. C., Caleb, B. L., and Karnovsky, M. J., 1985, Binding and internalization of heparin by vascular smooth muscle cells, J. Cell. Physiol. 124:13–20.

    Article  PubMed  CAS  Google Scholar 

  • Castellot, J. J., Wright, T. C., and Karnovsky, M. J., 1987, Regulation of vascular smooth muscle cell growth by heparin and heparan sulfates, Semin. Thromb. Hemost. 13:489–503.

    Article  CAS  Google Scholar 

  • Cheifetz, S., and Massague, J., 1989, Transforming growth factor-ß (TGF-ß) receptor proteoglycan. Cell surface expression and ligand binding in the absence of glycosaminoglycan chains. J. Biol. Chem. 264:12025–12028.

    PubMed  CAS  Google Scholar 

  • Chen, W. Y. J., Grant, M. E., Schor, A. M., and Schor, S. L., 1989, Differences between adult and foetal fibroblasts in the regulation of hyaluronate synthesis: Correlation with migratory activity, J. Cell Sci. 94:577–584.

    CAS  Google Scholar 

  • Chernoff, E. A., 1988, The role of endogenous heparan sulfate proteoglycan in adhesion and neurite outgrowth from dorsal root ganglia, Tissue Cell 20:165–178.

    CAS  Google Scholar 

  • Chiu, A. Y., Matthew, W. D., and Patterson, P. H., 1986, A monoclonal antibody that blocks the activity of a neurite regeneration-promoting factor: Studies on the binding site and its localization in vivo, J. Cell Biol. 103:1383–1398.

    Article  PubMed  CAS  Google Scholar 

  • Clement, B., Segui-Real, B., Hassell, J. R., Martin, G. R., and 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  CAS  Google Scholar 

  • Cochran, D. L., Castellot, J. J., Robinson, J. M., and Karnovsky, M. J., 1988, Heparin modulates the secretion of a major excreted protein-like molecule by vascular smooth muscle cells, Biochim. Biophys. Acta 967:289–295.

    CAS  Google Scholar 

  • Comper, W. D., and Laurent, T. C., 1978, Physiological function of connective tissue polysaccharides, Physiol. Rev. 58:255–315.

    PubMed  CAS  Google Scholar 

  • Copp, A. J., and Bernfield, M., 1988, Accumulation of basement membrane-associated hyaluronate is reduced in the posterior neuropore region of mutant (curly tail) mouse embryos developing spinal neural tube defects, Dev. Biol. 130:583–590.

    CAS  Google Scholar 

  • Crossman, M. V., and Mason, R. M., 1990, Purification and characterization of a hyaluronanbinding protein from rat chondrosarcoma, Biochem. J. 266: 399–406.

    PubMed  CAS  Google Scholar 

  • Culty, M., Miyake, K., Kincade, P. W., Sikorski, E., Butcher, E. C., and Underhill, C., 1990, The hyaluronate receptor is a member of the CD44 family of cell surface glycoproteins, J. Cell Biol. 111:2765–2774.

    Article  PubMed  CAS  Google Scholar 

  • Damon, D. H., Lobb, R. R., D’Amore, P. A., and Wagner, J. A., 1989, Heparin potentiates the action of acidic fibroblast growth factor by prolonging its biological half-life, J. Cell. Physiol. 138:221–226.

    Article  PubMed  CAS  Google Scholar 

  • Dauca, M., Bouziges, F., Colin, S., Kedinger, M., Keller, J. M., Schilt, J., Simon-Assmann, P., and Haffen, K., 1990, Development of the vertebrate small intestine and mechanisms of cell differentiation, Int. J. Dev. Biol. 34:205–218.

    CAS  Google Scholar 

  • Decker, M., Chiu, E. S., Dollbaum, C., Moiin, A., Hall, J., Spendlove, R., Longaker, M. T., and Stern, R., 1989, Hyaluronic acid-stimulating activity in sera from the bovine fetus and from breast cancer patients, Cancer Res. 49:3499–3505.

    PubMed  CAS  Google Scholar 

  • DiMario, J., Buffinger, N., Yamada, S., and Strohman, R. C., 1989, Fibroblast growth factor in the extracellular matrix of dystrophic (mdx) mouse muscle, Science 244:688–690.

    Article  PubMed  CAS  Google Scholar 

  • Dow, K. E., Mirski, S. E. L., Roder, J. C., and Riopelle, R. J., 1988, Neuronal proteoglycans• Biosynthesis and functional interaction with neurons in vitro, J. Neurosci. 8:3278–3289.

    PubMed  CAS  Google Scholar 

  • Edgar, D., Timpl, R., and Thoenen, H., 1988, Structural requirements for the stimulation of neurite outgrowth by two variants of laminin and their inhibition by antibodies, J. Cell Biol. 106:1299–1306.

    Article  PubMed  CAS  Google Scholar 

  • Ekblom, P., Vestweber, D., and Kemler, R., 1986, Cell–matrix interactions and cell adhesion during development, Annu. Rev. Cell Biol. 2:27–47.

    Article  CAS  Google Scholar 

  • Erickson, C. A., and Turley, E. A., 1983, Substrata formed by combinations of extracellular matrix components alter neural crest cell motility in vitro, J. Cell Sci. 61:299–323.

    PubMed  CAS  Google Scholar 

  • Fedarko, N. S., and Conrad, H. E., 1986, A unique heparan sulfate in the nuclei of hepatocytes: Structural changes with the growth state of the cells, J. Cell Biol. 102:587–599.

    Article  PubMed  CAS  Google Scholar 

  • Fekardo, N. S., Ishihara, M., and Conrad, H. E., 1989, Control of cell division in hepatoma cells by exogenous heparan sulfate proteoglycan, J. Cell Physiol. 139:287–294.

    Article  Google Scholar 

  • Flaumenhaft, R., Moscatelli, D., Saksela, O., and Rifkin, D. B., 1989, Role of extracellular matrix in the action of basic fibroblast growth factor: Matrix as a source of growth factor for long-term stimulation of plasminogen activator production and DNA synthesis, J. Cell. Physiol. 140:75–81.

    Article  PubMed  CAS  Google Scholar 

  • Folkman, J., Klagsbrun, M., Sasse, J., Wadzinski, M., Ingber, D., and Vlodaysky, I., 1988, A heparin-binding angiogenic protein—basic fibroblast growth factor—is stored within basement membrane, Am. J. Pathol. 130:393–400.

    CAS  Google Scholar 

  • Frenz, D. A., Akiyama, S. K., Paulsen, D. F., and Newman, S. A., 1989, Latex beads as probes of cell surface–extracellular matrix interactions during chondrogenesis: Evidence for a role for amino-terminal heparin-binding domain of fibronectin, Dev. Biol. 136:87–96.

    CAS  Google Scholar 

  • Fritze, L. M. S., Reilley, C. F., and Rosenberg, R. D., 1985, An antiproliferative heparan sulfate species produced by postconfluent smooth muscle cells, J. Cell Biol. 100:1041–1049.

    Article  PubMed  CAS  Google Scholar 

  • Frost, S. J., and Weigel, P. H., 1990, Binding of hyaluronic acid to mammalian fibrinogens, Biochim. Biophys. Acta 1034:39–45.

    Article  PubMed  CAS  Google Scholar 

  • Fukuda, Y., Masuda, Y., Kishi, J.-I., Hashimoto, Y., Hayakawa, T., Nogawa, H., and Nakanishi, Y., 1988, The role of interstitial collagens in cleft formation of mouse embryonic submandibular gland during initial branching, Development 103:259–267.

    PubMed  CAS  Google Scholar 

  • Goetinck, P. F., Stirpe, N. S., Tsonis, P. A., and Carlone, D., 1987, The tandemly repeated sequences of cartilage link protein contain the sites for interaction with hyaluronic acid, J. Cell Biol. 105:2403–2408.

    Article  PubMed  CAS  Google Scholar 

  • Goldberg, R. L., and Toole, B. P., 1984, Pericellular coat of chick embryo chondrocytes: Structural role of hyaluronate, J. Cell Biol. 99:2114–2122.

    Article  PubMed  CAS  Google Scholar 

  • Goldberg, R. L., and Toole, B. P., 1987, Hyaluronate inhibition of cell proliferation, Arthritis Rheum. 30:769–778.

    Article  PubMed  CAS  Google Scholar 

  • Goldstein, L. A., Zhou, D. F. H., Picker, L. J., Minty, C. N., Bargatze, R. F., Ding, J. F., and Butcher, E. C., 1989, A human lymphocyte homing receptor, the Hermes antigen, is related to cartilage proteoglycan core and link proteins, Cell 56:1063–1072.

    Article  PubMed  CAS  Google Scholar 

  • Green, S. J., Tarone, G., and Underhill, C. B., 1988, Aggregation of macrophages and fibroblasts is inhibited by a monoclonal antibody to the hyaluronate receptor, Exp. Cell Res. 178:224–232.

    Article  CAS  Google Scholar 

  • Hantaz-Ambroise, D., Vigny, M., and Koenig, J., 1987, Heparan sulfate proteoglycan and laminin mediate two different types of neurite outgrowth, J. Neurosci. 7:2293–2304.

    CAS  Google Scholar 

  • Hausser, H., Hoppe, W., Rauch, U., and Kresse, H., 1989, Endocytosis of a small dermatan sulphate proteoglycan. Identification of binding proteinsBiochem. J. 263:137–142.

    PubMed  CAS  Google Scholar 

  • Hautanen, A., Gailit, J., Mann, D. M., and Ruoslahti, E., 1989, Effects of modifications of the RGD sequence and its context on recognition by the fibronectin receptor, J. Biol. Chem. 264:1437–1442.

    PubMed  CAS  Google Scholar 

  • Hayashi, K., Hayashi, M., Jalkanen, M., Firestone, J. H., Trelstad, R. L., and Bernfield, M., 1987, Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissues. A light and electron microscopic study, J. Histochem. Cytochem. 35:1079–1088.

    Article  PubMed  CAS  Google Scholar 

  • Haynes, B. F., Telen, M. J., Hale, L. P., and Denning, S. M., 1989, CD44—A molecule involved in leukocyte adherence and T-cell activation, Immunol. Today 10:423–428.

    CAS  Google Scholar 

  • Herman, I. M., and Castellot, J. J., 1987, Regulation of vascular smooth muscle cell growth by endothelial-synthesized extracellular matrices, Arteriosclerosis 7:463–469.

    Article  PubMed  CAS  Google Scholar 

  • Herndon, M. E., and Lander, A. D., 1990, A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system, Neuron 4:949–961.

    Article  PubMed  CAS  Google Scholar 

  • Hockfield, S., 1990, Proteoglycans in neural development, Semin. Dev. Biol. 1:55–63.

    Google Scholar 

  • Hoffman, S., and Edelman, G. M., 1987, A proteoglycan with HNK-1 antigenic determinants is a neuron-associated ligand for cytotactin, Proc. Natl. Acad. Sci. USA 84:2523–2527.

    Article  PubMed  CAS  Google Scholar 

  • Hurle, J. M., Ganan, Y., and Macias, D., 1989, Experimental analysis of the in vivo chondrogenic potential of the interdigital mesenchyme of the chick leg bud subjected to local ectodermal removal, Dev. Biol. 132:368–374.

    CAS  Google Scholar 

  • Ishihara, M., and Conrad, H. E., 1989, Correlations between heparan sulfate metabolism and hepatoma growth, J. Cell Physiol. 138:467–476.

    Article  PubMed  CAS  Google Scholar 

  • Ishihara, M., Fedarko, N. S., and Conrad, H. E., 1987, Involvement of phosphatidylinositol and insulin in the coordinate regulation of proteoheparan sulfate metabolism and hepatocyte growth, J. Biol. Chem. 262:4708–4716.

    PubMed  CAS  Google Scholar 

  • Kardami, E., Spector, D., and Strohman, R. C., 1988, Heparin inhibits skeletal muscle growth in vitro, Dev. Biol. 126:19–28.

    CAS  Google Scholar 

  • Kimata, K., Oike, Y., Tani, K., Shinomura, T., Yamagata, M., Uritani, M., and Suzuki, S., 1986, A large chondroitin sulfate proteoglycan (PG-M) synthesized before chondrogenesis in the limb bud of chick embryo, J. Biol. Chem. 261:13517–13525.

    PubMed  CAS  Google Scholar 

  • Kinsella, M. G., and Wight, T. N., 1986, Modulation of sulfated proteoglycan synthesis by bovine aortic endothelial cells during migration, J. Cell Biol. 102:679–687.

    Article  PubMed  CAS  Google Scholar 

  • Kjellen, L., Oldberg, A., and Hook, M., 1980, Cell-surface heparan sulfate: Mechanisms of proteoglycan–cell association, J. Biol. Chem. 255:10407–10413.

    PubMed  CAS  Google Scholar 

  • Kjellen, L., Pettersson, I., and Hook, M., 1981, Cell-surface heparan sulfate: An intercalated membrane proteoglycan, Proc. Natl. Acad. Sci. USA 78:5371–5375.

    Article  PubMed  CAS  Google Scholar 

  • Knudson, C. B., 1991, Cell–cell adhesion of limb bud mesoderm mediated by hyaluronan, submitted.

    Google Scholar 

  • Knudson, C. B., and Knudson, W., 1990, Similar epithelial–stromal interactions in the regulation of hyaluronate production during limb morphogenesis and tumor invasion, Cancer Lett. 52:113–122.

    Article  PubMed  CAS  Google Scholar 

  • Knudson, W., and Knudson, C. B., 1991, Assembly of a chondrocyte-like pericellular matrix on non-chondrogenic cells. Role of the cell surface hyaluronan receptors in the assembly of a pericellular matrix, J. Cell Sci. 99:227–235.

    Google Scholar 

  • Knudson, C. B., and Toole, B. P., 1985, Changes in the pericellular matrix during differentiation of limb bud mesoderm, Dev. Biol. 112:308–318.

    CAS  Google Scholar 

  • Knudson, C. B., and Toole, B. P., 1987, Hyaluronate–cell interactions during differentiation of chick embryo limb mesoderm, Dev. Biol. 124:82–90.

    CAS  Google Scholar 

  • Knudson, C. B., and Toole, B. P., 1988, Epithelial—mesenchymal interaction in the regulation of hyaluronate production during limb development, Biochem. Int. 17:735–745.

    CAS  Google Scholar 

  • Knudson, W., Biswas, C., and Toole, B. P., 1984, Interactions between human tumor cells and fibroblasts stimulate hyaluronate synthesis, Proc. Natl. Acad. Sci. USA 81:6767–6771.

    Article  PubMed  CAS  Google Scholar 

  • Koda, J. E., Rapraeger, A., and Bernfield, M., 1985, Heparan sulfate proteoglycans from mouse mammary epithelial cells. Cell surface proteoglycan as a receptor for interstitial collagens, J. Biol. Chem. 260:8157–8162.

    PubMed  CAS  Google Scholar 

  • Kujawa, M. J., Pechak, D. G., Fiszman, M. Y., and Caplan, A. I., 1986, Hyaluronic acid bonded to cell culture surfaces inhibits the program of myogenesis, Dev. Biol. 113:10–16.

    CAS  Google Scholar 

  • Kulyk, W. M., Rodgers, B. J., Greer, K., and Kosher, R. A., 1989, Promotion of embryonic chick limb cartilage differentiation by transforming growth factor-beta, Dev. Biol. 135:424–430.

    CAS  Google Scholar 

  • Lacy, B. E., and Underhill, C. B., 1987, The hyaluronate receptor is associated with actin filaments, J. Cell Biol. 105:1395–1404.

    Article  PubMed  CAS  Google Scholar 

  • Lander, A. D., 1989, Understanding the molecules of neural cell contacts: Emerging patterns of structure and function, Trends Neurosci. 12:189–195.

    Article  PubMed  CAS  Google Scholar 

  • Lankes, W., Griesmacher, A., Grunwald, J., Schwartz-Albiez, R., and Keller, R., 1988, A heparin-binding protein involved in inhibition of smooth-muscle cell proliferation, Biochem. J. 251:831–842.

    PubMed  CAS  Google Scholar 

  • Laurent, T. C., Fraser, J. R. E., Pertoft, H., and Smedsrod, B., 1986, Binding of hyaluronate and chondroitin sulphate to liver endothelial cells, Biochem. J. 234:653–658.

    PubMed  CAS  Google Scholar 

  • LeBaron, R. G., Esko, J. D., Woods, A., Johansson, S., and Hook, M., 1988, Adhesion of glycosaminoglycan-deficient Chinese hamster ovary cell mutants to fibronectin substrata, J. Cell Biol. 106:945–952.

    Article  CAS  Google Scholar 

  • LeBaron, R. G., Hook, A., Esko, J. D., Gay, S., and Hook, M., 1989, Binding of heparan sulfate to type V collagen. A mechanism of cell—substrate adhesion, J. Biol. Chem. 264:7950–7956.

    PubMed  CAS  Google Scholar 

  • Lelongt, B., Makino, H., Dalecki, T. M., and Kanwar, Y. S., 1988, Role of proteoglycans in renal development, Dev. Biol. 128:256–276.

    CAS  Google Scholar 

  • Lesley, J., Schulte, R., and Hyman, R., 1990, Binding of hyaluronic acid to lymphoid cell lines is inhibited by monoclonal antibodies against Pgp-1, Exp. Cell Res. 187:224–233.

    Article  CAS  Google Scholar 

  • Lewandowska, K., Choi, H. U., Rosenberg, L. C., Zardi, L., and Culp, L. A., 1987, Fibronectinmediated adhesion of fibroblasts: Inhibition by dermatan sulfate proteoglycan and evidence for a cryptic glycosaminoglycan-binding domain, J. Cell Biol. 105:1443–1454.

    Article  PubMed  CAS  Google Scholar 

  • Luikart, S. D., Maniglia, C. A., Furcht, L. T., McCarthy, J. B., and Oegema, T. R., 1990, A heparin sulfate-containing fraction of bone marrow stroma induces maturation of HL-60 cells in vitro, Cancer Res. 50:3781–3785.

    PubMed  CAS  Google Scholar 

  • Majack, R. A., and Bornstein, P., 1985, Heparin regulates the collagen phenotype of vascular smooth muscle cells: Induced synthesis of an Mi. 60,000 collagen, J. Cell Biol. 100:613–619.

    Article  PubMed  CAS  Google Scholar 

  • Majack, R. A., Goodman, L. V., and Dixit, V. M., 1988, Cell surface thrombospondin is functionally essential for vascular smooth muscle cell proliferation, J. Cell Biol. 106:415–422.

    Article  PubMed  CAS  Google Scholar 

  • Margolis, R. U., and Margolis, R. K., 1989, Nervous tissue proteoglycans, Dev. Neurosci. 11:276–288.

    CAS  Google Scholar 

  • McCaffrey, T. A., Falcone, D. J., Brayton, C. F., Agarwal, L. A., Welt, F. G. P., and Weksler, B. B., 1989, Transforming growth factor-I3 activity is potentiated by heparin via dissociation of the transforming growth factor-ß/a2-macroglobulin inactive complex, J. Cell Biol. 109:441–448.

    Article  PubMed  CAS  Google Scholar 

  • McGary, C. T., Raja, R. H., and Weigel, P. H., 1989, Endocytosis of hyaluronic acid by rat liver endothelial cells. Evidence for receptor recycling, Biochem. J. 257:875–884.

    CAS  Google Scholar 

  • Miller, D. J., Winer, M. A., and Ax, R. L., 1990, Heparin-binding proteins from seminal plasma bind to bovine spermatozoa and modulate capacitation by heparin, Biol. Reprod. 42:899–915.

    Article  CAS  Google Scholar 

  • Miyake, K., Underhill, C. B., Lesley, J., and Kincade, P. W., 1990, Hyaluronate can function as a cell adhesion molecule and CD44 participates in hyaluronate recognition, J. Exp. Med. 172:69–75.

    Article  PubMed  CAS  Google Scholar 

  • Morriss-Kay, G., and Tuckett, F., 1989, Immunohistochemical localisation of chondroitin sulphate proteoglycans and the effects of chondroitinase ABC in 9-to 11-day rat embryos, Development 106:787–798.

    PubMed  CAS  Google Scholar 

  • Morriss-Kay, G. M., Tuckett, F., and Solursh, M., 1986, The effects of Streptomyces hyaluronidase on tissue organization and cell cycle time in rat embryos, J. Embryol. Exp. Morphol. 98:59–70.

    PubMed  CAS  Google Scholar 

  • Morris-Wiman, J., and Brinkley, L. L., 1990, Changes in mesenchymal cell and hyaluronate distribution correlate with in vivo elevation of the mouse mesencephalic neural folds, Anat. Rec. 226:383–395.

    Article  PubMed  CAS  Google Scholar 

  • Munaim, S. I., Klagsbrun, M., and Toole, B. P., 1988, Developmental changes in fibroblast growth factor in the chicken embryo limb bud, Proc. Natl. Acad. Sci. USA 85:8091–8093.

    Article  CAS  Google Scholar 

  • Munaim, S. I., Klagsbrun, M., and Toole, B. P., 1991, Hyaluronan-dependent pericellular coats of chick embryo limb mesodermal cells: induction by basic fibroblast growth factor, Dev. Biol. 143:297–302.

    CAS  Google Scholar 

  • Murphy-Ullrich, J. E., and Hook, M., 1989, Thrombospondin modulates focal adhesions in endothelial cells, J. Cell Biol. 109:1309–1319.

    Article  PubMed  CAS  Google Scholar 

  • Neame, P. J., Christner, J. E., and Baker, J. R., 1987, Cartilage proteoglycan aggregates. The link protein and proteoglycan amino-terminal globular domains have similar structures, J. Biol. Chem. 262:17768–17778.

    PubMed  CAS  Google Scholar 

  • Nemec, R. E., Toole, B. P., and Knudson, W., 1987, The cell surface hyaluronate binding sites of invasive human bladder carcinoma cells, Biochem. Biophys. Res. Commun. 149:249–257.

    CAS  Google Scholar 

  • Orkin, R. W., Knudson, W., and Toole, B. P., 1985, Loss of hyaluronate-dependent coat during myoblast fusion, Dev. Biol. 107:527–530.

    CAS  Google Scholar 

  • Pericles, G., Lane, W. S., Andrews, D., Dahl, D., and Bignami, A., 1989, Isolation and partial characterization of a glial hyaluronate-binding proteinJ. Biol. Chem. 264:5981–5987.

    Google Scholar 

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

    CAS  Google Scholar 

  • Philipson, L. H., Westley, J., and Schwartz, N. B., 1985, Effect of hyaluronidase treatment of intact cells on hyaluronate synthetase activity, Biochemistry 24:7899–7906.

    Article  PubMed  CAS  Google Scholar 

  • Presta, M., Maier, J. A. M., Rusnati, M., and Ragnotti, G., 1989, Basic fibroblast growth factor is released from endothelial extracellular matrix in a biologically active form, J. Cell Physiol. 140:68–74.

    Article  PubMed  CAS  Google Scholar 

  • Pukac, L. A., Castellot, J. J., Wright, T. C., Caleb, B. L., and Karnovsky, M. J., 1990, Heparin inhibits cfos and c-myc mRNA expression in vascular smooth muscle cells, Cell Regul. 1:435–443.

    PubMed  CAS  Google Scholar 

  • Raja, R. H., McGary, C. T., and Weigel, P. H., 1988, Affinity and distribution of surface and intracellular hyaluronic acid receptors in isolated rat liver endothelial cells, J. Biol. Chem. 263:16661–16668.

    PubMed  CAS  Google Scholar 

  • Rasmussen, S., and Rapraeger, A., 1988, Altered structure of the hybrid cell surface proteoglycan of mammary epithelial cells in response to transforming growth factor-V., J. Cell Biol. 107:1959–1967.

    Article  PubMed  CAS  Google Scholar 

  • Ratner, N., Hong, D., Lieberman, M. A., Bunge, R. P., and Glaser, L., 1988, The neuronal cell-surface molecule mitogenic for Schwann cells is a heparin-binding protein, Proc. Natl. Acad. Sci. USA 85:6992–6996.

    Article  PubMed  CAS  Google Scholar 

  • Reilly, C. F., Fritze, L. M. S., and Rosenberg, R. D., 1986, Heparin inhibition of smooth muscle cell proliferation: A cellular site of action, J. Cell. Physiol. 129:11–19.

    Article  PubMed  CAS  Google Scholar 

  • Reyes, A. A., Akeson, R., Brezina, L., and Cole, G. J., 1990, Structural requirements for neural cell adhesion molecule—heparin interaction, Cell Regul. 1:567–576.

    PubMed  CAS  Google Scholar 

  • Rogelj, S., Klagsbrun, M., Atzmon, R., Kurokawa, M., Haimovitz, A., Fuks, Z., and Vlodaysky, I., 1989, Basic fibroblast growth factor is an extracellular matrix component required for supporting the proliferation of vascular endothelial cells and the differentiation of PC12 cells, J. Cell Biol. 109:823–831.

    Article  PubMed  CAS  Google Scholar 

  • Rollins, B. J., and Culp, L. A., 1979, Glycosaminoglycans in the substrate adhesion sites of normal and virus-transformed murine cells, Biochemistry 18:141–148.

    Article  PubMed  CAS  Google Scholar 

  • Rutishauser, U., Acheson, A., Hall, A. K., Mann, D. M., and Sunshine, J., 1988, The neural cell adhesion molecule (NCAM) as a regulator of cell—cell interactions, Science 240:53–57.

    Article  PubMed  CAS  Google Scholar 

  • Saksela, O., Moscatelli, D., Sommer, A., and Rifkin, D. B., 1988, Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation, J. Cell Biol. 107:743–751.

    Article  PubMed  CAS  Google Scholar 

  • Sanderson, R. D., and Bernfield, M., 1988, Molecular polymorphism of a cell surface proteoglycan: Distinct structures on simple and stratified epithelia, Proc. Natl. Acad. Sci. USA 85:9562–9566.

    Article  PubMed  CAS  Google Scholar 

  • Sanderson, R. D., Lalor, P., and Bernfield, M., 1989, B lymphocytes express and lose syndecan at specific stages of differentiation, Cell Regul. 1:27–35.

    PubMed  CAS  Google Scholar 

  • Sanes, J. R., 1989, Extracellular matrix molecules that influence neural development, Annu. Rev. Neurosci. 12:491–516.

    Article  CAS  Google Scholar 

  • Saunders, S., and Bernfield, M., 1988, Cell surface proteoglycan binds mouse mammary epithelial cells to fibronectin and behaves as a receptor for interstitial matrix, J. Cell Biol. 106:423–430.

    Article  PubMed  CAS  Google Scholar 

  • Saunders, S., Jalkanen, M., O’Farrell, S., and Bernfield, M., 1989, Molecular cloning of syndecan, an integral membrane proteoglycan, J. Cell Biol. 108:1547–1556.

    Article  PubMed  CAS  Google Scholar 

  • Schoenwolf, G. C., and Fisher, M., 1983, Analysis of the effects of Streptomyces hyaluronidase on formation of the neural tube, J. Embryol. Exp. Morphol. 73:1–15.

    PubMed  CAS  Google Scholar 

  • Schor, S. L., Schor, A. M., Grey, A. M., Chen, J., Rushton, G., Grant, M. E., and Ellis, I., 1989, Mechanism of action of the migration stimulating factor produced by fetal and cancer patient fibroblasts: Effect on hyaluronic acid synthesis, In Vitro Cell Dev. Biol. 25:737–746.

    Article  CAS  Google Scholar 

  • Seed, J., Olwin, B. B., and Hauschka, S. D., 1988, Fibroblast growth factor levels in the whole embryo and limb bud during chick development, Dev. Biol. 128:50–57.

    CAS  Google Scholar 

  • Shannon, B. T., Love, S. H., and Myrvik, Q. N., 1980, Participation of hyaluronic acid in the macrophage disappearance reaction, Immunol. Commun. 9:357–370.

    CAS  Google Scholar 

  • Singley, C. T., and Solursh, M., 1981, The spatial distribution of hyaluronic acid and mesenchymal condensation in the embryonic chick wing, Dev. Biol. 84:102–120.

    CAS  Google Scholar 

  • Smith, J. C., 1989, Mesoderm induction and mesoderm-inducing factors in early amphibian development, Development 105:665–677.

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Solursh, M., 1990, The role of extracellular matrix molecules in early limb development, Semin. Dev. Biol. 1:45–53.

    Google Scholar 

  • Solursh, M., and Jensen, K. L., 1988, The accumulation of basement membrane components during the onset of chondrogenesis and myogenesis in the chick wing bud, Development 104:41–49.

    PubMed  CAS  Google Scholar 

  • Solursh, M., Singley, C. T., and Reiter, R. S., 1981, The influence of epithelia on cartilage and loose connective tissue formation by limb mesenchyme cultures, Dev. Biol. 86:471–482.

    CAS  Google Scholar 

  • Solursh, M., Reiter, R. S., Jensen, K. L., Kato, M., and Bernfield, M., 1990, Transient expression of a cell surface heparan sulfate proteoglycan (syndecan) during limb development, Dev. Biol. 140:83–92.

    CAS  Google Scholar 

  • Spooner, B. S., Bassett, K., and Stokes, B., 1985, Sulfated glycosaminoglycan deposition and processing at the basal epithelial surface in branching and ß-n-xyloside-inhibited embryonic salivary glands, Dev. Biol. 109:177–183.

    CAS  Google Scholar 

  • Spooner, B. S., Thompson-Pletscher, H. A., Stokes, B., and Bassett, K. E., 1986, Extracellular matrix involvement in epithelial branching morphogenesis, in: Developmental Biology: A Comprehensive Synthesis (M. S. Steinberg, ed.), pp. 225–260, Plenum Press, New York.

    Google Scholar 

  • Spray, D. C., Fujita, M., Saez, J. C., Choi, H., Watanabe, T., Hertzberg, E., Rosenberg, L. C., and Reid, L. M., 1987, Proteoglycans and glycosaminoglycans induce gap junction synthesis and function in primary liver cultures, J. Cell Biol. 105:541–551.

    Article  PubMed  CAS  Google Scholar 

  • Stamenkovic, I., Amiot, M., Pesando, J. M., and Seed, B., 1989, A lymphocyte molecule implicated in lymph node homing is a member of the cartilage link protein family, Cell 56:1057–1062.

    Article  PubMed  CAS  Google Scholar 

  • Sun, X., Mosher, D. F., and Rapraeger, A., 1989, Heparan sulfate-mediated binding of epithelial cell surface proteoglycan to thrombospondin, J. Biol. Chem. 264:2885–2889.

    PubMed  CAS  Google Scholar 

  • Tammi, R., Ripellino, J. A., Margolis, R. U., Maibach, H. I., and Tammi, M., 1989, Hyaluronate accumulation in human epidermis treated with retinoic acid in skin organ culture, J. Invest. Derma tol. 92:326–332.

    Article  CAS  Google Scholar 

  • Tengblad, A., 1981, A comparative study of the binding of cartilage link protein and the hyaluronate-binding region of the cartilage proteoglycan to hyaluronate-substituted Sepharose gel, Biochem. J. 199:297–305.

    CAS  Google Scholar 

  • Toole, B. P., 1981, Glycosaminoglycans in morphogenesis, in: Cell Biology of Extracellular Matrix (E. D. Hay, ed.), pp. 259–294, Plenum Press, New York.

    Chapter  Google Scholar 

  • Toole, B. P., 1990, Hyaluronan and its binding proteins, the hyaladherins, Curr. Opin. Cell Biol. 2:839–844.

    CAS  Google Scholar 

  • Toole, B. P., Munaim, S. I., Welles, S., and Knudson, C. B., 1989, Hyaluronate–cell interactions and growth factor regulation of hyaluronate synthesis during limb development, Ciba Found. Symp. 143:138–149.

    CAS  Google Scholar 

  • Turley, E. A., 1989, Hyaluronic acid stimulates protein kinase activity in intact cells and in an isolated protein complex, J. Biol. Chem. 264:8951–8955.

    PubMed  CAS  Google Scholar 

  • Turley, E., and Auersperg, N., 1989, A hyaluronate binding protein transiently codistributes with p21k-ras in cultured cell lines, Exp. Cell Res. 182:340–348.

    Article  CAS  Google Scholar 

  • Turley, E. A., Bowman, P., and Kytryk, M. A., 1985, Effects of hyaluronate and hyaluronate binding proteins on cell motile and contact behavior, J. Cell Sci. 78:133–145.

    PubMed  CAS  Google Scholar 

  • Turley, E. A., Brassel, P., and Moore, D., 1990, A hyaluronan-binding protein shows a partial and temporally regulated codistribution with actin on locomoting chick heart fibroblasts, Exp. Cell Res. 187:243–249.

    Article  CAS  Google Scholar 

  • Underhill, C. B., and Toole, B. P., 1979, Binding of hyaluronate to the surface of cultured cells, J. Cell Biol. 82:475–484.

    Article  PubMed  CAS  Google Scholar 

  • Underhill, C. B., and Toole, B. P., 1980, Physical characteristics of hyaluronate binding to the surface of simian virus 40-transformed 3T3 cells, J. Biol. Chem. 255:4544–4549.

    PubMed  CAS  Google Scholar 

  • Underhill, C. B., and Toole, B. P., 1981, Receptors for hyaluronate on the surface of parent and virus-transformed cell lines—Binding and aggregation studies, Exp. Cell Res. 131:419–424.

    Article  CAS  Google Scholar 

  • Underhill, C. B., Chi-Rosso, G., and Toole, B. P., 1983, Effects of detergent solubilization on the hyaluronate-binding protein from membranes of simian virus 40-transformed 3T3 cells, J. Biol. Chem. 258:8086–8091.

    PubMed  CAS  Google Scholar 

  • Underhill, C. B., Green, S. J., Comoglio, P. M., and Tarone, G., 1987, The hyaluronate receptor is identical to a glycoprotein of Mr 85,000 (gp85) as shown by a monoclonal antibody that interferes with binding activity, J. Biol. Chem. 262:13142–13146.

    PubMed  CAS  Google Scholar 

  • Vainio, S., Jalkanen, M., and Thesleff, I., 1989, Syndecan and tenascin expression is induced by epithelial–mesenchymál interactions in embryonic tooth mesenchyme, J. Cell Biol. 108:1945–1954.

    Article  PubMed  CAS  Google Scholar 

  • West, D. C., and Kumar, S., 1989, The effect of hyaluronate and its oligosaccharides on endothelial cell proliferation and monolayer integrity, Exp. Cell Res. 183:179–196.

    Article  CAS  Google Scholar 

  • Whitman, M., and Melton, D. A., 1989, Growth factors in early embryogenesis, Annu. Rev. Cell Biol. 5:93–117.

    Article  CAS  Google Scholar 

  • Woods, A., Couchman, J. R., and Hook, M., 1985, Heparan sulfate of rat embryo fibroblasts. A hydrophobic form may link cytoskeleton and matrix components, J. Biol. Chem. 260:10872–10879.

    PubMed  CAS  Google Scholar 

  • Wright, T. C., Castellot, J. J., Petitou, M., Lormeau, J. C., Choay, J., and Karnovsky, M. J., 1989, Structural determinants of heparin’s growth inhibitory activity. Interdependence of oligosaccharide size and charge, J. Biol. Chem. 264:1534–1542.

    PubMed  CAS  Google Scholar 

  • Yamagata, M., Yamada, K. M., Yoneda, M., Suzuki, S., and Kimata, K., 1986, Chondroitin sulfate proteoglycan (PG-M-like proteoglycan) is involved in the binding of hyaluronic acid to cellular fibronectin, J. Biol. Chem. 261:13526–13535.

    PubMed  CAS  Google Scholar 

  • Yamagata, M., Suzuki, S., Akiyama, S. K., Yamada, K. M., and Kimata, K., 1989, Regulation of cell–substrate adhesion by proteoglycans immobilized on extracellular substrates, J. Biol. Chem. 264:8012–8018.

    PubMed  CAS  Google Scholar 

  • Yamaguchi, Y., Mann, D. M., and Ruoslahti, E., 1990, Negative regulation of transforming growth factor-ß by the proteoglycan decorin, Nature 346:281–284.

    Article  PubMed  CAS  Google Scholar 

  • Yoneda, M., Suzuki, S., and Kimata, K., 1990, Hyaluronic acid associated with the surfaces of cultured fibroblasts is linked to a serum-derived 85-kDa protein, J. Biol. Chem. 265:5247–5257.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Springer Science+Business Media New York

About this chapter

Cite this chapter

Toole, B.P. (1991). Proteoglycans and Hyaluronan in Morphogenesis and Differentiation. In: Hay, E.D. (eds) Cell Biology of Extracellular Matrix. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3770-0_10

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-3770-0_10

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6680-5

  • Online ISBN: 978-1-4615-3770-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics