Skip to main content
SpringerLink
Log in

Syndecan family of cell surface proteoglycans: Developmentally regulated receptors for extracellular effector molecules

  • Multi-author Reviews
  • Extracellular Matrix in Animal Development
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

Syndecans are a family of integral membrane proteoglycans with conserved membrane-spanning and intracellular domains but with structurally distinct extracellular domains (ectodomains). They are known to function as heparan sulphate co-receptors in fibroblast growth factor signalling as well as to link cells directly to the extracellular matrix. These and other biological activities of syndecans involve specific interactions of the heparan sulphate side chains of syndecans with cytokines and extracellular matrix proteins. Four different vertebrate syndecans, designated as syndecans 1–4 (or syndecan, fibroglycan, N-syndecan and amphiglycan, respectively), are known. During embryonic development, syndecans have specific and highly regulated expression patterns that are distinct from the expression in adult tissue, suggesting an active role in morphogenetic processes. The developmental expression of syndecans is particularly intense in mesenchymal condensates and at epithelium mesenchyme interfaces, where a number of heparan sulphate-binding cytokines and matrix components are also expressed in a regulated manner, ofter spatially and temporally co-ordinated with the syndecan expression. Recent evidence indicates that the regulation of heparan sulphate fine structure (mainly the number and arrangement of sulphate groups along the polymer) provides a mechanism for the cellular control of syndecan-protein interactions. Furthermore, morphogenetically active cytokines such as fibroblast growth factor-2 and transforming growth factor-β participate in the regulation of syndecan expression and glycosaminoglycan structure. This review discusses the developmental expression and binding functions of syndecans as well as the molecular regulation of specific heparan sulphate-protein interactions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Andres, J., DeFalcis, D., Noda, M., and Massagué, J., Binding of two growth factor families to separate domains of the proteoglycan betaglycan. J. biol. Chem.267 (1992) 5827–5930.

    Article  Google Scholar 

  2. Baciu, P., Acaster, C., and Goetinck, P. F., Temporal and spatial expression of syndecan-4 during avian embryonic development. Molec. Biol. Cell4 (1993) 413a.

    Google Scholar 

  3. Bernfield, M., Banerjee, S., and Cohn, R., Dependence of salivary epithelial morphology and branching morphogenesis upon acid mucopolysaccharide-protein (proteoglycan) at the epithelial surface J. Cell Biol.52 (1972) 674–689.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bernfield, M., Kokenyesi, R., Kato, M., Hinkes, M. T., Spring, J., Gallo, R. L., and Lose, E. J., Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. A. Rev. Cell Biol.8 (1992) 365–393.

    Article  CAS  Google Scholar 

  5. Bourin, M. C., and Lindahl, U., Glycosaminoglycans and the regulation of blood coagulation. Biochem. J.289 (1993) 313–330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Brauker, J., Trautman, M., and Bernfield, M., Syndecan, a cell surface proteoglycan exhibits molecular polymorphism during lung development. Devl Biol.147 (1991) 285–292.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Brown, T. A., Bouchard, T., St. John, T., Wayner, E., and Carter, W. G., Human keratinocytes express a new CD44 core protein (CD44E) as a heparan-sulfate intrinsic membrane proteoglycan with additional exons. J. Cell Biol.113 (1991) 207–221.

    Article  CAS  PubMed  Google Scholar 

  9. Cardin, A. D., and Weintraub, H. J. R., Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis9 (1989) 21–32.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  11. Carey, D. J., Stahl, R. C., Cizmeci-Smith, G., and Asundi, V. K., Syndecan-1 expressed in Schwann cells causes morphological transformation and cytoskeletal reorganization and associates with actin during cell spreading. J. Cell Biol.124 (1994) 161–170.

    Article  CAS  PubMed  Google Scholar 

  12. Chang, J.-Y., Binding of heparin to human antithrombin III activates selective chemical modification at lysine 236. LYS-107, LYS-125 and LYS-136 are situated within the heparin-binding site of antithrombin III. J. biol. Chem.264 (1898) 3111–3115.

    Article  Google Scholar 

  13. Chernousov, M. A., and Carey, D. J., N-syndecan (syndecan 3) from neonatal rat brain binds basic fibroblast growth factor. J. biol. Chem.268 (1993) 16810–16814.

    Article  CAS  PubMed  Google Scholar 

  14. Chiquet-Ehrismann, R., Anti-adhesive proteins of the extracellular matrix. Curr. Opin. Cell Biol.3 (1991) 800–804.

    Article  CAS  PubMed  Google Scholar 

  15. David, G., Integral membrane heparan sulfate proteoglycans. FASEB J.7 (1993) 1023–1030.

    Article  CAS  PubMed  Google Scholar 

  16. 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.III (1990) 3165–3176.

    Article  Google Scholar 

  17. David, G., van der Schueren, B., Marynen, P., Cassiman, J.-J., and Van Den Berghe, H., Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and gibroblastic cells. J. Cell Biol.118 (1992) 961–969.

    Article  CAS  PubMed  Google Scholar 

  18. David, G., Xiao, M. B., Van der Schueren, B., Marynen P., Cassiman, J.-J., and Van Den Berghe, H., Spatial and temporal changes in the expression of fibroglycan (syndecan-2) during mouse embryonic development. Development119 (1993) 841–854.

    Article  CAS  PubMed  Google Scholar 

  19. Elenius, K., and Jalkanen, M., Function of the syndecans — a family of cell surface proteoglycans. J. Cell Sci.107 (1994) 2975–2982.

    Article  CAS  PubMed  Google Scholar 

  20. Elenius, K., Maatta, A., Salmivirta, M., and Jalkanen, M., Growth factors induce 3T3 cells to express bFGF-binding syndecan. J. biol. Chem.267 (1992) 6435–6441.

    Article  CAS  PubMed  Google Scholar 

  21. Elenius, K., Salmivirta, M., Inki, P., Mali, M., and Jalkanen, M. Binding of human syndecan to extracellular matrix proteins. J. biol. Chem.265 (1990) 17837–17843.

    Article  CAS  PubMed  Google Scholar 

  22. Fritz, T. A., Lugemwa, F. N., Sarkar, A. K., and Esko, J. D., Biosynthesis of heparan sulfate on beta-D-xylosides depends on aglycone structure. J. biol. Chem.269 (1994) 300–307.

    Article  CAS  PubMed  Google Scholar 

  23. Gallagher, J. T., The extended family of proteoglycans: social residents of the pericellular zone. Curr. Opin. Cell Biol.4 (1989) 766–771.

    Google Scholar 

  24. Gallagher, J. T., Turnbull, J. E., and Lyon, M., Patterns of sulphation in heparan sulphate: polymorphism based on a common structural theme. Int. J. Biochem.24 (1992) 553–560.

    Article  CAS  PubMed  Google Scholar 

  25. Gallo, R. L., Siebert, E., and Bernfield, M., Members of the syndecan family of heparan sulfate proteoglycans show distinct expression during mouse development. Molec. Biol. Cell4 (1993) 413a.

    Google Scholar 

  26. Gould, S. E., Upholt, W. B., and Kosher, R. A., Syndecan 3: a member of the syndecan family of membrane-intercalated proteoglycans that is expressed in high amounts at the onset of chicken limb cartilage differentiation. Proc. natl Acad. Sci. USA89 (1992) 3271–3275.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Guimond, S., Maccarana, M., Olwin, B. B., Lindahl, U., and Rapraeger, A. C., Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J. biol. Chem.268 (1993) 23906–23914.

    Article  CAS  PubMed  Google Scholar 

  28. Habuchi, H., Suzuki, S., Saito, T., Tamura, T., Harada, T., Yoshida, K., and Kimata, K., Structure of a heparan sulphate oligosaccharide that binds to basic fibroblast growth factor. Biochem. J.285 (1992) 805–813.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  30. Hayashi, K., Madri, J. A., and Yurchenco, P. D., Endothelial cells interact with the core protein of basement membrane perlecan through beta 1 and beta 3 integrins: an adhesion modulated by glycosaminoglycan. J. Cell Biol.119 (1992) 945–957.

    Article  CAS  PubMed  Google Scholar 

  31. Heine, U., Munoz, E., Flanders, K., Ellingsworth, L., Lam, H., Thompson, N., Roberts, A., and Sporn, M., Role of transforming growth factor-beta in development of the mouse embryo. J. Cell Biol.105 (1989) 2861–2876.

    Article  Google Scholar 

  32. Heino, J., Integrin-type extracellular matrix receptors in cancer and inflammation. Ann. Med.25 (1993) 335–342.

    Article  CAS  PubMed  Google Scholar 

  33. Hynes, R. O., Integrins: versatility, modulation, and signaling in cell adhesion. Cell69 (1992) 11–25.

    Article  CAS  PubMed  Google Scholar 

  34. Iida, J., Skubitz, A. P., Furcht, L. T., Wayner, E. A., and McCarthy, J. B., Coordinate role for cell surface chondroitin sulfate proteoglycan and alpha 4 beta 1 integrin in mediating melenoma cell adhesion to fibronectin. J. Cell Biol.118 (1992) 431–444.

    Article  CAS  PubMed  Google Scholar 

  35. Ishihara, M., Tyrrell, D. J., Stauber, G. B., Brown, S., Cousens, L. S., and Stack, R. J., Preparation of affinity-fractionated, heparin-derived oligosaccharides and their effects on selected biological activities mediated by basic fibroblast growth factor. J. biol. Chem.268 (1993) 4675–4683.

    Article  CAS  PubMed  Google Scholar 

  36. Jackson, R., Bush, S., and Cardin A., Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol. Rev.71 (1991) 481–539.

    Article  CAS  PubMed  Google Scholar 

  37. Jalkanen, M., Elenius, K., and Rapraeger, A., Syndecan: Regulator of cell morphology and growth factor action at the cell-matrix interface. Trends Glycosci. Glycotechnol.5 (1993) 107–120.

    Article  CAS  Google Scholar 

  38. Jalkanen, M., Rapraeger, A., Saunders, S., and Bernfield, M., Cell surface proteoglycan of mammary epithelial cells is shed by cleavage of its matrix-binding ectodomain from its membrane-associated domain. J. Cell Biol.105 (1987) 3087–3096.

    Article  CAS  PubMed  Google Scholar 

  39. Jalkanen, S. and Jalkanen, M., Lymphocyte CD44 binds the COOH-terminal heparin-binding domain of fibronectin. J. Cell Biol.116 (1992) 817–825.

    Article  CAS  PubMed  Google Scholar 

  40. Kan, M., Wang, F., Xu, J., Crabb, J. W., Hou, J., and McKeehan, W. L., An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science259 (1993) 1918–1921.

    Article  CAS  PubMed  Google Scholar 

  41. Keynes, R., and Cook, G., Cell-cell repulsion: Clues from the growth cone? Cell62 (1990) 609–610.

    Article  CAS  PubMed  Google Scholar 

  42. Kiefer, M., Stephens, J., Crawford, K., Okino, K., and Barr, P., Ligand-affinity cloning and structure of a cell surface proteoglycan that binds basic fibroblast growth factor. Proc. natl Acad. Sci. USA87 (1990) 6985–6989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kim, C., Goldberger, O., Gallo, R. L., and Bernfield, M., Individual members of the syndecan family of heparan sulfate proteoglycans show cell- and tissue-specific expression. Mol. Biol. Cell4 (1993) 413a.

    Google Scholar 

  44. Kjellén, L., and Lindahl, U., Proteglycans: Structures and interactions. A. Rev. Biochem.60, (1991) 443–475.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  46. Kojima, T., Shworak, N. W., and Rosenberg, R. D., Molecular cloning and expression of two distinct cDNA-encoding heparan sulfate proteoglycan core proteins from a rat endothelial cell line. J. biol. Chem.267 (1992) 4870–4877.

    Article  CAS  PubMed  Google Scholar 

  47. Kojima, T., Inazawa, J., Takamatsu, J., Rosenberg, J. D., and Saito, H., Human ryudocan core protein: Molecular cloning and characterization of the cDNA, and chromosomal localization of the gene. Biochem. biophys. Res. Commun.190 (1993) 814–822.

    Article  CAS  PubMed  Google Scholar 

  48. Kokenyesi, R., and Bernfield, M., Core protein structure and sequence determine the site and presence of heparan sulfate and chrondroitin sulfate on syndecan-1. J. biol. Chem.269 (1994) 12304–12309.

    Article  CAS  PubMed  Google Scholar 

  49. Leppä, S., Mali, M., Miettinen, H. M., and Jalkanen, M., Syndecan expression regulates cell morphology and growth of mouse mammary epithelial tumor cells. Proc. natl Acad. Sci. USA89 (1992) 932–936.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Lindahl, U., Lidholt, K., Spillmann, D., and Kjellén, L., More to ‘heparin’ than anticoagulation. Thromb. Res.75 (1994) 1–32.

    Article  CAS  PubMed  Google Scholar 

  51. Lyon, M., Deakin, J. A., and Gallagher, J. T., Liver heparan sulfate structure: A novel molecular design. J. biol. Chem.269 (1994) 11208–11215.

    Article  CAS  PubMed  Google Scholar 

  52. Lyon, M., Deakin, J. A., Mizuno, K., Nakamura, T., and Gallagher, J. T., Interaction of hepatocyte growth factor with heparan sulfate: Elucidation of the major heparan sulfate structural determinants. J. biol. Chem.269 (1994) 11216–11223.

    Article  CAS  PubMed  Google Scholar 

  53. Maccarana, M., Casu, B., and Lindahl, U., Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor. J. biol. Chem.268 (1993) 23898–23905.

    Article  CAS  PubMed  Google Scholar 

  54. Maccarana, M., and Lindahl, U., Mode of interaction between platelet factor 4 and heparin. Glycobiology3 (1993) 271–277.

    Article  CAS  PubMed  Google Scholar 

  55. Mach, H., Volkin, D. B., Burke, C. J., Middaugh, C. R., Linhardt, R. J., Fromm, J. R., Loganathan, D., and Mattsson, L., Nature of the interaction of heparin with acidic fibroblast growth factor. Biochemistry32 (1993) 5480–5489.

    Article  CAS  PubMed  Google Scholar 

  56. Mali, M., Andtfolk, H., Miettinen, H., and Jalkanen, M., Suppression of tumor cell growth by syndecan-1 ectodomain. J. biol. Chem.269 (1994) 27795–27798.

    Article  CAS  PubMed  Google Scholar 

  57. Mali, M., Elenius, K., Miettinen, H. M., and Jalkanen, M., Inhibition of basic fibroblast growth factor-induced growth promotion by overexpression of syndecan-1. J. biol. Chem.268 (1993) 24215–24222.

    Article  CAS  PubMed  Google Scholar 

  58. Mali, M., Jaakkola, P., Arvilommi, A.-M., and Jalkanen, M., Sequence of human syndecan indicates a novel gene family of integral membrane proteoglycans. J. biol. Chem.265 (1990) 6884–6889.

    Article  CAS  PubMed  Google Scholar 

  59. Margalit, H., Fischer, N., and Sa, B-S., Comparative analysis of structurally defined heparin binding sequences reveals a distinct spatial distribution of basic residues. J. biol. Chem.268 (1993) 19228–19231.

    Article  CAS  PubMed  Google Scholar 

  60. Maryen, 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  Google Scholar 

  61. Miettinen, H., Edwards, S., and Jalkanen, M., Analysis of transport and targeting of syndecan-1: Effect of cytoplasmic tail deletions. Molec. Biol. Cell5 (1994) 1325–1339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Miettinen, H. M., and Jalkanen, M., The cytoplasmic domain of syndecan-1 is not required for association with the detergent-insoluble cytoskeleton. J. Cell Sci.107 (1994) 1571–1581.

    Article  CAS  PubMed  Google Scholar 

  63. Mina, M., and Kollar, E., The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium. Arch. Oral Biol.32 (1987) 123–127.

    Article  CAS  PubMed  Google Scholar 

  64. Mitsiadis, T., Salmivirta, M., Muramatsu, T., Muramatsu, H., Rauvala, H., Lehtonen, E., Jalkanen, M., and Thesleff, I., Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin), is associated with epithelial mesenchymal interactions during fetal development and organogenesis. Development121 (1995) 37–51.

    Article  CAS  PubMed  Google Scholar 

  65. Nietfeld, J. J., Cytokines and proteoglycans. Experientia49 (1993) 456–469.

    Article  CAS  PubMed  Google Scholar 

  66. Noonan, D., Fulle, A., Valente, P., Cai, S., Horigan, E., Sasaki, M., Yoshihiko, Y., Yamada, Y., and Hassell, R., The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveal extensive similarity with laminin A chain, low density lipoprotein receptor and the neural cell adhesion molecule. J. biol. Chem.266 (1991) 22939–22947.

    Article  CAS  PubMed  Google Scholar 

  67. Nurcombe, V., Ford, M. D., Wildschut, J. A. and Bartlett, P. F., Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science260 (1993) 103–106.

    Article  CAS  PubMed  Google Scholar 

  68. Olwin, B. B., and Rapraeger, A., Repression of myogenic differentiation by aFGF, bFGF, and K-FGF is dependent on cellular heparan sulfate. J. Cell Biol.118 (1992) 631–639.

    Article  CAS  PubMed  Google Scholar 

  69. Parkkinen, J., Raulo, E., Merenmies, J., Nolo, R., Kajander, E. O., Baumann, M., and Rauvala, H., Amphoterin, the 30-kDa protein in a family of HMG1-type polypeptides. Enhanced expression in transformed cells, leading edge localization, and interactions with plasminogen activation. J. biol. Chem.268 (1993) 19726–19738.

    Article  CAS  PubMed  Google Scholar 

  70. Parkkinen, J., and Rauvala, H., Interactions of plasminogen and tissue plasminogen activator (t-PA) with amphoterin. Enhancement of t-PA-catalyzed plasminogen activation by amphoterin. J. biol. Chem.266 (1991) 16730–16735.

    Article  CAS  PubMed  Google Scholar 

  71. 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 

  72. Rapraeger, A., Transforming growth factor (type beta) promotes the addition of chondroitin sulfate to the cell surface proteoglycan (syndecan) of mouse mammary epithelia. J. Cell. Biol.109 (1989) 2509–2518.

    Article  CAS  PubMed  Google Scholar 

  73. Rapraeger, A., Jalkanen, M., and Bernfield, M., Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J. Cell Biol.103 (1986) 2683–2696.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  75. Rapraeger, A. C., Krufka, A., and Olwin, B. B., Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science252 (1991) 1705–1708.

    Article  CAS  PubMed  Google Scholar 

  76. Raulo, E., Chernousov, M. J., Carey, D. J., Nolo, R., and Rauvala, H., Isolation of neuronal cell surface receptor of heparin binding growth-associated molecule (HB-GAM). Identifications as N-syndecan (syndecan-3). J. biol. Chem.269 (1994) 12999–13004.

    Article  CAS  PubMed  Google Scholar 

  77. Raulo, E., Julkunen, I., Merenmies, J., Pihlaskari, R., and Rauvala, H., Secretion and biological activities of heparinbinding growth-associated molecule. Neurite outgrowth-promoting and mitogenic actions of the recombinant and tissue-derived protein. J. biol. Chem.267 (1992) 11408–11416.

    Article  CAS  PubMed  Google Scholar 

  78. Rauvala, H., An 18-kd heparin-binding protein of developing brain that is distinct from fibroblast growth factors. EMBO J.8 (1989) 2933–2941.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Sage, H., and Bornstein, P., Extracellular proteins that modulate cell-matrix interactions. J. biol. Chem.266 (1991) 14831–14834.

    Article  CAS  PubMed  Google Scholar 

  80. Salmivirta, M. Elenius, K., Vainio, S., Hofer, U., Chiquet-Ehrismann, R., Thesleff, I., and Jalkanen, M., Syndecan from embryonic tooth mesenchyme binds tenascin. J. biol. Chem.266 (1991) 7733–7739.

    Article  CAS  PubMed  Google Scholar 

  81. Salmivirta, M., Heino, J., and Jalkanen, M., Basic fibroblast growth factor-syndecan complex at cell surface or immobilized to matrix promotes cell growth. J. biol. Chem.267 (1992) 17606–17610.

    Article  CAS  PubMed  Google Scholar 

  82. Salmivirta, M., Mali, M., Heino, J., Hermonen, J., and Jalkanen, M., A novel laminin-binding form of syndecan-1 (cell surface proteoglycan) produced by syndecan-1 cDNA-transfected NIH-3T3 cells. Expl Cell Res.215 (1994) 180–188.

    Article  CAS  Google Scholar 

  83. Salmivirta, M., Rauvala, H., Elenius, K., and Jalkanen, M., Neurite growth-promoting protein (amphoterin, p30) binds syndecan. Expl Cell Res.200 (1992) 444–451.

    Article  CAS  Google Scholar 

  84. San Antonio, J. D., Karnovsky, M. J., Gay, S., Sanderson, R. D., and Lander, A. D., Interactions of syndecan-1 and heparin with human collagens. Glycobiology4 (1994) 327–332.

    Article  Google Scholar 

  85. San Antonio, J. D., Slover, J., Lawler, J., Karnovsky, M. J., and Lander, A. D., Specificyty in the interactions of extracellular matrix proteins with subpopulations of the glycosaminoglycan heparin. Biochemistry32 (1993) 4746–4755.

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Sanderson, R., Sneed, T., Young, L., Sullivan, G., and Lander, A., Adhesion of B lymphoid (MPC-11) cells to type I collagen is mediated by the integral membrane proteoglycan, syndecan. J. Immun.148 (1992) 3902–3911.

    Article  CAS  PubMed  Google Scholar 

  88. Sanderson, R. D., Turnbull, J. E., Gallagher, J. T., and Lander, A. D., Fine structure of heparan sulfate regulates syndecan-1 function and cell behavior. J. biol. Chem.269 (1994) 13100–13106.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  90. Saunders, S., Jalkanen, M., O'Farrell, S., and Bernfield, M., Molecular cloning of syndecan, and integral membrane proteoglycan. J. Cell Biol.108 (1989) 1547–1556.

    Article  CAS  PubMed  Google Scholar 

  91. Sneed, T., Stanley, D., Young, L., and Sanderson, R., Interleukin-6 regulates expression of the syndecan-1 proteoglycan on B lymphoid cells. Cells. Immun.153 (1994) 456–467.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  93. Spring, J., Paine-Saunders, S., Hynes, R., and Bernlfield, M., Drosophila syndecan: Conservation of a cell surface heparan sulfate proteoglycan. Proc. natl Acad. Sci. USA91 (1994) 3334–3338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Springer, T. A., The sensation and regulation of interactions with the extracellular environment: The cell biology of lymphocyte adhesion receptors. A. Rev. Cell Biol.6 (1990) 359–402.

    Article  CAS  Google Scholar 

  95. Stamenkovic, I., Aruffo, A., Amiot, M., and Seed, B., The hematopoietic and epithelial forms of CD44 are distinct polypeptides with different adhesion potentials for hyaluronate-bearing cells. EMBO J.10 (1991) 343–348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Stipp, C. S., Litwack, E. D., and Lander, A. D., Cerebroglycan: An integral membrane heparan sulfate proteoglycan that is unique to the developing nervous system are expressed specifically during neuronal differentiation. J. Cell Biol.124 (1994) 149–160.

    Article  CAS  PubMed  Google Scholar 

  97. Sun, X., Mosher, D., and Rapraeger, A., Heparan sulfate-mediated binding of epithelial cell surface proteoglycan to thrombospondin. J. biol. Chem.264 (1989) 2885–2889.

    Article  CAS  PubMed  Google Scholar 

  98. Sutherland, A. E., Sanderson, R. D., Mayes, M., Seibert, M., Calarco, P. G., Bernfield, M., and Damsky, C. H., Expression of syndecan, a putative low affinity fiboblast growth factor receptor, in the early mouse embryo. Development113 (1991) 339–351.

    Article  CAS  PubMed  Google Scholar 

  99. Teyton, L., and Peterson, P. A., Assembly and transport of MHC class II molecules. New Biol.4 (1992) 441–447.

    CAS  PubMed  Google Scholar 

  100. Thesleff, I., Jalkanen, M., Vainio, S., and Bernfield, M., Cell surface proteoglycan expression correlates with epithelial-mesenchymal interactions during tooth morphogenesis. Devl Biol.129 (1988) 565–572.

    Article  CAS  Google Scholar 

  101. Thesleff, I., Vainio, S., Salmivirta, M., and Jalkanen, M., Syndecan and tenascin: induction during early tooth morphogenesis and possible interactions. Cell Differ. Dev.32 (1990) 383–389.

    Article  CAS  PubMed  Google Scholar 

  102. Thompson, L. D., Pantoliano, M. W., and Springer, B. A., Energetic characterization of the basic fibroblast growth factor-heparin interaction: Identification of the heparin binding domain. Biochemistry33 (1994) 3831–3840.

    Article  CAS  PubMed  Google Scholar 

  103. Thompson, S. A., Higashiyama, S., Wood, K., Pollitt, N. S., Damm, D., McEnroe, G., Garrick, B., Ashton, N., Lau, K., Hancock, N., Klagsbrun, M., and Abraham, J. A., Characterization of sequences within heparin-binding EGF-like growth factor that mediate interaction with heparin. J. biol. Chem.269 (1994) 2541–2549.

    Article  CAS  PubMed  Google Scholar 

  104. Trautman, M., Kimelman, J., and Bernfield, M., Developmental expression of syndecan, an integral membrane proteoglycan, correlates with cell differentiation. Development111 (1991) 213–220.

    Article  CAS  PubMed  Google Scholar 

  105. Turnbull, J. E., Fernig, D. G., Ke, Y., Wilkinson, M. C., and Gallagher, J. T., Identification of the basic fibroblast growth factor binding sequence in fiboblast heparan sulfate. J. biol. Chem.267 (1992) 10337–10341.

    Article  CAS  PubMed  Google Scholar 

  106. Turnbull, J. E., and Gallagher, J. T., Heparan sulphate: Functional role as a modulator of fibroblast growth factor activity. Biochem. Soc. Trans.21 (1993) 477–482.

    Article  CAS  PubMed  Google Scholar 

  107. Tyrrell, D. J., Ishihara, M., Rao, N., Horne, A., Kiefer, M. C., Stauber, G. B., Lam, L. H., and Stack, R. J., Structure and biological activities of a heparin-derived hexasaccharide with high affinity for basic fibroblast growth factor. J. biol. Chem.268 (1993) 4684–4689.

    Article  CAS  PubMed  Google Scholar 

  108. Underhill, C., CD44: The hyaluronan receptor. J. Cell Sci.103 (1992) 293–298.

    Article  CAS  PubMed  Google Scholar 

  109. Vaahtokari, A., Vainio, S., and Thesleff, I., Associations between transforming growth factor beta-1 mRNA expression and epithelial-mesenchymal interactions during tooth development. Development113 (1991) 985–994.

    Article  CAS  PubMed  Google Scholar 

  110. Vainio, S., Jalkanen, M., Bernfield, M., and Saxen, L., Transient expression of syndecan mesenchymal cell aggregates of the embryonic kidney. Devl Biol.152 (1992) 221–232.

    Article  CAS  Google Scholar 

  111. Vainio, S., Jalkanen, M., and Thesleff, I., Syndecan and tenascin expression is induced by epithelial-mesenchymal interactions in the embryonic tooth mesenchyme. J. Cell Biol.108 (1989) 1945–1954.

    Article  CAS  PubMed  Google Scholar 

  112. Vainio, S., Jalkanen, M., Vaahtokari, A., Sahlberg, C., Mali, M., Bernfield, M., and Thesleff, I., Expression of syndecan gene is induced early, is transient, and correlates with changes in mesenchymal cell proliferation during tooth organogenesis. Devl Biol.147 (1991) 322–333.

    Article  CAS  Google Scholar 

  113. Vainio, S., and Thesleff, I., Coordinated induction of cell proliferation and syndecan expression in dental mesenchyme by epithelium: Evidence for diffusible signals. Dev. Dyn.194 (1992) 105–117.

    Article  CAS  PubMed  Google Scholar 

  114. Walker, A., Turnbull, J. E., and Gallagher, J. T., Specific heparan sulfate saccharides mediate the activity of basic fibroblast growth factor. J. biol. Chem.269 (1994) 931–935.

    Article  CAS  PubMed  Google Scholar 

  115. Wayner, E., and Carter, W., Identification of multiple cell adhesion receptors for collagen and in fibronectin in human fibrosarcoma cells possessing unique alpha and common beta subunits. J. Cell Biol.105 (1987) 1873–1884.

    Article  CAS  PubMed  Google Scholar 

  116. Weitzhandler, M., Streeter, H., Henzel, W., and Bernfield, M., The cell surface proteoglycan of mammary epithelial cells. The extracellular domain contains the N terminus and a peptide sequence present in a conditioned medium proteoglycan. J. biol. Chem.263 (1988) 6949–6952.

    Article  CAS  PubMed  Google Scholar 

  117. Woods, A., and Couchman, J. R., Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Molec. Biol. Cell5 (1994) 183–192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Yayon, A., Klagsbrun, M., Esko, J. D., Leder, P., and Ornitz, D. M., Cell surface, heparan-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 

Download references

Author information

Authors and Affiliations

  1. Turku Centre for Biotechnology, University of Turku and Åbo Akademi University, P.O. Box 123, FIN-20521, Turku, Finland

    M. Salmivirta &  M. Jalkanen

  2. Department of Medical Biochemistry, University of Turku, FIN-20520, Turku, Finland

    M. Salmivirta

  3. Department of Medical and Physiological Chemistry, Uppsala University, S-75123, Uppsala, Sweden

    M. Salmivirta

Authors
  1. M. Salmivirta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Jalkanen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Salmivirta, M., Jalkanen, M. Syndecan family of cell surface proteoglycans: Developmentally regulated receptors for extracellular effector molecules. Experientia 51, 863–872 (1995). https://doi.org/10.1007/BF01921737

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01921737

Key words

Search

Navigation