Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1997 Oct 1;327(Pt 1):1–16. doi: 10.1042/bj3270001

Syndecans: multifunctional cell-surface co-receptors.

D J Carey 1
PMCID: PMC1218755  PMID: 9355727

Abstract

This review will summarize our current state of knowledge of the structure, biochemical properties and functions of syndecans, a family of transmembrane heparan sulphate proteoglycans. Syndecans bind a variety of extracellular ligands via their covalently attached heparan sulphate chains. Syndecans have been proposed to play a role in a variety of cellular functions, including cell proliferation and cell-matrix and cell-cell adhesion. Syndecan expression is highly regulated and is cell-type- and developmental-stage-specific. The main function of syndecans appears to be to modulate the ligand-dependent activation of primary signalling receptors at the cell surface. Principal functions of the syndecan core proteins are to target the heparan sulphate chains to the appropriate plasma-membrane compartment and to interact with components of the actin-based cytoskeleton. Several functions of the syndecans, including syndecan oligomerization and actin cytoskeleton association, have been localized to specific structural domains of syndecan core proteins.

Full Text

The Full Text of this article is available as a PDF (460.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arribas J., Coodly L., Vollmer P., Kishimoto T. K., Rose-John S., Massagué J. Diverse cell surface protein ectodomains are shed by a system sensitive to metalloprotease inhibitors. J Biol Chem. 1996 May 10;271(19):11376–11382. doi: 10.1074/jbc.271.19.11376. [DOI] [PubMed] [Google Scholar]
  2. Ashikari S., Habuchi H., Kimata K. Characterization of heparan sulfate oligosaccharides that bind to hepatocyte growth factor. J Biol Chem. 1995 Dec 8;270(49):29586–29593. doi: 10.1074/jbc.270.49.29586. [DOI] [PubMed] [Google Scholar]
  3. Asundi V. K., Carey D. J. Self-association of N-syndecan (syndecan-3) core protein is mediated by a novel structural motif in the transmembrane domain and ectodomain flanking region. J Biol Chem. 1995 Nov 3;270(44):26404–26410. doi: 10.1074/jbc.270.44.26404. [DOI] [PubMed] [Google Scholar]
  4. Asundi V. K., Keister B. F., Stahl R. C., Carey D. J. Developmental and cell-type-specific expression of cell surface heparan sulfate proteoglycans in the rat heart. Exp Cell Res. 1997 Jan 10;230(1):145–153. doi: 10.1006/excr.1996.3400. [DOI] [PubMed] [Google Scholar]
  5. Aviezer D., Hecht D., Safran M., Eisinger M., David G., Yayon A. Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell. 1994 Dec 16;79(6):1005–1013. doi: 10.1016/0092-8674(94)90031-0. [DOI] [PubMed] [Google Scholar]
  6. Aviezer D., Levy E., Safran M., Svahn C., Buddecke E., Schmidt A., David G., Vlodavsky I., Yayon A. Differential structural requirements of heparin and heparan sulfate proteoglycans that promote binding of basic fibroblast growth factor to its receptor. J Biol Chem. 1994 Jan 7;269(1):114–121. [PubMed] [Google Scholar]
  7. Baciu P. C., Goetinck P. F. Protein kinase C regulates the recruitment of syndecan-4 into focal contacts. Mol Biol Cell. 1995 Nov;6(11):1503–1513. doi: 10.1091/mbc.6.11.1503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Baciu P. C., Goetinck P. F. Protein kinase C regulates the recruitment of syndecan-4 into focal contacts. Mol Biol Cell. 1995 Nov;6(11):1503–1513. doi: 10.1091/mbc.6.11.1503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bernfield M., Hooper K. C. Possible regulation of FGF activity by syndecan, an integral membrane heparan sulfate proteoglycan. Ann N Y Acad Sci. 1991;638:182–194. doi: 10.1111/j.1749-6632.1991.tb49029.x. [DOI] [PubMed] [Google Scholar]
  10. Bernfield M., Kokenyesi R., Kato M., Hinkes M. T., Spring J., Gallo R. L., Lose E. J. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol. 1992;8:365–393. doi: 10.1146/annurev.cb.08.110192.002053. [DOI] [PubMed] [Google Scholar]
  11. Berryman D. E., Bensadoun A. Heparan sulfate proteoglycans are primarily responsible for the maintenance of enzyme activity, binding, and degradation of lipoprotein lipase in Chinese hamster ovary cells. J Biol Chem. 1995 Oct 13;270(41):24525–24531. doi: 10.1074/jbc.270.41.24525. [DOI] [PubMed] [Google Scholar]
  12. Boutin E. L., Sanderson R. D., Bernfield M., Cunha G. R. Epithelial-mesenchymal interactions in uterus and vagina alter the expression of the cell surface proteoglycan, syndecan. Dev Biol. 1991 Nov;148(1):63–74. doi: 10.1016/0012-1606(91)90317-v. [DOI] [PubMed] [Google Scholar]
  13. Brickman Y. G., Ford M. D., Small D. H., Bartlett P. F., Nurcombe V. Heparan sulfates mediate the binding of basic fibroblast growth factor to a specific receptor on neural precursor cells. J Biol Chem. 1995 Oct 20;270(42):24941–24948. doi: 10.1074/jbc.270.42.24941. [DOI] [PubMed] [Google Scholar]
  14. Brieher W. M., Yap A. S., Gumbiner B. M. Lateral dimerization is required for the homophilic binding activity of C-cadherin. J Cell Biol. 1996 Oct;135(2):487–496. doi: 10.1083/jcb.135.2.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Burridge K., Fath K., Kelly T., Nuckolls G., Turner C. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu Rev Cell Biol. 1988;4:487–525. doi: 10.1146/annurev.cb.04.110188.002415. [DOI] [PubMed] [Google Scholar]
  16. Carey D. J., Bendt K. M., Stahl R. C. The cytoplasmic domain of syndecan-1 is required for cytoskeleton association but not detergent insolubility. Identification of essential cytoplasmic domain residues. J Biol Chem. 1996 Jun 21;271(25):15253–15260. doi: 10.1074/jbc.271.25.15253. [DOI] [PubMed] [Google Scholar]
  17. Carey D. J., Conner K., Asundi V. K., O'Mahony D. J., Stahl R. C., Showalter L., Cizmeci-Smith G., Hartman J., Rothblum L. I. cDNA cloning, genomic organization, and in vivo expression of rat N-syndecan. J Biol Chem. 1997 Jan 31;272(5):2873–2879. doi: 10.1074/jbc.272.5.2873. [DOI] [PubMed] [Google Scholar]
  18. Carey D. J., Evans D. M., Stahl R. C., Asundi V. K., Conner K. J., Garbes P., Cizmeci-Smith G. Molecular cloning and characterization of N-syndecan, a novel transmembrane heparan sulfate proteoglycan. J Cell Biol. 1992 Apr;117(1):191–201. doi: 10.1083/jcb.117.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Carey D. J., Stahl R. C., Cizmeci-Smith G., 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. 1994 Jan;124(1-2):161–170. doi: 10.1083/jcb.124.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Carey D. J., Stahl R. C., Tucker B., Bendt K. A., Cizmeci-Smith G. Aggregation-induced association of syndecan-1 with microfilaments mediated by the cytoplasmic domain. Exp Cell Res. 1994 Sep;214(1):12–21. doi: 10.1006/excr.1994.1228. [DOI] [PubMed] [Google Scholar]
  21. Chacko G. W., Duchemin A. M., Coggeshall K. M., Osborne J. M., Brandt J. T., Anderson C. L. Clustering of the platelet Fc gamma receptor induces noncovalent association with the tyrosine kinase p72syk. J Biol Chem. 1994 Dec 23;269(51):32435–32440. [PubMed] [Google Scholar]
  22. Chen H., Strickland D. K., Mosher D. F. Metabolism of thrombospondin 2. Binding and degradation by 3t3 cells and glycosaminoglycan-variant Chinese hamster ovary cells. J Biol Chem. 1996 Jul 5;271(27):15993–15999. doi: 10.1074/jbc.271.27.15993. [DOI] [PubMed] [Google Scholar]
  23. Chernousov M. A., Carey D. J. N-syndecan (syndecan 3) from neonatal rat brain binds basic fibroblast growth factor. J Biol Chem. 1993 Aug 5;268(22):16810–16814. [PubMed] [Google Scholar]
  24. Cizmeci-Smith G., Asundi V., Stahl R. C., Teichman L. J., Chernousov M., Cowan K., Carey D. J. Regulated expression of syndecan in vascular smooth muscle cells and cloning of rat syndecan core protein cDNA. J Biol Chem. 1992 Aug 5;267(22):15729–15736. [PubMed] [Google Scholar]
  25. Cizmeci-Smith G., Langan E., Youkey J., Showalter L. J., Carey D. J. Syndecan-4 is a primary-response gene induced by basic fibroblast growth factor and arterial injury in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 1997 Jan;17(1):172–180. doi: 10.1161/01.atv.17.1.172. [DOI] [PubMed] [Google Scholar]
  26. Cizmeci-Smith G., Stahl R. C., Showalter L. J., Carey D. J. Differential expression of transmembrane proteoglycans in vascular smooth muscle cells. J Biol Chem. 1993 Sep 5;268(25):18740–18747. [PubMed] [Google Scholar]
  27. David G., van der Schueren B., Marynen P., Cassiman J. J., van den Berghe H. Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and fibroblastic cells. J Cell Biol. 1992 Aug;118(4):961–969. doi: 10.1083/jcb.118.4.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. DeLisser H. M., Yan H. C., Newman P. J., Muller W. A., Buck C. A., Albelda S. M. Platelet/endothelial cell adhesion molecule-1 (CD31)-mediated cellular aggregation involves cell surface glycosaminoglycans. J Biol Chem. 1993 Jul 25;268(21):16037–16046. [PubMed] [Google Scholar]
  29. Diamond M. S., Alon R., Parkos C. A., Quinn M. T., Springer T. A. Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD1). J Cell Biol. 1995 Sep;130(6):1473–1482. doi: 10.1083/jcb.130.6.1473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Elenius K., Mättä A., Salmivirta M., Jalkanen M. Growth factors induce 3T3 cells to express bFGF-binding syndecan. J Biol Chem. 1992 Mar 25;267(9):6435–6441. [PubMed] [Google Scholar]
  31. Elenius K., Salmivirta M., Inki P., Mali M., Jalkanen M. Binding of human syndecan to extracellular matrix proteins. J Biol Chem. 1990 Oct 15;265(29):17837–17843. [PubMed] [Google Scholar]
  32. Elenius K., Vainio S., Laato M., Salmivirta M., Thesleff I., Jalkanen M. Induced expression of syndecan in healing wounds. J Cell Biol. 1991 Aug;114(3):585–595. doi: 10.1083/jcb.114.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Faham S., Hileman R. E., Fromm J. R., Linhardt R. J., Rees D. C. Heparin structure and interactions with basic fibroblast growth factor. Science. 1996 Feb 23;271(5252):1116–1120. doi: 10.1126/science.271.5252.1116. [DOI] [PubMed] [Google Scholar]
  34. Fannon M., Nugent M. A. Basic fibroblast growth factor binds its receptors, is internalized, and stimulates DNA synthesis in Balb/c3T3 cells in the absence of heparan sulfate. J Biol Chem. 1996 Jul 26;271(30):17949–17956. doi: 10.1074/jbc.271.30.17949. [DOI] [PubMed] [Google Scholar]
  35. Feyzi E., Lustig F., Fager G., Spillmann D., Lindahl U., Salmivirta M. Characterization of heparin and heparan sulfate domains binding to the long splice variant of platelet-derived growth factor A chain. J Biol Chem. 1997 Feb 28;272(9):5518–5524. doi: 10.1074/jbc.272.9.5518. [DOI] [PubMed] [Google Scholar]
  36. Gallo R. L., Ono M., Povsic T., Page C., Eriksson E., Klagsbrun M., Bernfield M. Syndecans, cell surface heparan sulfate proteoglycans, are induced by a proline-rich antimicrobial peptide from wounds. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):11035–11039. doi: 10.1073/pnas.91.23.11035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Gallo R., Kim C., Kokenyesi R., Adzick N. S., Bernfield M. Syndecans-1 and -4 are induced during wound repair of neonatal but not fetal skin. J Invest Dermatol. 1996 Nov;107(5):676–683. doi: 10.1111/1523-1747.ep12365571. [DOI] [PubMed] [Google Scholar]
  38. Gitay-Goren H., Soker S., Vlodavsky I., Neufeld G. The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules. J Biol Chem. 1992 Mar 25;267(9):6093–6098. [PubMed] [Google Scholar]
  39. Giuffrè L., Cordey A. S., Monai N., Tardy Y., Schapira M., Spertini O. Monocyte adhesion to activated aortic endothelium: role of L-selectin and heparan sulfate proteoglycans. J Cell Biol. 1997 Feb 24;136(4):945–956. doi: 10.1083/jcb.136.4.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Gould S. E., Upholt W. B., Kosher R. A. Characterization of chicken syndecan-3 as a heparan sulfate proteoglycan and its expression during embryogenesis. Dev Biol. 1995 Apr;168(2):438–451. doi: 10.1006/dbio.1995.1093. [DOI] [PubMed] [Google Scholar]
  41. Gould S. E., Upholt W. B., 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 U S A. 1992 Apr 15;89(8):3271–3275. doi: 10.1073/pnas.89.8.3271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Hayashi K., Hayashi M., Jalkanen M., Firestone J. H., Trelstad R. L., Bernfield M. Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissues. A light and electron microscopic study. J Histochem Cytochem. 1987 Oct;35(10):1079–1088. doi: 10.1177/35.10.2957423. [DOI] [PubMed] [Google Scholar]
  43. Heldin C. H. Dimerization of cell surface receptors in signal transduction. Cell. 1995 Jan 27;80(2):213–223. doi: 10.1016/0092-8674(95)90404-2. [DOI] [PubMed] [Google Scholar]
  44. Higashiyama S., Abraham J. A., Klagsbrun M. Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulfate. J Cell Biol. 1993 Aug;122(4):933–940. doi: 10.1083/jcb.122.4.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Hinkes M. T., Goldberger O. A., Neumann P. E., Kokenyesi R., Bernfield M. Organization and promoter activity of the mouse syndecan-1 gene. J Biol Chem. 1993 May 25;268(15):11440–11448. [PubMed] [Google Scholar]
  46. Hirano S., Kimoto N., Shimoyama Y., Hirohashi S., Takeichi M. Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization. Cell. 1992 Jul 24;70(2):293–301. doi: 10.1016/0092-8674(92)90103-j. [DOI] [PubMed] [Google Scholar]
  47. Horwitz A., Duggan K., Buck C., Beckerle M. C., Burridge K. Interaction of plasma membrane fibronectin receptor with talin--a transmembrane linkage. Nature. 1986 Apr 10;320(6062):531–533. doi: 10.1038/320531a0. [DOI] [PubMed] [Google Scholar]
  48. Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
  49. Hynes R. O., Lander A. D. Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell. 1992 Jan 24;68(2):303–322. doi: 10.1016/0092-8674(92)90472-o. [DOI] [PubMed] [Google Scholar]
  50. Inki P., Joensuu H., Grénman R., Klemi P., Jalkanen M. Association between syndecan-1 expression and clinical outcome in squamous cell carcinoma of the head and neck. Br J Cancer. 1994 Aug;70(2):319–323. doi: 10.1038/bjc.1994.300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Jalkanen M., Rapraeger A., Saunders S., Bernfield M. Cell surface proteoglycan of mouse mammary epithelial cells is shed by cleavage of its matrix-binding ectodomain from its membrane-associated domain. J Cell Biol. 1987 Dec;105(6 Pt 2):3087–3096. doi: 10.1083/jcb.105.6.3087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Johnson G. R., Wong L. Heparan sulfate is essential to amphiregulin-induced mitogenic signaling by the epidermal growth factor receptor. J Biol Chem. 1994 Oct 28;269(43):27149–27154. [PubMed] [Google Scholar]
  53. Juliano R. L., Haskill S. Signal transduction from the extracellular matrix. J Cell Biol. 1993 Feb;120(3):577–585. doi: 10.1083/jcb.120.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Kainulainen V., Nelimarkka L., Järveläinen H., Laato M., Jalkanen M., Elenius K. Suppression of syndecan-1 expression in endothelial cells by tumor necrosis factor-alpha. J Biol Chem. 1996 Aug 2;271(31):18759–18766. doi: 10.1074/jbc.271.31.18759. [DOI] [PubMed] [Google Scholar]
  55. Kan M., Wang F., To B., Gabriel J. L., McKeehan W. L. Divalent cations and heparin/heparan sulfate cooperate to control assembly and activity of the fibroblast growth factor receptor complex. J Biol Chem. 1996 Oct 18;271(42):26143–26148. doi: 10.1074/jbc.271.42.26143. [DOI] [PubMed] [Google Scholar]
  56. Kan M., Wang F., Xu J., Crabb J. W., Hou J., McKeehan W. L. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science. 1993 Mar 26;259(5103):1918–1921. doi: 10.1126/science.8456318. [DOI] [PubMed] [Google Scholar]
  57. Kato M., Saunders S., Nguyen H., Bernfield M. Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells. Mol Biol Cell. 1995 May;6(5):559–576. doi: 10.1091/mbc.6.5.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Kato M., Wang H., Bernfield M., Gallagher J. T., Turnbull J. E. Cell surface syndecan-1 on distinct cell types differs in fine structure and ligand binding of its heparan sulfate chains. J Biol Chem. 1994 Jul 22;269(29):18881–18890. [PubMed] [Google Scholar]
  59. Kiefer M. C., Stephans J. C., Crawford K., Okino K., Barr P. J. Ligand-affinity cloning and structure of a cell surface heparan sulfate proteoglycan that binds basic fibroblast growth factor. Proc Natl Acad Sci U S A. 1990 Sep;87(18):6985–6989. doi: 10.1073/pnas.87.18.6985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Kim C. W., Goldberger O. A., Gallo R. L., Bernfield M. Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. Mol Biol Cell. 1994 Jul;5(7):797–805. doi: 10.1091/mbc.5.7.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Kinnunen T., Raulo E., Nolo R., Maccarana M., Lindahl U., Rauvala H. Neurite outgrowth in brain neurons induced by heparin-binding growth-associated molecule (HB-GAM) depends on the specific interaction of HB-GAM with heparan sulfate at the cell surface. J Biol Chem. 1996 Jan 26;271(4):2243–2248. doi: 10.1074/jbc.271.4.2243. [DOI] [PubMed] [Google Scholar]
  62. Kirjavainen J., Leppä S., Hynes N. E., Jalkanen M. Translational suppression of syndecan-1 expression in Ha-ras transformed mouse mammary epithelial cells. Mol Biol Cell. 1993 Aug;4(8):849–858. doi: 10.1091/mbc.4.8.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Koda J. E., Rapraeger A., Bernfield M. Heparan sulfate proteoglycans from mouse mammary epithelial cells. Cell surface proteoglycan as a receptor for interstitial collagens. J Biol Chem. 1985 Jul 5;260(13):8157–8162. [PubMed] [Google Scholar]
  64. Kojima T., Katsumi A., Yamazaki T., Muramatsu T., Nagasaka T., Ohsumi K., Saito H. Human ryudocan from endothelium-like cells binds basic fibroblast growth factor, midkine, and tissue factor pathway inhibitor. J Biol Chem. 1996 Mar 8;271(10):5914–5920. doi: 10.1074/jbc.271.10.5914. [DOI] [PubMed] [Google Scholar]
  65. Kojima T., Leone C. W., Marchildon G. A., Marcum J. A., Rosenberg R. D. Isolation and characterization of heparan sulfate proteoglycans produced by cloned rat microvascular endothelial cells. J Biol Chem. 1992 Mar 5;267(7):4859–4869. [PubMed] [Google Scholar]
  66. Kojima T., Shworak N. W., 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. 1992 Mar 5;267(7):4870–4877. [PubMed] [Google Scholar]
  67. Kokenyesi R., Bernfield M. Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1. J Biol Chem. 1994 Apr 22;269(16):12304–12309. [PubMed] [Google Scholar]
  68. LeBaron R. G., Esko J. D., Woods A., Johansson S., Hök M. Adhesion of glycosaminoglycan-deficient chinese hamster ovary cell mutants to fibronectin substrata. J Cell Biol. 1988 Mar;106(3):945–952. doi: 10.1083/jcb.106.3.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Leppä S., Mali M., Miettinen H. M., Jalkanen M. Syndecan expression regulates cell morphology and growth of mouse mammary epithelial tumor cells. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):932–936. doi: 10.1073/pnas.89.3.932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Letourneur F., Klausner R. D. Activation of T cells by a tyrosine kinase activation domain in the cytoplasmic tail of CD3 epsilon. Science. 1992 Jan 3;255(5040):79–82. doi: 10.1126/science.1532456. [DOI] [PubMed] [Google Scholar]
  71. Liebersbach B. F., Sanderson R. D. Expression of syndecan-1 inhibits cell invasion into type I collagen. J Biol Chem. 1994 Aug 5;269(31):20013–20019. [PubMed] [Google Scholar]
  72. Lyon M., Deakin J. A., Gallagher J. T. Liver heparan sulfate structure. A novel molecular design. J Biol Chem. 1994 Apr 15;269(15):11208–11215. [PubMed] [Google Scholar]
  73. Lyon M., Deakin J. A., Mizuno K., Nakamura T., Gallagher J. T. Interaction of hepatocyte growth factor with heparan sulfate. Elucidation of the major heparan sulfate structural determinants. J Biol Chem. 1994 Apr 15;269(15):11216–11223. [PubMed] [Google Scholar]
  74. Maccarana M., Casu B., Lindahl U. Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor. J Biol Chem. 1993 Nov 15;268(32):23898–23905. [PubMed] [Google Scholar]
  75. Mali M., Andtfolk H., Miettinen H. M., Jalkanen M. Suppression of tumor cell growth by syndecan-1 ectodomain. J Biol Chem. 1994 Nov 11;269(45):27795–27798. [PubMed] [Google Scholar]
  76. Mali M., Elenius K., Miettinen H. M., Jalkanen M. Inhibition of basic fibroblast growth factor-induced growth promotion by overexpression of syndecan-1. J Biol Chem. 1993 Nov 15;268(32):24215–24222. [PubMed] [Google Scholar]
  77. Mali M., Elenius K., Miettinen H. M., Jalkanen M. Inhibition of basic fibroblast growth factor-induced growth promotion by overexpression of syndecan-1. J Biol Chem. 1993 Nov 15;268(32):24215–24222. [PubMed] [Google Scholar]
  78. Mali M., Jaakkola P., Arvilommi A. M., Jalkanen M. Sequence of human syndecan indicates a novel gene family of integral membrane proteoglycans. J Biol Chem. 1990 Apr 25;265(12):6884–6889. [PubMed] [Google Scholar]
  79. Marynen P., Zhang J., Cassiman J. J., Van den Berghe H., David G. Partial primary structure of the 48- and 90-kilodalton core proteins of cell surface-associated heparan sulfate proteoglycans of lung fibroblasts. Prediction of an integral membrane domain and evidence for multiple distinct core proteins at the cell surface of human lung fibroblasts. J Biol Chem. 1989 Apr 25;264(12):7017–7024. [PubMed] [Google Scholar]
  80. Miettinen H. M., Edwards S. N., Jalkanen M. Analysis of transport and targeting of syndecan-1: effect of cytoplasmic tail deletions. Mol Biol Cell. 1994 Dec;5(12):1325–1339. doi: 10.1091/mbc.5.12.1325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Miettinen H. M., Jalkanen M. The cytoplasmic domain of syndecan-1 is not required for association with Triton X-100-insoluble material. J Cell Sci. 1994 Jun;107(Pt 6):1571–1581. doi: 10.1242/jcs.107.6.1571. [DOI] [PubMed] [Google Scholar]
  82. Misra K. B., Kim K. C., Cho S., Low M. G., Bensadoun A. Purification and characterization of adipocyte heparan sulfate proteoglycans with affinity for lipoprotein lipase. J Biol Chem. 1994 Sep 23;269(38):23838–23844. [PubMed] [Google Scholar]
  83. Mitsiadis T. A., Muramatsu T., Muramatsu H., Thesleff I. Midkine (MK), a heparin-binding growth/differentiation factor, is regulated by retinoic acid and epithelial-mesenchymal interactions in the developing mouse tooth, and affects cell proliferation and morphogenesis. J Cell Biol. 1995 Apr;129(1):267–281. doi: 10.1083/jcb.129.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Miyamoto S., Akiyama S. K., Yamada K. M. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science. 1995 Feb 10;267(5199):883–885. doi: 10.1126/science.7846531. [DOI] [PubMed] [Google Scholar]
  85. Miyamoto S., Teramoto H., Coso O. A., Gutkind J. S., Burbelo P. D., Akiyama S. K., Yamada K. M. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol. 1995 Nov;131(3):791–805. doi: 10.1083/jcb.131.3.791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Norgard-Sumnicht K. E., Varki N. M., Varki A. Calcium-dependent heparin-like ligands for L-selectin in nonlymphoid endothelial cells. Science. 1993 Jul 23;261(5120):480–483. doi: 10.1126/science.7687382. [DOI] [PubMed] [Google Scholar]
  87. Nugent M. A., Edelman E. R. Kinetics of basic fibroblast growth factor binding to its receptor and heparan sulfate proteoglycan: a mechanism for cooperactivity. Biochemistry. 1992 Sep 22;31(37):8876–8883. doi: 10.1021/bi00152a026. [DOI] [PubMed] [Google Scholar]
  88. Nurcombe V., Ford M. D., Wildschut J. A., Bartlett P. F. Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science. 1993 Apr 2;260(5104):103–106. doi: 10.1126/science.7682010. [DOI] [PubMed] [Google Scholar]
  89. Oh E. S., Woods A., Couchman J. R. Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J Biol Chem. 1997 Mar 28;272(13):8133–8136. doi: 10.1074/jbc.272.13.8133. [DOI] [PubMed] [Google Scholar]
  90. Ornitz D. M., Yayon A., Flanagan J. G., Svahn C. M., Levi E., Leder P. Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol Cell Biol. 1992 Jan;12(1):240–247. doi: 10.1128/mcb.12.1.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Otey C. A., Pavalko F. M., Burridge K. An interaction between alpha-actinin and the beta 1 integrin subunit in vitro. J Cell Biol. 1990 Aug;111(2):721–729. doi: 10.1083/jcb.111.2.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Palecek S. P., Loftus J. C., Ginsberg M. H., Lauffenburger D. A., Horwitz A. F. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature. 1997 Feb 6;385(6616):537–540. doi: 10.1038/385537a0. [DOI] [PubMed] [Google Scholar]
  93. Parthasarathy N., Goldberg I. J., Sivaram P., Mulloy B., Flory D. M., Wagner W. D. Oligosaccharide sequences of endothelial cell surface heparan sulfate proteoglycan with affinity for lipoprotein lipase. J Biol Chem. 1994 Sep 2;269(35):22391–22396. [PubMed] [Google Scholar]
  94. Pavalko F. M., Walker D. M., Graham L., Goheen M., Doerschuk C. M., Kansas G. S. The cytoplasmic domain of L-selectin interacts with cytoskeletal proteins via alpha-actinin: receptor positioning in microvilli does not require interaction with alpha-actinin. J Cell Biol. 1995 May;129(4):1155–1164. doi: 10.1083/jcb.129.4.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Pierce A., Lyon M., Hampson I. N., Cowling G. J., Gallagher J. T. Molecular cloning of the major cell surface heparan sulfate proteoglycan from rat liver. J Biol Chem. 1992 Feb 25;267(6):3894–3900. [PubMed] [Google Scholar]
  96. Rapraeger A. C., Krufka A., Olwin B. B. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science. 1991 Jun 21;252(5013):1705–1708. doi: 10.1126/science.1646484. [DOI] [PubMed] [Google Scholar]
  97. Rapraeger A., Jalkanen M., Bernfield M. Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J Cell Biol. 1986 Dec;103(6 Pt 2):2683–2696. doi: 10.1083/jcb.103.6.2683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Rapraeger A., Jalkanen M., Endo E., Koda J., Bernfield M. The cell surface proteoglycan from mouse mammary epithelial cells bears chondroitin sulfate and heparan sulfate glycosaminoglycans. J Biol Chem. 1985 Sep 15;260(20):11046–11052. [PubMed] [Google Scholar]
  99. Raulo E., Chernousov M. A., Carey D. J., Nolo R., Rauvala H. Isolation of a neuronal cell surface receptor of heparin binding growth-associated molecule (HB-GAM). Identification as N-syndecan (syndecan-3). J Biol Chem. 1994 Apr 29;269(17):12999–13004. [PubMed] [Google Scholar]
  100. Raulo E., Julkunen I., Merenmies J., Pihlaskari R., Rauvala H. Secretion and biological activities of heparin-binding growth-associated molecule. Neurite outgrowth-promoting and mitogenic actions of the recombinant and tissue-derived protein. J Biol Chem. 1992 Jun 5;267(16):11408–11416. [PubMed] [Google Scholar]
  101. Rauvala H., Vanhala A., Castrén E., Nolo R., Raulo E., Merenmies J., Panula P. Expression of HB-GAM (heparin-binding growth-associated molecules) in the pathways of developing axonal processes in vivo and neurite outgrowth in vitro induced by HB-GAM. Brain Res Dev Brain Res. 1994 Jun 17;79(2):157–176. doi: 10.1016/0165-3806(94)90121-x. [DOI] [PubMed] [Google Scholar]
  102. Reich-Slotky R., Bonneh-Barkay D., Shaoul E., Bluma B., Svahn C. M., Ron D. Differential effect of cell-associated heparan sulfates on the binding of keratinocyte growth factor (KGF) and acidic fibroblast growth factor to the KGF receptor. J Biol Chem. 1994 Dec 23;269(51):32279–32285. [PubMed] [Google Scholar]
  103. Reichsman F., Smith L., Cumberledge S. Glycosaminoglycans can modulate extracellular localization of the wingless protein and promote signal transduction. J Cell Biol. 1996 Nov;135(3):819–827. doi: 10.1083/jcb.135.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Reiland J., Rapraeger A. C. Heparan sulfate proteoglycan and FGF receptor target basic FGF to different intracellular destinations. J Cell Sci. 1993 Aug;105(Pt 4):1085–1093. doi: 10.1242/jcs.105.4.1085. [DOI] [PubMed] [Google Scholar]
  105. Reyes A. A., Akeson R., Brezina L., Cole G. J. Structural requirements for neural cell adhesion molecule-heparin interaction. Cell Regul. 1990 Jul;1(8):567–576. doi: 10.1091/mbc.1.8.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Roghani M., Mansukhani A., Dell'Era P., Bellosta P., Basilico C., Rifkin D. B., Moscatelli D. Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding. J Biol Chem. 1994 Feb 11;269(6):3976–3984. [PubMed] [Google Scholar]
  107. Roghani M., Moscatelli D. Basic fibroblast growth factor is internalized through both receptor-mediated and heparan sulfate-mediated mechanisms. J Biol Chem. 1992 Nov 5;267(31):22156–22162. [PubMed] [Google Scholar]
  108. Rosenblum N. D., Botelho B. B., Bernfield M. Expression of a Xenopus counterpart of mammalian syndecan 2 during embryogenesis. Biochem J. 1995 Jul 1;309(Pt 1):69–76. doi: 10.1042/bj3090069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Salmivirta M., Elenius K., Vainio S., Hofer U., Chiquet-Ehrismann R., Thesleff I., Jalkanen M. Syndecan from embryonic tooth mesenchyme binds tenascin. J Biol Chem. 1991 Apr 25;266(12):7733–7739. [PubMed] [Google Scholar]
  110. Salmivirta M., Heino J., Jalkanen M. Basic fibroblast growth factor-syndecan complex at cell surface or immobilized to matrix promotes cell growth. J Biol Chem. 1992 Sep 5;267(25):17606–17610. [PubMed] [Google Scholar]
  111. Salmivirta M., Mali M., Heino J., Hermonen J., Jalkanen M. A novel laminin-binding form of syndecan-1 (cell surface proteoglycan) produced by syndecan-1 cDNA-transfected NIH-3T3 cells. Exp Cell Res. 1994 Nov;215(1):180–188. doi: 10.1006/excr.1994.1330. [DOI] [PubMed] [Google Scholar]
  112. San Antonio J. D., Karnovsky M. J., Gay S., Sanderson R. D., Lander A. D. Interactions of syndecan-1 and heparin with human collagens. Glycobiology. 1994 Jun;4(3):327–332. doi: 10.1093/glycob/4.3.327. [DOI] [PubMed] [Google Scholar]
  113. Sanderson R. D., Bernfield M. Molecular polymorphism of a cell surface proteoglycan: distinct structures on simple and stratified epithelia. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9562–9566. doi: 10.1073/pnas.85.24.9562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Sanderson R. D., Lalor P., Bernfield M. B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul. 1989 Nov;1(1):27–35. doi: 10.1091/mbc.1.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Sanderson R. D., Sneed T. B., Young L. A., Sullivan G. L., Lander A. D. Adhesion of B lymphoid (MPC-11) cells to type I collagen is mediated by integral membrane proteoglycan, syndecan. J Immunol. 1992 Jun 15;148(12):3902–3911. [PubMed] [Google Scholar]
  116. Sanderson R. D., Turnbull J. E., Gallagher J. T., Lander A. D. Fine structure of heparan sulfate regulates syndecan-1 function and cell behavior. J Biol Chem. 1994 May 6;269(18):13100–13106. [PubMed] [Google Scholar]
  117. Saunders S., Bernfield M. Cell surface proteoglycan binds mouse mammary epithelial cells to fibronectin and behaves as a receptor for interstitial matrix. J Cell Biol. 1988 Feb;106(2):423–430. doi: 10.1083/jcb.106.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Saunders S., Jalkanen M., O'Farrell S., Bernfield M. Molecular cloning of syndecan, an integral membrane proteoglycan. J Cell Biol. 1989 Apr;108(4):1547–1556. doi: 10.1083/jcb.108.4.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Schwall R. H., Chang L. Y., Godowski P. J., Kahn D. W., Hillan K. J., Bauer K. D., Zioncheck T. F. Heparin induces dimerization and confers proliferative activity onto the hepatocyte growth factor antagonists NK1 and NK2. J Cell Biol. 1996 May;133(3):709–718. doi: 10.1083/jcb.133.3.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Shieh M. T., WuDunn D., Montgomery R. I., Esko J. D., Spear P. G. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J Cell Biol. 1992 Mar;116(5):1273–1281. doi: 10.1083/jcb.116.5.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Shimazu A., Nah H. D., Kirsch T., Koyama E., Leatherman J. L., Golden E. B., Kosher R. A., Pacifici M. Syndecan-3 and the control of chondrocyte proliferation during endochondral ossification. Exp Cell Res. 1996 Nov 25;229(1):126–136. doi: 10.1006/excr.1996.0350. [DOI] [PubMed] [Google Scholar]
  122. Shishido Y., Sharma K. D., Higashiyama S., Klagsbrun M., Mekada E. Heparin-like molecules on the cell surface potentiate binding of diphtheria toxin to the diphtheria toxin receptor/membrane-anchored heparin-binding epidermal growth factor-like growth factor. J Biol Chem. 1995 Dec 8;270(49):29578–29585. doi: 10.1074/jbc.270.49.29578. [DOI] [PubMed] [Google Scholar]
  123. Shworak N. W., Shirakawa M., Colliec-Jouault S., Liu J., Mulligan R. C., Birinyi L. K., Rosenberg R. D. Pathway-specific regulation of the synthesis of anticoagulantly active heparan sulfate. J Biol Chem. 1994 Oct 7;269(40):24941–24952. [PubMed] [Google Scholar]
  124. Shworak N. W., Shirakawa M., Mulligan R. C., Rosenberg R. D. Characterization of ryudocan glycosaminoglycan acceptor sites. J Biol Chem. 1994 Aug 19;269(33):21204–21214. [PubMed] [Google Scholar]
  125. Shyng S. L., Lehmann S., Moulder K. L., Harris D. A. Sulfated glycans stimulate endocytosis of the cellular isoform of the prion protein, PrPC, in cultured cells. J Biol Chem. 1995 Dec 15;270(50):30221–30229. doi: 10.1074/jbc.270.50.30221. [DOI] [PubMed] [Google Scholar]
  126. Sleeman J., Rudy W., Hofmann M., Moll J., Herrlich P., Ponta H. Regulated clustering of variant CD44 proteins increases their hyaluronate binding capacity. J Cell Biol. 1996 Nov;135(4):1139–1150. doi: 10.1083/jcb.135.4.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Solursh M., Reiter R. S., Jensen K. L., Kato M., Bernfield M. Transient expression of a cell surface heparan sulfate proteoglycan (syndecan) during limb development. Dev Biol. 1990 Jul;140(1):83–92. doi: 10.1016/0012-1606(90)90055-n. [DOI] [PubMed] [Google Scholar]
  128. Spivak-Kroizman T., Lemmon M. A., Dikic I., Ladbury J. E., Pinchasi D., Huang J., Jaye M., Crumley G., Schlessinger J., Lax I. Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell. 1994 Dec 16;79(6):1015–1024. doi: 10.1016/0092-8674(94)90032-9. [DOI] [PubMed] [Google Scholar]
  129. Spring J., Goldberger O. A., Jenkins N. A., Gilbert D. J., Copeland N. G., Bernfield M. Mapping of the syndecan genes in the mouse: linkage with members of the myc gene family. Genomics. 1994 Jun;21(3):597–601. doi: 10.1006/geno.1994.1319. [DOI] [PubMed] [Google Scholar]
  130. Spring J., Paine-Saunders S. E., Hynes R. O., Bernfield M. Drosophila syndecan: conservation of a cell-surface heparan sulfate proteoglycan. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3334–3338. doi: 10.1073/pnas.91.8.3334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Springer T. A. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu Rev Physiol. 1995;57:827–872. doi: 10.1146/annurev.ph.57.030195.004143. [DOI] [PubMed] [Google Scholar]
  132. Stanley M. J., Liebersbach B. F., Liu W., Anhalt D. J., Sanderson R. D. Heparan sulfate-mediated cell aggregation. Syndecans-1 and -4 mediate intercellular adhesion following their transfection into human B lymphoid cells. J Biol Chem. 1995 Mar 10;270(10):5077–5083. doi: 10.1074/jbc.270.10.5077. [DOI] [PubMed] [Google Scholar]
  133. Steinfeld R., Van Den Berghe H., David G. Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J Cell Biol. 1996 Apr;133(2):405–416. doi: 10.1083/jcb.133.2.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Sternberg M. J., Gullick W. J. A sequence motif in the transmembrane region of growth factor receptors with tyrosine kinase activity mediates dimerization. Protein Eng. 1990 Mar;3(4):245–248. doi: 10.1093/protein/3.4.245. [DOI] [PubMed] [Google Scholar]
  135. Sudhalter J., Whitehouse L., Rusche J. R., Marchionni M. A., Mahanthappa N. K. Schwann cell heparan sulfate proteoglycans play a critical role in glial growth factor/neuregulin signaling. Glia. 1996 May;17(1):28–38. doi: 10.1002/(SICI)1098-1136(199605)17:1<28::AID-GLIA3>3.0.CO;2-3. [DOI] [PubMed] [Google Scholar]
  136. Sun X., Mosher D. F., Rapraeger A. Heparan sulfate-mediated binding of epithelial cell surface proteoglycan to thrombospondin. J Biol Chem. 1989 Feb 15;264(5):2885–2889. [PubMed] [Google Scholar]
  137. Turnbull J. E., Fernig D. G., Ke Y., Wilkinson M. C., Gallagher J. T. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J Biol Chem. 1992 May 25;267(15):10337–10341. [PubMed] [Google Scholar]
  138. Turnbull J. E., Gallagher J. T. Distribution of iduronate 2-sulphate residues in heparan sulphate. Evidence for an ordered polymeric structure. Biochem J. 1991 Feb 1;273(Pt 3):553–559. doi: 10.1042/bj2730553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  139. Vainio S., Jalkanen M., Bernfield M., Saxén L. Transient expression of syndecan in mesenchymal cell aggregates of the embryonic kidney. Dev Biol. 1992 Aug;152(2):221–232. doi: 10.1016/0012-1606(92)90130-9. [DOI] [PubMed] [Google Scholar]
  140. Vainio S., Jalkanen M., Thesleff I. Syndecan and tenascin expression is induced by epithelial-mesenchymal interactions in embryonic tooth mesenchyme. J Cell Biol. 1989 May;108(5):1945–1953. doi: 10.1083/jcb.108.5.1945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  141. Vainio S., Jalkanen M., Vaahtokari A., Sahlberg C., Mali M., Bernfield M., Thesleff I. Expression of syndecan gene is induced early, is transient, and correlates with changes in mesenchymal cell proliferation during tooth organogenesis. Dev Biol. 1991 Oct;147(2):322–333. doi: 10.1016/0012-1606(91)90290-j. [DOI] [PubMed] [Google Scholar]
  142. Vihinen T., Auvinen P., Alanen-Kurki L., Jalkanen M. Structural organization and genomic sequence of mouse syndecan-1 gene. J Biol Chem. 1993 Aug 15;268(23):17261–17269. [PubMed] [Google Scholar]
  143. Vihinen T., Mättä A., Jaakkola P., Auvinen P., Jalkanen M. Functional characterization of mouse syndecan-1 promoter. J Biol Chem. 1996 May 24;271(21):12532–12541. doi: 10.1074/jbc.271.21.12532. [DOI] [PubMed] [Google Scholar]
  144. Walker A., Turnbull J. E., Gallagher J. T. Specific heparan sulfate saccharides mediate the activity of basic fibroblast growth factor. J Biol Chem. 1994 Jan 14;269(2):931–935. [PubMed] [Google Scholar]
  145. Wei Z., Swiedler S. J., Ishihara M., Orellana A., Hirschberg C. B. A single protein catalyzes both N-deacetylation and N-sulfation during the biosynthesis of heparan sulfate. Proc Natl Acad Sci U S A. 1993 May 1;90(9):3885–3888. doi: 10.1073/pnas.90.9.3885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Weitzhandler M., Streeter H. B., Henzel W. J., Bernfield M. The cell surface proteoglycan of mouse mammary epithelial cells. The extracellular domain contains N terminus and a peptide sequence present in a conditioned medium proteoglycan. J Biol Chem. 1988 May 25;263(15):6949–6952. [PubMed] [Google Scholar]
  147. Wong J. Y., Kuhl T. L., Israelachvili J. N., Mullah N., Zalipsky S. Direct measurement of a tethered ligand-receptor interaction potential. Science. 1997 Feb 7;275(5301):820–822. doi: 10.1126/science.275.5301.820. [DOI] [PubMed] [Google Scholar]
  148. Woods A., Couchman J. R. Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol Biol Cell. 1994 Feb;5(2):183–192. doi: 10.1091/mbc.5.2.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  149. Woods A., McCarthy J. B., Furcht L. T., Couchman J. R. A synthetic peptide from the COOH-terminal heparin-binding domain of fibronectin promotes focal adhesion formation. Mol Biol Cell. 1993 Jun;4(6):605–613. doi: 10.1091/mbc.4.6.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  150. Yamada K. M., Geiger B. Molecular interactions in cell adhesion complexes. Curr Opin Cell Biol. 1997 Feb;9(1):76–85. doi: 10.1016/s0955-0674(97)80155-x. [DOI] [PubMed] [Google Scholar]
  151. Yayon A., Klagsbrun M., Esko J. D., Leder P., Ornitz D. M. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 1991 Feb 22;64(4):841–848. doi: 10.1016/0092-8674(91)90512-w. [DOI] [PubMed] [Google Scholar]
  152. Yeaman C., Rapraeger A. C. Post-transcriptional regulation of syndecan-1 expression by cAMP in peritoneal macrophages. J Cell Biol. 1993 Aug;122(4):941–950. doi: 10.1083/jcb.122.4.941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  153. Zhang L., David G., Esko J. D. Repetitive Ser-Gly sequences enhance heparan sulfate assembly in proteoglycans. J Biol Chem. 1995 Nov 10;270(45):27127–27135. doi: 10.1074/jbc.270.45.27127. [DOI] [PubMed] [Google Scholar]
  154. Zhang L., Esko J. D. Amino acid determinants that drive heparan sulfate assembly in a proteoglycan. J Biol Chem. 1994 Jul 29;269(30):19295–19299. [PubMed] [Google Scholar]
  155. de Agostini A. I., Watkins S. C., Slayter H. S., Youssoufian H., Rosenberg R. D. Localization of anticoagulantly active heparan sulfate proteoglycans in vascular endothelium: antithrombin binding on cultured endothelial cells and perfused rat aorta. J Cell Biol. 1990 Sep;111(3):1293–1304. doi: 10.1083/jcb.111.3.1293. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES