Syndecans: Proteoglycan regulators of cell-surface microdomains?

Nature Reviews Molecular Cell Biology

Volumn 4, Issue 12, 2003, Pages 926-937

  Couchman, John R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSAMINOGLYCAN; LIGAND; MEMBRANE RECEPTOR; PROTEOGLYCAN; SYNDECAN;

CELL MEMBRANE; CELL SURFACE; CONCENTRATION (PARAMETERS); CYTOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW;

ANIMALS; BODY PATTERNING; CYTOSKELETON; DIMERIZATION; FOCAL ADHESIONS; MEMBRANE GLYCOPROTEINS; MEMBRANE MICRODOMAINS; MODELS, MOLECULAR; MULTIGENE FAMILY; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEOGLYCANS; SYNDECANS; THROMBOSPONDIN 1;

EID: 0345169052     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1257     Document Type: Review

References (111)

1. Selleck, S. B. Proteoglycans and pattern formation. Sugar biochemistry meets developmental genetics. Trends Genet. 16, 206-212 (2000).
2. Perrimon, N. & Bernfield, M. Specificities of heparan sulphate proteoglycans in developmental processes, Nature 404, 725-728 (2000).
3. Park, P. W., Reizes, O. & Bernfield, M. Cell surface heparan sulfate proteoglycans: selective regulators of ligand-receptor encounters. J. Biol. Chem. 275, 29923-29926 (2000).
4. Filmus, J. Glypicans in growth and cancer. Glycobiology 11, 19R-23R (2001).
5. Bernfield, M. et al. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777 (1999).
6. Rapraeger, A. C. Molecular interactions of syndecans during development. Semin. Cell Dev. Biol. 12, 107-116 (2001).
7. Couchman, J. R., Chen, L. & Woods, A. Syndecans and cell adhesion. Int. Rev. Cytol. 207,113-150 (2001).
8. Saunders, S., Jalkanen, M., O'Farrell, S. & Bernfield, M. Molecular cloning of syndecan, an integral membrane proteoglycan. J. Cell Biol. 108, 1547-1556 (1989).
9. Bernfield, M. et al. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8, 365-393 (1992).
10. 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 protecglycan expressed by epithelial and fibroblastic cells. J. Cell Biol. 118, 961-969 (1992).
11. McFall, A. J. & Rapraeger, A. C. Identification of an adhesion site within the syndecan-4 extracellular protein domain. J. Biol. Chem, 272, 12901-12904 (1997).
12. McFall, A. J. & Rapraeger, A. C. Characterization of the high affinity cell-binding domain in the cell surface proteoglycan syndecan-4. J. Biol. Chem. 273, 28270-28276 (1998).
13. Liu, W. et al. Heparan sulfate proteoglycans as adhesive and anti-invasive molecules. Syndecans and glypican have distinct functions. J. Biol. Chem. 273, 22825-22832 (1998).
14. Carey, D. J. Syndecans: multifunctional cell-surface co-receptors. Biochem. J. 327, 1-16 (1997).
15. Oh, E.-S., Woods, A. & Couchman, J. R. Multimerization of the cytoplasmic domain of syndecan-4 is required for its ability to activate protein kinase C. J. Biol. Chem. 272, 11805-11811 (1997).
16. Lee, D., Oh, E.-S., Woods, A., Couchman, J. R. & Lee, W. Solution structure of a syndecan-4 cytoplasmic domain and its interaction with phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 273, 13022-13029 (1998).
17. Shin, J. et al. Solution structure of the dimeric cytoplasmic domain of syndecan-4. Biochemistry 40, 8471-8478 (2001). This and the preceding paper provide the only structural data on a syndecan cytoplasmic domain.
18. Lories, V., Cassiman, J. J., Van den Berghe, H. & David, G. Multiple distinct membrane heparan sulfate proteoglycans in human lung fibroblasts. J. Biol. Chem. 264, 7009-7016 (1989).
19. Baciu, P. C. et al. Syndesmos, a protein that interacts with the cytoplasmic domain of syndecan-4, mediates cell spreading and actin cytoskeletal organization. J. Cell Sci. 113, 315-324 (2000).
20. Filmus, J. & Selleck, S. B. Glypicans: proteoglycans with a surprise. J. Clin. Invest. 108, 497-501 (2001).
21. 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 6, 559-576 (1995).
22. Anttonnen, A., Kajanti, M., Heikkila, R., Jalkanen, M. & Joensuu, H. Syndecan-1 expression has prognostic significance in head and neck carcinoma. Br. J. Cancer 79, 558-564 (1999).
23. Rintala, M., Inki, P., Klemi, P., Jalkanen, M. & Grenman, S. Association of syndecan-1 with tumor grade and histology in primary invasive cervical carcinoma. Gynecol. Oncol. 75, 372-378 (1999).
24. Leppa, S., Vleminckx, K., Van Roy, F. & Jafkanen, M. Syndecan-1 expression in mammary epithelial tumor cells is E-cadherin-dependent. J. Cell Sci. 109, 1393-1403 (1996).
25. Berx, G. & Van Roy, F. The E-cadhedn/catenin complex: an important gatekeeper in breast cancer tumorigenesis and malignant progression, Breast Cancer Res. 3, 289-293 (2001).
26. 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. 214, 12-21 (1994).
27. Miettinen, H. & Jalkanen, M. The cytoplasmic domain of syndecan-1 is not required for association with Triton-X-100-insoluble material. J. Cell Sci. 107, 1571-1581 (1994).
28. Kinnunen, T. et al. Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J. Biol. Chem. 273, 10702-10708 (1998).
29. Adams, J. C., Kureishy, N. & Taylor, A. L. A role for syndecan-1 in coupling fascin spike formation by thrombospondin-1. J. Cell Biol. 152, 1169-1182 (2001). A specific system for analysing the signalling pathway from syndecan 1 to the actin cytoskeleton and the role of GTPases.
30. Dhodapkar, M. V. & Sanderson, R. D. Syndecan-1 (CD138) in myeloma and lymphoid malignancies: a multifunctional regulator of cell behavior within the tumor microenvironment. Leuk. Lymphoma 34, 35-43 (1999).
31. Dhodapkar, M. V. et al. Elevated levels of shed syndecan-1 correlate with tumour mass and decreased matrix metalloproteinase-9 activity in the serum of patients with multiple myeloma. Br. J. Haematol 99, 368-371 (1997).
32. Yang, Y., Borset, M., Langford, J. K. & Sanderson, R. D. Heparan sulfate regulates targeting of syndecan-1 to a functional domain on the cell surface. J. Biol. Chem, 278, 12888-12893 (2003).
33. Kainulainen, V., Wang, H., Schick, C. & Bernfield, M. Syndecans, heparan sulfate proteoglycans, maintain the proteolytic balance of acute wound fluid. J. Biol. Chem. 273, 11563-11569 (1998).
34. Fitzgerald, M. L., Wang, Z., Park, P. W., Murphy, G. & Bernfield, M. Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J. Cell Biol. 148, 811-824 (2000).
35. Dhodapkar, M. V. et al. Syndecan-1 is a multifunctional regulator of myeloma pathobiology: control of tumor cell survival, growth, and bone cell differentiation. Blood 91, 2679-2688 (1998).
36. Kato, M. et al. Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nature Med. 4, 691-697 (1998).
37. Li, Q., Park, P. W., Wilson, C. L. & Parks, W. C. Matrilysin shedding of syndecan-1 regulates chemokines mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111, 635-646 (2002). Elegant demonstration of how syndecan that Is shed from the cell surface is functional in localizing an inflammatory response.
38. Ethell, I. M. & Yamaguchi, Y. Cell surface heparan sulfate proteoglycan syndecan-2 induces the maturation of dendritic spines in rat hippocampal neurons. J. Cell Biol. 144, 575-586 (1999).
39. Ethell, I. M. et al. EphB/syndecan-2 signaling in dendritic spine morphogenesis, Neuron 31, 1001-1013 (2001). Lateral association of syndecan 2 with the Eph receptor tyrosine kinase provides a basis for syndecan phosphorylation and clustering associated with dendritic maturation.
40. Ethell, I. M., Hagihara, K., Miura, Y., Irie, F. & Yamaguchi, Y. Synbindin, a novel syndecan-2-binding protein in neuronal dendritic spines. J. Cell Biol. 151, 53-67 (2000).
41. Cohen, A. R. et al. Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J. Cell Biol. 142, 120-138 (1998).
42. Hsueh, Y.-P. & Sheng, M. Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/UN-2 during rat brain development. J. Neurosci. 19, 7415-7425 (1999).
43. Ire, F. & Yamaguchi, Y. EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP Nature Neurosci. 5, 1117-1118 (2002).
44. Klass, C. M., Couchman, J. R. & Woods, A. Control of extracellular matrix assembly by syndecan-2 proteoglycan. J. Cell Sci. 113, 493-506 (2000).
45. Cukierman, E., Pankov, R., Stevens, D. R. & Yamada, K. M. Taking cell-matrix adhesions to the third dimension. Science 294, 1661-1663 (2001).
46. Granés, F., Ureña, J. M., Rocamora, N. & Vilaró, S. Ezrin links syndecan-2 to the cytoskeleton. J. Cell Sci. 113, 1267-1276 (2000).
47. Granés, F. et al. Syndecan-2 induces filopodia by active cdc42Hs. Exp. Cell Res. 248, 439-456 (1999).
48. 1: structural characteristics of heparan sulfate chains with avidity to COOH-terminal heparin-binding domain of fibronectin. Exp. Cell Res. 256, 434-444 (2000).
49. Munesue, S. et al. The role of syndecan-2 in regulation of actin-cytoskeletal organization of Lewis lung carcinoma-derived metastatic clones. Biochem. J. 363, 201-209 (2002).
50. Woods, A & Couchman, J. R. Syndecan-4 and focal adhesion function. Curr. Opin. Cell Biol. 13, 578-583 (2001).
51. Kramer, K. L. & Yost, H. J. Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev. Cell 2, 115-124 (2002).
52. Kramer, K. L., Barnette, J. E. & Yost, H. J. PKCγ regulates syndecan-2 inside-out signaling during Xenopus left-right development. Cell 111, 981-990 (2002). References 51 and 52 provide not only evidence for the role of syndecan 2 in early vertebrate development, but also a molecular basis for the signalling process.
53. Tumova, S., Woods, A. & Couchman, J. R. Heparan sulfate chains from glypican and syndecans bind Hep II domain of fibronectin similarly despite minor structural differences, J. Biol. Chem. 275, 9410-9417 (2000).
54. Zako, M. et al. Syndecan-1 and -4 synthesized simultaneously by mouse mammary gland epithelial cells bear heparan sulfate chains that are apparently structurally indistinguishable. J. Biol. Chem. 278, 13561-13569 (2003).
55. Calderwood, D. A. Shattil, S. J. & Ginsberg, M. H. Integrins and actin filaments: reciprocal regulation of cell adhesion and signaling. J. Biol. Chem. 275, 22607-22610 (2000).
56. Oh, E.-S., Couchman, J. R. &Woods, A. Serine phosphorylation of syndecan-2 proteoglycan cytoplasmic domain. Arch. Biochem. Biophys. 344, 67-74 (1997).
57. Woods, A. & Couchman, J. R. Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol. Biol. Cell 5, 183-192 (1994).
58. Baciu, P. C. & Goetinck, P. F. Protein kinase C regulates the recruitment of syndecan-4 into local contacts. Mol. Biol. Cell 6, 1503-1513 (1995).
59. Longley, R. L. et al. Control of morphology, cytoskeleton and migration by syndecan-4. J. Cell Sci. 112, 3421-3431 (1999).
60. Oh, E.-S., Woods, A., Lim, S.-T, Theibert, A. W. & Couchman, J. R. Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol 4,5-bisphosphate coordinately regulate protein kinase C activity. J. Biol. Chem. 273, 10624-10629.
61. Horowitz, A., Murakami, M., Gao, Y. & Simons, M. Phosphatidylinositol-4,5-bisphosphate mediates the interaction of syndecan-4 with protein kinase C. Biochemistry 38, 15871-15877 (1999).
62. Couchman, J. R. et al. Regulation of inositol phospholipid binding and signaling through syndecan-4. J. Biol. Chem. 277, 49296-49303 (2002).
63. Oh, E.-S., Woods, A. & Couchman, J. R. Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J. Biol. Chem. 272, 8133-8136 (1997).
64. Horowitz, A. & Simons, M. Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase Cα. J. Biol. Chem. 273, 25548-25551 (1998).
65. Lim, S.-T., Longley, R. L., Couchman, J. R. & Woods, A. Direct binding of syndecan-4 cytoplasmic domain to the catalyc domain of PKCα increases focal adhesion localization of PKCα. J. Biol. Chem. 278, 13795-13802 (2003). This brings together evidence for a role for syndecan 4 in focal-adhesion formation and the localization of PKCα.
66. Corbalán-García, S., García-García, J., Rodriguez-Alfaro, J. A. & Gómez-Fernández, J. C. A new phosphatidylinositol 4,5-bisphoshate-binding site located in the C2 domain of protein kinase Cα. J. Biol. Chem. 278, 4972-4980 (2003).
67. Woods, A. & Couchman, J. R. Integrin modulation by lateral association. J. Biol. Chem. 275, 24233-24236 (2000).
68. Bass, M. D., & Humphries, M. J. Cytoplasmic interactions of Syndecan-4 orchestrate adhesion receptor and growth factor receptor signalling. Biochem. J. 368, 1-15 (2002).
69. Bhatt, A., Kaverina, I., Otey, C. & Huttenlocher, A. Regulation of focal complex composition and disassembly by the calcium-dependent calpain. J. Cell Sci. 115, 3415-3425 (2002).
70. Horowitz, A. & Simons, M. Regulation of syndecan-4 phosphorylation in vivo. J. Biol. Chem. 273, 10914-10918 (1998).
71. Murakami, M., Horowitz, A., Tang, S., Ware, J. A. & Simons, M. Protein kinase C (PKC)5 regulates PKCA activity in a syndecan-4-dependent manner. J. Biol. Chem. 277, 20367-20371 (2002).
72. Denhez, F. et al. Syndesmos, a syndecan-4 cytoplasmic domain interactor, binds to the focal adhesion adaptor proteins paxillin and Hic-5. J. Biol. Chem. 277, 12270-12274 (2002).
73. Greene, D. K., Tumova, S., Couchman, J. R. & Woods, A. Syndecan-4 associates with α-actinin. J. Biol. Chem. 278, 7617-7623 (2003).
74. Critchley, D. R. Focal adhesions - the cytoskeletal connection. Curr. Opin. Cell Biol. 12, 133-139 (2000).
75. Saoncella, S. et al. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc. Natl Acad. Sci. USA 96, 2805-2810 (1999).
76. Bishop, A. & Hall, A. Rho GTPases and their effector proteins. Biochem. J. 348, 241-255 (2000).
77. Slater, S. J., Seiz, J. L., Stagliano, B. A. & Stubbs, C. D. Interaction of protein kinase C isozymes with Rho GTPases. Biochemistry 40, 4437-4445 (2001).
78. Defilippi, P. et al. Dissection of pathways implicated in integrin-mediated actin cytosketeton assembly. Involvement of protein kinase C, Rho GTPase, and tyrosine phosphorylation. J. Biol. Chem. 272, 21726-21734 (1997).
79. Thodeti, C. K. et al. ADAM12/syndcan-4 signaling promotes β1 integrin-dependent cell spreading through PKCα and Rho A. J. Biol. Chem. 278, 9576-9584 (2003).
80. Fukata, Y., Amano, M. & Kaibuchi, K. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci. 22, 32-39 (2001).
81. Watanabe, N. et al. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16, 30440-3056 (1997).
82. Stanley, M. J., Liebersbach, B. F., Liu, W., Anhalt, D. J. & Sanderson, R. D. Heparan sulfate-mediated eel aggregation. Syndecans-1 and-4 mediate intercelluIar adhesion following their transfection into human B lymphoid cells. J. Biol. Chem. 270, 5077-5083 (1995).
83. Fuki I. V. et al. The syndecan family of proteoglycans. Novel receptors mediating internalization of atherogenic lipoproteins in vitro. J. Clin. Invest. 100, 1611-1622 (1997).
84. Fuki, I. V., Meyer, M. E. & Williams, K. J. Transmembrane and cytoplasmic domains of syndecan mediate a multi-step endocytic pathway involving detergent-insoluble membrane rafts. Biochem. J. 351, 607-612 (2000). The importance of syndecan clustering and translocation to a membrane domain following ligand binding is illustrated.
85. Tkachenko, E. & Simons, M. Clustering induces redistribution of syndecan-4 core protein into raft membrane domains, J. Biol. Chem. 277, 19946-19951 (2002).
86. Grootjans, J. J. et al. Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl Acad. Sci. USA 94, 13683-13688 (1997).
87. Gao, Y., Li, M., Chen, W. & Simons, M. Synectin, syndecan-4 cytoplasmic domain binding PDZ protein, inhibits cell migration. J. Cell Physiol. 184, 373-379 (2000).
88. Hung, A. Y. & Sheng, M. PDZ domains: structural modules for protein complex assembly. J. Biol. Chem. 277, 5699-5702 (2002).
89. Zimmermann, P. et al. Characterization of syntenin, a syndecan-binding PDZ protein, as a component of cell adhesion sites and microfilaments. Mol. Biol. Cell 13, 339-350 (2001).
90. Fialka, I. et al. Identification of syntenin as a protein of the apical early endocytic compartment in Madin-Darby canine kidney cells. J. Biol. Chem. 274, 26233-26239 (1999).
91. Lin, D., Gish, G. D., Songyang, Z. & Pawson, T. The carboxyl terminus of B class ephrins constitutes a PDZ domain binding motif. J. Biol. Chem. 274, 3726-3733 (1999).
92. 6 subunits. Matrix Biol. 21, 207-214 (2002).
93. Stepp, M. A. et al. Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J. Cell Sci. 115, 4517-4531 (2002).
94. Götte, M. et al. Role of syndecan-1 in leukocyte-endothelial interactions in the ocular vasculature. Invest. Ophthalmol. Vis. Sci. 34, 1135-1141 (2002).
95. Alexander, C. M., Hinkes, M. T. & Bernfield, M. Syndecan-1 is required for Wnt-1-induced tumorigenesis but not for morphogenesis of mouse mammary epithelia. Nature Genet. 25, 329-332 (2000).
96. Stanley, M. J., Stanley, M. W., Sanderson, R. D. & Zera, R. Syndecan-1 expression is induced in the stroma of infiltrating breast carcinoma. Am. J. Clin. Pathol 112, 377-383 (1999).
97. Echtermeyer, F. et al. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J. Clin. Invest. 107, R9-R14 (2001).
98. Ishiguro, K. et al. Syndecan-4 deficiency impairs focal adhesion formation only under restricted conditions. J. Biol. Chem. 275, 5249-5252 (2000).
99. Ishiguro, K. et al. Syndecan-4 deficiency leads to high mortality of lipopolysaccharide-injected mice. J. Biol. Chem. 276, 47483-47488 (2001).
100. Ishiguro, K. et al. Syndecan-4 deficiency increases susceptibility to κ-carrageenan-induced renal damage. Lab. Invest. 81,509-516 (2001).
101. Yung, S. et al. Syndecan-4 up-regulation in proliferative renal disease is related to microfilament organization. FASEB J. 15, 1631-1633 (2001).
102. Zhang, Y., Pasparakis, M., Kollias, G. & Simons, M. Myocyte-dependent regulation of endothelial cell syndecan-4 expression. Role of TNF-α. J. Biol. Chem, 274, 14786-14796 (1999).
103. 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. 17, 172-180 (1997).
104. Lindahl, U., Kusche-Gullberg, M. & Kiellén, L. Regulated diversity of heparan sulfate. J. Biol. Chem. 273, 24979-24982 (1998).
105. Esko, J. D. & Undahl, U. Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169-173 (2001).
106. Esko, J. D. & Selleck, S. B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev Biochem. 71, 435-471 (2002).
107. Van Kuppevelt, T. H., Dennissen, M. A., van Venrooij, W. J. Hoet, R. M. & Veerkamp, J. H. Generation and application of type-specific anti-heparan sulfate antibodies using phage display technology. Further evidence for heparan sulfate heterogeneity in the kidney. J. Biol. Chem. 278, 12960-12966 (1998).
108. Gallagher, J. T. Heparan sulfate: growth control with a restricted sequence menu. J. Clin. Invest. 108, 357-361 (2001).
109. Lander, A. D. Proteoglycans: master regulators of molecular encounter? Matrix Biol. 17, 465-472 (1998).
110. Fanning, A. S. & Anderson, J. M. PDZ domains: fundamental building blocks in the organization of protein complexes at the plasma membrane. J. Clin. Invest. 103, 767-772 (1999).
111. 2-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol. Cell 9, 1215-1225 (2002).