Syndecans play dual roles as cell adhesion receptors and docking receptors

FEBS Letters

Volumn 586, Issue 16, 2012, Pages 2207-2211

  Kwon, Mi Jung ^a   Jang, Bohee ^a   Yi, Jae Youn ^b   Han, Inn Oc ^c   Oh, Eok Soo ^a  

^a Ewha Womans University   (South Korea)

^b Korea Atomic Energy Research Institute   (South Korea)

^c Inha University School of Medicine   (South Korea)

Author keywords

Adhesion receptor; Cell adhesion; Docking receptor; Extracellular matrix; Signal transduction; Syndecan

Indexed keywords

CELL ADHESION RECEPTOR; CELL SURFACE RECEPTOR; CYTOKINE; DOCKING RECEPTOR; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE A; INTEGRIN; MATRILYSIN; PROTEIN TYROSINE KINASE; RECEPTOR; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SYNDECAN; SYNDECAN 1; SYNDECAN 2; UNCLASSIFIED DRUG; VASCULOTROPIN 165; VASCULOTROPIN RECEPTOR 2;

CELL ADHESION; CELL COMMUNICATION; CELL FUNCTION; ENZYME REGULATION; EXTRACELLULAR MATRIX; HUMAN; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION; CELL COMMUNICATION; CELL MEMBRANE; GENE EXPRESSION REGULATION; HUMANS; LIGANDS; MEMBRANE GLYCOPROTEINS; MODELS, BIOLOGICAL; PROTEOGLYCANS; RECEPTORS, CELL SURFACE; SYNDECANS;

EID: 84864277708     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.05.037     Document Type: Review

References (61)

1. E. Tkachenko, J.M. Rhodes, and M. Simons Syndecans: new kids on the signaling block Circ. Res. 96 2005 488 500 (Pubitemid 40463457)
2. K. Lambaerts, S.A. Wilcox-Adelman, and P. Zimmermann The signaling mechanisms of syndecan heparan sulfate proteoglycans Curr. Opin. Cell Biol. 21 2009 662 669
3. A.C. Rapraeger Syndecan-regulated receptor signaling J. Cell. Biol. 149 2000 995 998
4. M.R. Morgan, M.J. Humphries, and M.D. Bass Synergistic control of cell adhesion by integrins and syndecans Nat. Rev. Mol. Cell. Biol. 8 2007 957 969 (Pubitemid 350174639)
5. Y. Choi, H. Chung, H. Jung, J.R. Couchman, and E.S. Oh Syndecans as cell surface receptors: unique structure equates with functional diversity Matrix. Biol. 30 2011 93 99
6. A. Woods, R.L. Longley, S. Tumova, and J.R. Couchman Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts Arch. Biochem. Biophys. 374 2000 66 72 (Pubitemid 30084409)
7. Y. Mahalingam, J.T. Gallagher, and J.R. Couchman Cellular adhesion responses to the heparin-binding (HepII) domain of fibronectin require heparan sulfate with specific properties J. Biol. Chem. 282 2007 3221 3230 (Pubitemid 47084330)
8. S.T. Lim, R.L. Longley, J.R. Couchman, and A. Woods Direct binding of syndecan-4 cytoplasmic domain to the catalytic domain of protein kinase Cα (PKCα) increases focal adhesion localization of PKCα J. Biol. Chem. 278 2003 13795 13802 (Pubitemid 36799917)
9. C.M. Mahoney, M.R. Morgan, A. Harrison, M.J. Humphries, and M.D. Bass Therapeutic ultrasound bypasses canonical syndecan-4 signaling to activate rac1 J. Biol. Chem. 284 2009 8898 8909
10. M.J. Humphries, Z. Mostafavi-Pour, M.R. Morgan, N.O. Deakin, A.J. Massent, and M.D. Bass Integrin-syndecan cooperation governs the assembly of signaling complexes during cell spreading Novartis. Found. Symp. 269 2005 178 188
11. M.D. Bass, K.A. Roach, M.R. Morgan, Z. Mostafavi-Pour, T. Schoen, T. Muramatsu, U. Mayer, C. Ballestrem, J.P. Spatz, and M.J. Humphries Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix J. Cell Biol. 177 2007 527 538 (Pubitemid 46718280)
12. J. Yoo, M.J. Jeong, H.J. Cho, E.S. Oh, and M.Y. Han Dynamin II interacts with syndecan-4, a regulator of focal adhesion and stress-fiber formation Biochem. Biophys. Res. Commun. 328 2005 424 431 (Pubitemid 40208328)
13. H. Park, I. Han, H.J. Kwon, and E.S. Oh Focal adhesion kinase regulates syndecan-2-mediated tumorigenic activity of HT-1080 fibrosarcoma cells Cancer. Res. 65 2005 9899 9905 (Pubitemid 41541470)
14. S. Carulli, K. Beck, G. Dayan, S. Boulesteix, H. Lortat-Jacob, and P. Rousselle Cell surface proteoglycans syndecan-1 and -4 bind overlapping but distinct sites in laminin α3 LG45 protein domain J. Biol. Chem. 287 2012 12204 12216
15. J. Kim, J.H. Lee, H.S. Park, J. Hwang, I.O. Han, Y.S. Bae, and E.S. Oh Syndecan-4 regulates platelet-derived growth factor-mediated MAP kinase activation by altering intracellular reactive oxygen species FEBS. Lett. 582 2008 2725 2730
16. M. Sundaresan, Z.X. Yu, V.J. Ferrans, D.J. Sulciner, J.S. Gutkind, K. Irani, P.J. Goldschmidt-clermont, and T. Finkel Regulation of reactive-oxigen-species generation in fibroblasts by Rac1 Biochem. J. 318 1996 379 382 (Pubitemid 26305933)
17. 1: structural characteristics of heparan sulfate chains with avidity to COOH-terminal heparin-binding domain of fibronectin Exp. Cell. Res. 256 2000 434 444 (Pubitemid 30244202)
18. S. Munesue, Y. Kusano, K. Oguri, N. Itano, Y. Yoshitomi, H. Nakanishi, I. Yamashina, and M. Okayama The role of syndecan-2 in regulation of actin-cytoskeletal organization of Lewis lung carcinoma-derived metastatic clones Biochem. J. 363 2002 201 209 (Pubitemid 34415756)
19. 2 Biochem. Biophys. Res. Commun. 384 2009 231 235
20. Y.L. Lin, Y.T. Lei, C.J. Hong, and Y.P. Hsueh Syndecan-2 induced filopodia and dendritic spine formation viz the neurofibromin-PKA-Ena/VASP pathway J. Cell. Biol. 177 2007 829 841
21. E. Chen, S. Hermanson, and S.C. Ekker Syndecan-2 is essential for angiogenic sprouting during zebrafish development Blood 103 2004 1710 1719 (Pubitemid 38268963)
22. 3 integrin activity in human mammary carcinoma cells J. Cell. Biol. 167 2004 171 181 (Pubitemid 39363424)
23. 5 integrin activity in B82L fibroblasts J. Cell. Sci. 119 2006 2445 2456 (Pubitemid 44070426)
24. 4 chain Mol. Biol. Cell. 18 2007 1621 1633 (Pubitemid 46717545)
25. 5 integrin activation during angiogenesis and is blocked by synstatin, a novel peptide inhibitor J. Exp. Med. 206 2009 691 705
26. K. Vuoriluoto, J. Jokinen, K. Kallio, M. Salmivirta, J. Heino, and J. Ivaska Syndecan-1 supports integrin alpha2beta1-mediated adhesion to collagen Exp. Cell. Res. 314 2008 3369 3381
27. T. Ishikawa, and R.H. Kramer Sdc1 negatively modulated carcinoma cell motility and invasion Exp. Cell. Res. 316 2010 951 965
28. H. Wang, L. Leavitt, R. Ramaswamy, and A.C. Rapraeger Interaction of syndecan and alpha6beta4 integrin cytoplasmic domains: regulation of ErbB2-mediated integrin activation J. Biol. Chem. 285 2010 13569 13579
29. Q. Yu, and I. Stamenkovic Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion Genes Dev. 13 1999 35 48 (Pubitemid 29045114)
30. D.M. Beauvais, and A.C. Rapraeger Syndecan-1 couples the insulin-like growth factor-1 receptor to inside-out integrin activation J. Cell. Sci. 123 2010 3796 3807
31. H.Y. Ryu, J. Lee, S. Yang, H. Park, S. Choi, K.C. Jung, S.T. Lee, J.K. Seong, I.O. Han, and E.S. Oh Syndecan-2 functions as a docking receptor for pro-matrix metalloproteinase-7 in human colon cancer cells J. Biol. Chem. 284 2009 35692 35701
32. M. Bernfield, M. Götte, P.W. Park, O. Reizes, M.L. Fitzgerald, J. Lincecum, and M. Zako Functions of cell surface heparan sulfate proteoglycans Annu. Rev. Biochem. 68 1999 729 777 (Pubitemid 29449208)
33. D.J. Carey Syndecans: multifunctional cell-surface co-receptors Biochem. J. 327 1997 1 16 (Pubitemid 27455453)
34. W.H. Burgess, and T. Maciag The heparin-binding (Fibroblast) growth factor family of proteins Annu. Rev. Biochem. 58 1989 575 606 (Pubitemid 19172981)
35. A. Woods, E.S. Oh, and J.R. Couchman Syndecan proteoglycans and cell adhesion Matrix. Biol. 17 1998 477 483 (Pubitemid 28566882)
36. X. Xian, S. Gopal, and J.R. Couchman Syndecans as receptors and organizers of the extracellular matrix Cell. Tissue Res. 339 2010 31 46
37. G. Cizmeci-Smith, E. Langan, J. Youkey, L.J. Showalter, and D.J. Carey 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 1997 172 180 (Pubitemid 27057340)
38. K. Elenius, A. Maatta, M. Salmivirta, and M. Jalkanen Growth factors induce 3T3 cells to express bFGF-binding syndecan J. Biol. Chem. 267 1992 6435 6441
39. G. Cizmeci-Smith, R.C. Stahl, L.J. Showalter, and D.J. Carey Differential expression of transmembrane proteoglycans in vascular smooth muscle cells J. Biol. Chem. 268 1993 18740 18747 (Pubitemid 23273818)
40. R. Steinfeld, H.V.D. Berghe, and G. David Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican J. Cell. Biol. 133 1996 405 416 (Pubitemid 26132538)
41. J. Reiland, and A.C. Rapraeger Heparan sulfate proteoglycan and FGF receptor target basic FGF to different intracellular destinations J. Cell Sci. 105 1993 1085 1093 (Pubitemid 23258670)
42. T. Kajia, C. Yamamotoa, M. Oh-ia, Y. Fujiwaraa, Y. Yamazakic, T. Moritac, A.H. Plaasd, and T.N. Wighte The vascular endothelial growth factor VEGF165 induces perlecan synthesis via VEGF receptor-2 in cultured human brain microvascular endothelial cells Biochim. Biophys. Acta 1760 2006 1465 1474
43. K. Mahtouk, F.W. Cremer, T. Rème, M. Jourdan, M. Baudard, J. Moreaux, G. Requirand, G. Fiol, J. De Vos, M. Moos, P. Quittet, H. Goldschmidt, J.F. Rossi, D. Hose, and B. Klein Heparansulphate proteoglycans are essential for the myeloma cell growth activity of EGF-family ligands in multiple myeloma Oncogene 25 2006 7180 7191 (Pubitemid 44764187)
44. N.F. Andersen, T. Standal, J.L. Nielsen, L. Heickendorff, M. Borset, F.B. Sorensen, and N. Abildgaard Syndecan-1 and angiogenic cytokines in multiple myeloma: correlation with bone marrow angiogenesis and survival Br. J. Haematol. 128 2005 210 217
45. K. Mahtouk, M. Jourdan, J. De Vos, C. Hertogh, G. Fiol, E. Jourdan, J.F. Rossi, and B. Klein An inhibitor of the EGF receptor family blocks myeloma cell growth factor activity of HB-EGF and potentiates dexamethasone or anti-IL-6 antibody-induced apoptosis Blood 103 2004 1829 1837 (Pubitemid 38268980)
46. P.W. Derksen, R.M. Keehnen, L.M. Evers, M.H. van Oers, M. Spaargaren, and S.T. Pals Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma Blood 99 2002 1405 1410 (Pubitemid 34547098)
47. C. Seidel, M. Borset, O. Hjertner, D. Cao, N. Abildgaard, H. Hjorth-Hansen, R.D. Sanderson, A. Waage, and A. Sundan High levels of soluble syndecan-1 in myeloma-derived bone marrow: modulation of hepatocyte growth factor activity Blood 96 2000 3139 3146
48. L.J. Marshall, L.S. Ramdin, T. Brooks, P.C. Dphil, and J.K. Shute Plasminogen activator inhibitor-1 supports IL-8-mediated neutrophil transendothelial migration by inhibition of the constitutive shedding of endothelial IL-8/heparan sulfate/syndecan-1 complexes J. Immunol. 171 2003 2057 2065 (Pubitemid 36966489)
49. Y. Halden, A. Rek, W. Atzenhofer, L. Szilak, A. Wabnig, and A.J. Kungl Interleukin-8 binds to syndecan-2 on human endothelial cells Biochem. J. 377 2004 533 538 (Pubitemid 38142209)
50. A.M. Patterson, L. Gardner, J. Shaw, G. David, E. Loreau, L. Aguilar, B.A. Ashton, and J. Middleton Induction of a CXCL8 binding site on endothelial syndecan-3 in rheumatoid synovium Arthritis Rheum. 52 2005 2331 2342 (Pubitemid 41117417)
51. B. Goger, Y. Halden, A. Rek, R. Mosl, D. Pye, J. Gallagher, and A.J. Kungl Different affinities of glycosaminoglycan oligosaccharides for monomeric and dimeric interleukin-8: a model for chemokine regulation at inflammatory sites Biochemistry 41 2002 1640 1646 (Pubitemid 34112754)
52. D. Modrowski, M. Baslé, A. Lomri, and P.J. Marie Syndecan-2 is involved in the mitogenic activity and signaling of granulocyte-macrophage colony-stimulating factor in osteoblasts J. Biol. Chem. 275 2000 9178 9185 (Pubitemid 30185134)
53. Q. Li, P.W. Park, C.L. Wilson, and W.C. Parks Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury Cell 111 2002 635 646 (Pubitemid 35441246)
54. W.H. Yu, and J.F. Woessner Heparan sulfate proteoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7) J. Biol. Chem. 275 2000 4183 4191
55. Y. Koyama, H. Naruo, Y. Yoshitomi, S. Munesue, S. Kiyono, Y. Kusano, K. Hashimoto, T. Yokoi, H. Nakanishi, S. Shimizu, M. Okayama, and K. Oguri Matrix metalloproteinase-9 associated with heparan sulphate chains of GPI-anchored cell surface proteoglycans mediates motility of murine colon adenocarcinoma cells J. Biochem. 143 2008 581 592 (Pubitemid 351670646)
56. S. Munesue, Y. Yoshitomi, Y. Kusano, Y. Koyama, A. Nishiyama, H. Nakanishi, K. Miyazaki, T. Ishimaru, S. Miyaura, M. Okayama, and K. Oguri A novel function of syndecan-2, suppression of matrix metalloproteinase-2 activation, which causes suppression of metastasis J. Biol. Chem. 282 2007 28164 28174 (Pubitemid 47529519)
57. S. Brule, N. Charnaux, A. Sutton, D. Ledoux, T. Chaigneau, L. Saffar, and L. Gattegno The shedding of syndecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/CXCL12 and mediated by the matrix metalloproteinase-9 Glycobiology 16 2006 488 501 (Pubitemid 43779045)
58. F. De Ceuninck, F. Allain, A. Caliez, G. Spik, and P.M. Vanhoutte High binding capacity of cyclophilin B to chondrocyte heparan sulfate proteoglycans and its release from the cell surface by matrix metalloproteinases: Possible role as a proinflammatory mediator in arthritis Arthritis. Rheum. 48 2003 2197 2206 (Pubitemid 36959200)
59. A. Berton, C. Selvais, P. Lemoine, P. Henriet, P.J. Courtoy, E. Marbaix, and H. Emonard Binding of matrilysin-1 to human epithelial cells promotes its activity Cell. Mol. Life Sci. 64 2007 610 620 (Pubitemid 46712462)
60. 1 integrin activation PLoS. ONE 4 2009 e6565
61. K. Ding, M. Lopez-Burks, J.A. Sánchez-Duran, M. Korc, and A.D. Lander Growth factor-induced shedding of syndecan-1 confers glypican-1 dependence on mitogenic responses of cancer cells J. Cell. Biol. 171 2005 729 738 (Pubitemid 41668731)