Syndecan proteoglycan contributions to cytoskeletal organization and contractility

Scandinavian Journal of Medicine and Science in Sports

Volumn 19, Issue 4, 2009, Pages 479-489

  Okina, E ^a   Manon Jensen, T ^a   Whiteford, J R ^a   Couchman, J R ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Extracellular matrix; Focal adhesion; Heparan sulphate; Integrin; Syndecan

Indexed keywords

ACTIN; PROTEIN KINASE C; PROTEOHEPARAN SULFATE; SYNDECAN 4;

CYTOSKELETON; ENZYMOLOGY; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW;

ACTINS; CYTOSKELETON; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; PROTEIN KINASE C; SYNDECAN-4;

EID: 69149093277     PISSN: 09057188     EISSN: 16000838     Source Type: Journal    
DOI: 10.1111/j.1600-0838.2009.00941.x     Document Type: Review

References (95)

1. Alexander CM, Reichsman F, Hinkes MT, Lincecum J, Becker KA, Cumberledge S, Bernfield M. Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat Genet 2000 : 25 : 329 332.
2. Alexopoulou AN, Multhaupt HA, Couchman JR. Syndecans in wound healing, inflammation and vascular biology. Int J Biochem Cell Biol 2006 : 39 : 505 528.
3. Arnaout MA, Goodman SL, Xiong JP. Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol 2007 : 19 : 495 507.
4. Baciu PC, Saoncella S, Lee SH, Denhez F, Leuthardt D, Goetinck PF. Syndesmos, a protein that interacts with the cytoplasmic domain of syndecan-4, mediates cell spreading and actin cytoskeletal organization. J Cell Sci 2000 : 113 : 315 324.
5. Bass MD, Morgan MR, Roach KA, Settleman J, Goryachev AB, Humphries MJ. p190RhoGAP is the convergence point of adhesion signals from alpha 5 beta 1 integrin and syndecan-4. J Cell Biol 2008 : 181 : 1013 1026.
6. Bass MD, Roach KA, Morgan MR, Mostafavi-Pour Z, Schoen T, Muramatsu T, Mayer U, Ballestrem C, Spatz JP, Humphries MJ. Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J Cell Biol 2007 : 177 : 527 538.
7. Beauvais DM, Burbach BJ, Rapraeger AC. The syndecan-1 ectodomain regulates alpha(v) beta 3 integrin activity in mammalian carcinoma cells. J Cell Biol 2004 : 167 : 171 181.
8. Bellin R, Capila I, Lincecum J, Park PW, Reizes O, Bernfield MR. Unlocking the secrets of syndecans: transgenic organisms as a potential key. Glycoconj J 2002 : 19 : 295 304.
9. Brule S, Charnaux N, Sutton A, Ledoux D, Chaigneau T, Saffar L, Gattegno L. 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 2006 : 16 : 488 450.
10. Carey DJ, Evans DM, Stahl RC, Asundi VK, Conner KJ, Garbes P, Cizmeci-Smith G. Molecular cloning and characterization of N-syndecan, a novel transmembrane heparan sulfate proteoglycan. J Cell Biol 1992 : 117 : 191 201.
11. Chakravarti R, Adams JC. Comparative genomics of the syndecans defines an ancestral genomic context associated with matrilins in vertebrates. BMC Genom 2006 : 7 : 83.
12. Chen E, Hermanson S, Ekker SC. Syndecan-2 is essential for angiogenic sprouting during zebrafish development. Blood 2002 : 103 : 1710 1719.
13. Chen Y, Shi-Wen X, van Beek J, Kennedy L, McLeod M, Renzoni EA, Bou-Gharios G, Wilcox-Adelman S, Goetinck PF, Eastwood M, Black CM, Abraham DJ, Leask A. Matrix contraction by dermal fibroblasts requires transforming growth factor-beta/activin-linked kinase 5, heparan sulfate-containing proteoglycans, and MEK/ERK: insights into pathological scarring in chronic fibrotic disease. Am J Pathol 2005 : 167 : 1699 1711.
14. Choi S, Lee E, Kwon S, Park H, Yi JY, Kim S, Han IO, Yun Y, Oh ES. Transmembrane domain-induced oligomerization is crucial for the functions of syndecan-2 and syndecan-4. J Biol Chem 2005 : 280 : 42573 42579.
15. Clark EA, King WG, Brugge JS, Symons M, Hynes RO. Integrin-mediated signals regulated by members of the rho family of GTPases. J Cell Biol 1998 : 142 : 573 586.
16. Couchman JR. Syndecans: proteoglycan regulators of cell-surface microdomains? Nat Rev Mol Cell Biol 2003 : 4 : 926 937.
17. Couchman JR, Chen L, Woods A. Syndecans and Cell adhesion. Int Rev Cytol 2001 : 207 : 113 150.
18. Desai UR, Petitou M, Björk I, Olson ST. Mechanism of heparin activation of antithrombin. J Biol Chem 2002 : 273 : 7478 7487.
19. Dews IC, Mackenzie KR. Transmembrane domains of the syndecan family of growth factor coreceptors display a hierarchy of homotypic and heterotypic interactions. PNAS 2007 : 104 : 20782 20787.
20. Ding K, Lopez-Burks M, Sánchez-Duran JA, Korc M, Lander AD. Growth factor-induced shedding of syndecan-1 confers glypican-1 dependence on mitogenic responses of cancer cells. J Cell Biol 2005 : 171 : 729 738.
21. Dovas A, Yoneda A, Couchman JR. PKCalpha-dependent activation of RhoA by syndecan-4 during focal adhesion formation. J Cell Sci 2006 : 119 : 2837 2846.
22. Echtermeyer F, Streit M, Wilcox-Adelman S, Saoncella S, Denhez F, Detmar M, Goetinck P. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J Clin Invest 2001 : 107 : R9 R14.
23. Endo K, Takino T, Miyamori H, Kinsen H, Yoshizaki T, Furukawa M, Sato H. Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J Biol Chem 2003 : 278 : 40764 40770.
24. Fanning AS, Anderson J. Protein-protein interactions: PDZ domain networks. Curr Biol 1996 : 6 : 1385 1388.
25. Fears CY, Gladson CL, Woods A. Syndecan-2 is expressed in the microvasculature of gliomas and regulates angiogenic processes in microvascular endothelial cells. J Biol Chem 2006 : 281 : 14533 14536.
26. Fitzgerald ML, Wang Z, Park PW, 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 2000 : 148 : 811 824.
27. Gao Y, Li M, Chen W, Simons M. Synectin, syndecan-4 cytoplasmic binding protein, inhibits cell migration. J Cell Physiol 2000 : 184 : 373 379.
28. Granés F, Urena JM, Rocamora N, Vilaró S. Ezrin links syndecan-2 to the cytoskeleton. J Cell Sci 2000 : 113 : 1267 1276.
29. Greene DK, Tumova S, Couchman JR, Woods A. Syndecan-4 associates with alpha-actinin. J Biol Chem 2003 : 278 : 7617 7623.
30. Grootjans JJ, Zimmerman P, Reekmans G, Smets A, Degeest G, Durr J, David G. Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc Natl Acad Sci USA 1997 : 94 : 13683 13688.
31. Häcker U, Nybakken K, Perrimon N. Heparan sulphate proteoglycans: the sweet side of development. Nat Rev Mol Cell Biol 2006 : 393 : 741 748.
32. Hienola A, Tumova S, Kulesskiy E, Rauvala H. N-syndecan deficiency impairs neural migration in brain. J Cell Biol 2006 : 174 : 569 580.
33. Hinz B, Dugina V, Ballestrem C, Wehrle-Haller B, Chaponnier C. Alpha-smooth muscle actin is crucial for focal adhesion maturation in myofibroblasts. Mol Biol Cell 2003 : 14 : 2508 2519.
34. Hotchin NA, Hall A. The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases. J Cell Biol 1995 : 131 : 1857 1865.
35. Hsueh YP, Yang FC, Kharazia V, Naisbitt S, Cohen AR, Weinberg RJ, Sheng M. Direct ineraction of CASK/LIN-2 and syndecan heparan sulphate proteoglycan and their overlapping distribution in neuronal synapses. J Cell Biol 1998 : 142 : 139 151.
36. Humphries JD, Byron A, Humphries MJ. Integrin ligands at a glance. J Cell Sci 2006 : 119 : 3901 3903.
37. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002 : 110 : 673 687.
38. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Nakamura E, Ito M, Nagasaka T, Kobayashi H, Kusugami K, Saito H, Muramatsu T. Syndecan-4 deficiency impairs the fetal vessels in the placental labyrinth. Dev Dyn 2000a : 219 : 539 544.
39. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Nakamura E, Kusugami K, Saito H, Muramatsu T. Syndecan-4 deficiency impairs focal adhesion formation only under restricted conditions. J Biol Chem 2000b : 275 : 5249 5252.
40. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005 : 26 : 503 510.
41. Kaksonen M, Pavlov I, Võikar V, Lauri SE, Hienola A, Riekki R, Lakso M, Taira T, Rauvala H. Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Mol Cell Neurosci 2002 : 21 : 158 172.
42. Kim CW, Goldberger OA, Gallo RL, 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 : 5 : 797 805.
43. Kinashi T. Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol 2005 : 5 : 546 559.
44. Komoriya A, Green LJ, Mervic M, Yamada SS, Yamada KM, Humphries MJ. The minimal essential sequence for a major cell type-specific adhesion site (CS1) within the alternatively spliced type III connecting segment domain of fibronectin is leucine-aspartic acid - valine. J Biol Chem 1991 : 266 : 15075 15079.
45. Koo BK, Jung YS, Shin J, Han I, Mortier E, Zimmermann P, Whiteford JR, Couchman JR, Oh ES, Lee W. Structural basis of syndecan-4 phosphorylation as a molecular switch to regulate signaling. J Mol Biol 2006 : 355 : 651 663.
46. Kramer KL, Yost HJ. Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev Cell 2002 : 2 : 115 124.
47. Kuberan B, Lech MZ, Beeler DL, Wu ZL, Rosenberg RD. Enzymatic synthesis of antithrombin III-binding heparan sulphate pentasaccharide. Nat Biotechnol 2003 : 21 : 1343 1346.
48. Kveiborg J, Albrechtsen R, Couchman JR, Wewer UM. Cellular roles of ADAM12 in health and disease. Int J Biochem Cell Biol 2008 : 40 : 1685 1702.
49. Lee D, Oh ES, Woods A, Couchman JR, Lee W. Solution structure of a syndecan-4 cytoplasmic domain and its interaction with phosphatidylinositol 4,5-bisphosphate. J Biol Chem 1998 : 273 : 13022 13029.
50. Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 2002 : 111 : 635 646.
51. Lim ST, Longley RL, Couchman JR, Woods A. Direct binding of syndecan-4 cytoplasmic domain to the catalytic domain of protein kinase C alpha (PKC alpha) increases focal adhesion localization of PKC alpha. J Biol Chem 2003 : 278 : 13795 13802.
52. Lo SH. Focal adhesions: what's new inside. Dev Biol 2006 : 294 : 280 291.
53. Longley RL, Woods A, Fleetwood A, Cowling GJ, Gallagher JT, Couchman JR. Control of morphology, cytoskeleton and migration by syndecan-4. J Cell Sci 1999 : 112 : 3421 3431.
54. Lundin L, Larsson H, Kreuger J, Kanda S, Lindahl U, Salmivirta M, Claesson-Welsh L. Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis. J Biol Chem 2000 : 275 : 24653 24660.
55. Machesky LM, Hall A. Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization. J Cell Biol 1997 : 138 : 913 926.
56. Maday S, Anderson E, Chang HC, Shorter J, Satoh A, Sfakianos J, Flsch H, Anderson JM, Walther Z, Mellman I. A PDZ-binding motif controls basolateral targeting of syndecan-1 along the biosynthetic pathway in polarized epithelial cells. Traffic 2008 : 9 : 1915 1924.
57. Mahalingam Y, Gallagher JT, Couchman JR. Cellular adhesion responses to the heparin-binding (HepII) domain of fibronectin require heparan sulfate with specific properties. J Biol Chem 2007 : 282 : 3221 3230.
58. Marastoni S, Ligresti G, Lorenzon E, Colombatti A, Mongiat M. Extracellular matrix: a matter of life and death. Connect Tissue Res 2008 : 49 : 203 206.
59. Martin P, Leibovich SJ. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol 2005 : 15 : 599 560.
60. Matthews HK, Marchant L, Carmona-fontaine C, Kuriyama S, Larraíne J, Holt MR, Parsons M, Mayor R. Directional migration of neural crest cells in vivo is regulated by syndecan-4/Rac1 and non-canonical Wnt signalling/RhoA. Development 2008 : 135 : 1771 1780.
61. McFall AJ, Rapraeger AC. Characterization of the high affinity cell-binding domain in the cell surface proteoglycan syndecan-4. J Biol Chem 1998 : 273 : 28270 28276.
62. Mcquade KJ, Beauvais DM, Burbach BJ, Rapraeger AC. Syndecan-1 regulates alphaVbeta5 integrin activity in B82L fibroblasts. J Cell Sci 2006 : 119 : 2445 2456.
63. Mehrotra B, Elliott JT, Chen J, Olszewski JD, Profit AA, Chaudhary A, Fukuda M, Mikoshiba K, Prestwich GD. Selective photoaffinity labeling of the inositol polyphosphate binding C2B domains of synaptotagmins. J Biol Chem 1997 : 272 : 4237 4244.
64. Morgan MR, Humphries MJ, Bass MD. Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol 2007 : 8 : 957 969.
65. Muñoz R, Moreno M, Oliva C, Orbenes C, Larraín J. Syndecan-4 regulates non-canonical Wnt signalling and is essential for convergent and extension movements in Xenopus embryos. Nat Cell Biol 2006 : 8 : 492 500.
66. Murphy KJ, Merry CL, Lyon M, Thompson JE, Roberts IS, Gallagher JT. A new model for the domain structure of heparan sulfate based on the novel specificity of K5 lyase. J Biol Chem 2004 : 279 : 27239 27245.
67. Nadanaka S, Kitagawa H. Heparan sulphate biosynthesis and disease. J Biochem 2008 : 144 : 7 14.
68. Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995 : 81 : 53 62.
69. Oh ES, Woods A, Lim ST, Theibert A, Couchman JR. Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol 4,5-bisphosphate co-ordinately regulate protein kinase C activity. J Biol Chem 1998 : 273 : 10624 10629.
70. Rawson JM, Dimitroff B, Johnson KG, Rawson JM, Ge X, Van Vactor D, Selleck SB. The heparan sulfate proteoglycans Dally-like and Syndecan have distinct functions in axon guidance and visual-system assembly in Drosophila. Curr Biol 2005 : 15 : 833 838.
71. Reizes O, Lincecum J, Wang Z, Goldberger O, Huang L, Kaksonen M, Ahima R, Hinkes MT, Barsh GS, Rauvala H, Bernfield M. Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell 2001 : 106 : 105 116.
72. Rhiner C, Gysi S, Fröhli E, Hengartner MO, Hajnal A. Syndecan regulates cell migration and axon guidance in C. elegans. Development 2005 : 132 : 4621 4633.
73. Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992 : 70 : 389 399.
74. Sanderson RD, Yang Y, Kelly T, MacLeod V, Dai Y, Theus A. Enzymatic remodeling of heparan sulfate proteoglycans within the tumor microenvironment: growth regulation and the prospect of new cancer therapies. J Cell Biochem 2005 : 96 : 897 905.
75. Saoncella S, Calautti E, Neveu W, Goetinck PF. Syndecan-4 regulates ATF-2 transcriptional activity in a Rac1-dependent manner. J Biol Chem 2004 : 279 : 47172 47176.
76. Saoncella S, Echtermeyer F, Denhez F, Nowlen JK, Mosher DF, Robinson SD, Hynes RO, Goetinck PF. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibres. PNAS 1999 : 96 : 2805 2810.
77. Schäfer M, Werner S. Transcriptional control of wound repair. Annu Rev Cell Dev Biol 2007 : 23 : 60 92.
78. Schmidt A, Echtermeyer F, Alozie A, Brands K, Buddecke E. Plasmin- and thrombin-accelerated shedding of syndecan-4 ectodomain generates cleavage sites at Lys(114)-Arg(115) and Lys(129)-Val(130) bonds. J Biol Chem 2005 : 280 : 34441 34446.
79. Sheppard D. Integrin-mediated activation of latent transforming growth factor beta. Cancer Metastasis Rev 2005 : 24 : 395 402.
80. Shin J, Lee W, Lee D, Koo B-K, Han I, Lim Y, Woods A, Couchman JR, Oh E-S. Solution structure of the dimeric cytoplasmic domain of syndecan-4. Biochemistry 2001 : 40 : 8471 8478. (Pubitemid 32667251)
81. Singer AJ, Clark RA. Cutaneous wound healing. N Engl J Med 1999 : 341 : 738 746.
82. Skidmore MA, Guimond SE, Rudd TR, Fernig DG, Turnbull JE, Yates EA. The activities of heparan sulfate and its analogue heparin are dictated by biosynthesis, sequence and conformation. Conn Tiss Res 2008 : 49 : 207 210.
83. Stepp MA, Gibson HE, Gala PH, Iglesia DD, Pajoohesh-Ganji A, Pal-Ghosh S, Brown M, Aquino C, Schwartz AM, Goldberger O, Hinkes MT, Bernfield M. Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J Cell Sci 2002 : 115 : 4517 4531.
84. Subramanian S., Fitzgerald ML, Bernfield M. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J Biol Chem 1997 : 272 : 14713 14720.
85. Turnbull JE, Fernig DG, Ke Y, Wilkinson MC, Gallagher JT. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulphate. J Biol Chem 1992 : 267 : 10337 10341.
86. Wells CM, Walmsley M, Ooi S, Tybulewicz V, Ridley AJ. Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J Cell Sci 2004 : 117 : 1259 1268.
87. Wheeler AP, Ridley AJ. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp Cell Res 2004 : 301 : 43 49.
88. Wheeler AP, Wells CM, Smith SD, Vega FM, Henderson RB, Tybulewicz VL, Ridley AJ. Rac1 and Rac2 regulate macrophage morphology but are not essential for migration. J Cell Sci 2006 : 119 : 2749 2757.
89. Whiteford JR, Behrends V, Kirby H, Kusche-Gullberg M, Muramatsu T, Couchman JR. Syndecans promote integrin-mediated adhesion of mesenchymal cells in two distinct pathways. Exp Cell Res 2007 : 313 : 3902 3913.
90. Whiteford JR, Couchman JR. A conserved NXIP motif is required for cell adhesion properties of the syndecan-4 ectodomain. J Biol Chem 2006 : 281 : 32156 32163.
91. Whiteford JR, Ko S, Lee W, Couchman JR. Structural and cell adhesion properties of zebrafish syndecan-4 are shared with higher vertebrates. J Biol Chem 2008 : 283 : 29322 29330.
92. Woods A, Couchman JR. Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol Biol Cell 1994 : 5 : 183 192.
93. Woods A, Longley RL, Tumova S, Couchman JR. Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch Biochem Biophys 2000 : 374 : 66 72.
94. Yoneda A, Multhaupt HA, Couchman JR. The Rho kinases I and II regulate different aspects of myosin II activity. J Cell Biol 2005 : 170 : 443 453.
95. Zhang L, Esko JD. Amino acid determinants that drive heparan sulfate assembly in a proteoglycan. J Biol Chem 1994 : 269 : 19295 19299.