Syndecan-4 contributes to endothelial tubulogenesis through interactions with two motifs inside the pro-angiogenic N-terminal domain of thrombospondin-1

Journal of Cellular Physiology

Volumn 214, Issue 3, 2008, Pages 828-837

  Nunes, Sara Santana ^a   Do Outeiro Bernstein, Marianna A Ferrari ^a   Juliano, Luiz ^b   Vardiero, Francisco ^a   Nader, Helena B ^b   Woods, Anne ^c   Legrand, Chantal ^d,e   Morandi, Verônica ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d INSERM   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; GELATIN; MONOCLONAL ANTIBODY; PROTEIN KINASE B; PROTEIN KINASE C; RECOMBINANT PROTEIN; SYNDECAN 4; THROMBOSPONDIN 1; THROMBOSPONDIN 18; UNCLASSIFIED DRUG; ANGIOGENIC PROTEIN; ANTIBODY; PEPTIDE FRAGMENT; PROTEIN KINASE INHIBITOR;

AMINO TERMINAL SEQUENCE; ANGIOGENESIS; APOPTOSIS; ARTICLE; CELL ADHESION; CELL INTERACTION; CELL PROTECTION; CELL SPREADING; CELL SURFACE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CELL MOTION; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENDOTHELIUM; METABOLISM; MOLECULAR GENETICS; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; SWINE; VASCULARIZATION;

MAMMALIA;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANGIOGENIC PROTEINS; ANIMALS; ANTIBODIES; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM; ENZYME ACTIVATION; FIBRONECTINS; HUMANS; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDE FRAGMENTS; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; SWINE; SYNDECAN-4; THROMBOSPONDIN 1;

EID: 38449103435     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21281     Document Type: Article

References (48)

1. Adams JC, Lawler J. 2004. The thrombospondins. Int J Biochem Cell Biol 36:961-968.
2. Baciu PC, Saoncella S, Lee SH, Denhez F, Leuthardt D, Goetinck PF. 2000. Syndesmos, a protein that interacts with the cytoplasmic domain of syndecan-4, mediates cell spreading and actin cytoskeletal organization. J Cell Sci 2:315-324.
3. Bonnefoy A, Legrand C. 2000. Proteolysis of subendothelial adhesive glycoproteins (fibronectin, thrombospondin, and von Willebrand factor) by plasmin, leukocyte cathepsin G, and elastase. Thromb Res 98:323-332.
4. Carmeliet P. 2003. Angiogenesis in health and disease. Nat Med 9:653-660.
5. Chandrasekaran L, He CZ, Al-Barazi H, Krutzsch HC, Iruela-Arispe ML, Roberts DD. 2000. Cell contact-dependent activation of integrin α3β1 integrin modulates endothelial cell responses to thrombospondin-1. Mol Biol Cell 11:2885-2900.
6. Clezardin P, Lawler J, Amiral J, Quentin G, Delmas P. 1997. Identification of cell adhesive sites in the N-terminal domain of thrombospondin-1. Biochem J 321:819-827.
7. Cross MJ, Claesson-Welsh L. 2001. FGF and VEGF function in angiogenesis: Signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol Sci 22:201-207.
8. Echtermeyer F, Streit M, Wilcox-Adelman S, Saoncella S, Denhez F, Detmar M, Goetinck PF. 2001. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J Clin Invest 107:R9-R14.
9. Elzie CA, Murphy-Ullrich JE. 2004. The N-terminus of thrombospondin: The domain stands apart. Int J Biochem Cell Biol 36:1090-1101.
10. Fears CY, Woods A. 2006. The role of syndecans in disease and wound healing. Matrix Biol 25:443-456.
11. Fears CY, Gladson CL, Woods A. 2006. Syndecan-2 is expressed in the microvasculature of gliomas and regulates angiogenic processes in microvascular endothelial cells. J Biol Chem 281:14533-14536.
12. Ferrari do Outeiro-Bernstein MA, Nunes SS, Andrade ACM, Alves TR, Legrand C, Morandi V. 2002. A recombinant NH2-terminal heparin binding domain of the adhesive glycoprotein, thrombospondin-1, promotes endothelial tube formation and cell survival: A possible role for syndecan-4 proteoglycan. Matrix Biol 21:311-324.
13. Filleur S, Volpert OV, Degeorges A, Voland C, Reiher F, Clezardin P, Bouck N, Cabon F. 2001. In vivo mechanisms by which tumors producing thrombospondin I bypass its inhibitory effects. Genes Dev 15:1373-1382.
14. Fontana A, Filleur S, Guglielmi J, Frappart L, Boissier S, Cabon F, Bruno-Bossio G, Clézardin P. 2005. Human breast tumors override the antiangiogenic effect of stromal thrombospondin-1 in vivo. Int J Cancer 116:686-691.
15. Goicoechea S, Orr AW, Pallero MA, Eggleton P, Murphy-Ullrich JE. 2000. Thrombospondin mediates focal adhesion disassembly through interactions with cell surface calreticulin. J Biol Chem 275:36358-36368.
16. Greene DK, Tumova S, Couchman JR, Woods A. 2003. Syndecan-4 associates with alpha-actinin. J Biol Chem 278:7617-7623.
17. Homandberg GA, Kramer-Bjerke J. 1987. Thrombospondin binds to amino-terminal fragments of plasma fibronectin. Thromb Res 48:329-335.
18. Huang W, Chiquet-Ehrismann R, Moyano JV, Garcia-Pardo A, Orend G. 2001. Interference of tenascin-C with syndecan-4 binding to fibronectin blocks cell adhesion and stimulates tumor cell proliferation. Cancer Res 61:8586-8594.
19. Ilan N, Mahooti S, Madri JA. 1998. Distinct signal transduction pathways are utilized during the tube formation and survival phases of in vitro angiogenesis. J Cell Sci 111:3621-3631.
20. Iruela-Arispe ML, Lombardo M, Krutzsch HC, Lawler J, Roberts RR. 1999. Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type I repeats. Circulation 100:1423-1431.
21. Jaffe EA, Nachman RL, Becker CG, Minick CR. 1973. Culture of human endothelial cells derived from umbilical cord veins. Identification by morphologic and immunologic criteria. J Clin Invest 52:2745-2756.
22. Kennedy SG, Kandel ES, Cross TK, Hay N. 1999. Akt/Protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol Cell Biol 19:5800-5810.
23. Lee NV, Sato M, Annis DS, Loo JA, Wu L, Mosher DF, Iruela-Arispe ML. 2006. ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J 25:5270-5283.
24. Legrand C, Morandi V, Mendelovitz S, Shaked H, Hartman JR, Panet A. 1994. Selective inhibition of platelet macroaggregate formation by a recombinant heparin-binding domain of human thrombospondin. Arterioscler Thromb 14:1784-1791.
25. Longley RL, Woods A, Fleetwood A, Cowling GJ, Gallagher JT, Couchman JR. 1999. Control of morphology, cytoskeleton and migration by syndecan-4. J Cell Sci 112:3421-3431.
26. McFall AJ, Rapraeger AC. 1997. Identification of an adhesion site within the syndecan-4 extracellular protein domain. J Biol Chem 272:12901-12904.
27. Morandi V, Edelman L, Legrand YJ, Legrand C. 1994. Characterization of a novel monoclonal antibody (V58A4) raised against a recombinant NH2-terminal heparin-binding fragment of human endothelial cell thrombospondin. FEBS Lett 346:156-160.
28. Murphy-Ullrich JE. 2001. The de-adhesive activity of matricellular proteins: Is intermediate cell adhesion an adaptive state? J Clin Invest 107:785-790.
29. Murphy-Ullrich JE, Mosher DF. 1987. Interactions of thrombospondin with endothelial cells: receptor-mediated binding and degradation. J Cell Biol 105:1603-1611.
30. Murphy-Ullrich JE, Gurusiddappa S, Frazier WA, Hook M. 1993. Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity. J Biol Chem 268:26784-26789.
31. Oh ES, Woods A, Couchman JR. 1997. Multimerization of the cytoplasmic domain of syndecan-4 is required for its ability to activate protein kinase C. J Biol Chem 272:11805-11811.
32. Orr AW, Pedraza CE, Pallero MA, Elzie CA, Goicoechea S, Strickland DK, Murphy-Ullrich JE. 2003. Low density lipoprotein receptor-related protein is a calreticulin coreceptor that signals focal adhesion disassembly. J Cell Biol 161:1179-1189.
33. Poon RT, Chung KK, Cheung ST, Lau CP, Tong SW, Leung KL, Yu WC, Tuszynski G, Fan ST. 2004. Clinical significance of thrombospondin expression in hepatocellular carcinoma. Clin Cancer Res 10:4150-4157.
34. Pytela R, Pierschbacher MD, Ruoslahti E. 1985. Identification and isolation of a 140 kd cell surface glycoprotein with properties expected of a fibronectin receptor. Cell 40:191-198.
35. Roy R, Zhang B, Moses MA. 2006. Making the cut: Protease-mediated regulation of angiogenesis. Exp Cell Res 312:608-622.
36. Sanz L, Alvarez-Vallina L. 2003. The extracellular matrix: A new turn-of-the-screw for antiangiogenic strategies. Trends Mol Med 9:256-262.
37. Sutton CD, O'Byrne K, Goddard JC, Marshall L, Jones L, Garcea G, Dennison AR, Poston G, Lloyd DM, Berry DP. 2005. Expression of thrombospondin-1 in resected colorectal liver metastases predicts poor prognosis. Clin Cancer Res 11:6567-6573.
38. Suzuki N, Ichikawa N, Kasai S, Yamada M, Nishi N, Morioka H, Yamashita H, Kitagawa Y, Utani A, Hoffman MP, Nomizu M. 2003. Syndecan binding sites in the laminin alpha1 chain G domain. Biochemistry 42:12625-12633.
39. Tan K, Duquette M, Liu J, Zhang R, Joachimiak A, Wang J, Lawler J. 2006. The structures of the trombospondin-1 N-treminal domain and its complex with a synthetic pentameric heparin. Structure 14:33-42.
40. Taraboletti G, Morbidelli L, Donnini S, Parenti A, Granger H, Giavazzi R, Ziche M. 2000. The heparin binding 25 kDa fragment of thrombospondin-1 promotes angiogenesis and modulates gelatinase and TIMP-2 production in endothelial cells. FASEB J 14:1674-1676.
41. Tolsma SS, Volpert OV, Good DJ, Frazier WA, Polverini PJ, Bouck N. 1993. Peptides derived from two separate domains of the matrix protein thrombospondin-1 have antiangiogenic activity. J Cell Biol 122:497-511.
42. Vogel T, Guo N, Krutzsch HC, Blake DA, Hartman J, Mendelovitz S, Panet A, Roberts DD. 1993. Modulation of endothelial cell proliferation by recombinant heparin-binding domain and synthetic peptides from the type I repeats of thrombospondin. J Cell Biochem 53:74-84.
43. Vuori K, Ruoslahti E. 1993. Activation of protein kinase C precedes alpha 5 beta I integrin-mediated cell spreading on fibronectin. J Biol Chem 268:21459-21462.
44. Whiteford JR, Couchman JR. 2006. A conserved NXIP motif id required for cell adhesion properties of the syndecan-4 ectodomain. J Biol Chem 281:32156-32163.
45. Woods A, Couchman JR. 1994. Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol Biol Cell 5:183-192.
46. Woods A, McCarthy JB, Furcht LT, Couchman JR. 1993. A synthetic peptide from the COOH-terminal heparin-binding domain of fibronectin promotes focal adhesion formation. Mol Biol Cell 4:605-613.
47. Woods A, Longley RL, Tumova S, Couchman JR. 2000. Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch Biochem Biophys 374:66-72.
48. Zafar RS, Zeng Z, Walz DA. 1992. Localization of two binding domains for thrombospondin within fibronectin. Arch Biochem Biophys 297:271-276.