The soluble form of urokinase receptor promotes angiogenesis through its Ser88-Arg-Ser-Arg-Tyr92 chemotactic sequence

Journal of Thrombosis and Haemostasis

Volumn 8, Issue 12, 2010, Pages 2789-2799

  Bifulco, K ^a   Longanesi Cattani, I ^a   Gala, M ^a   Di Carluccio, G ^a   Masucci, M T ^a   Pavone, V ^b   Lista, L ^b   Arra, C ^a   Stoppelli, M P ^c   Carriero, M V ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

Angiogenesis; Endothelial cell migration; Formyl peptide receptor; Soluble urokinase receptor; Vitronectin receptor

Indexed keywords

ARGININE; FIBROBLAST GROWTH FACTOR 2; PROTEINASE; SERINE; TYROSINE; UROKINASE; UROKINASE RECEPTOR; VASCULOTROPIN; VITRONECTIN RECEPTOR;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CHEMOTAXIS; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CHEMOTAXIS; COCULTURE TECHNIQUES; HUMANS; MICE; MICE, NUDE; MICROSCOPY, FLUORESCENCE; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; SIGNAL TRANSDUCTION; SOLUBILITY;

EID: 78650006378     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2010.04075.x     Document Type: Article

References (41)

1. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003; 9: 653-60.
2. Mahabeleshwar GH, Feng W, Reddy K, Plow EF, Byzova TV. Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ Res 2007; 101: 570-80.
3. Prager GW, Breuss JM, Steurer S, Mihaly J, Binder BR. Vascular endothelial growth factor (VEGF) induces rapid prourokinase (pro-uPA) activation on the surface of endothelial cells. Blood 2004; 103: 955-6.
4. Binder BR, Mihaly J, Prager GW. uPAR-uPA-PAI-1 interactions and signalling: a vascular biologist's view. Thromb Haemost 2007; 97: 336-42.
5. Pepper MS. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 2001; 21: 1104-17.
6. Blasi F, Carmeliet P. uPAR: a versatile signaling orchestrator. Nat Rev Mol Cell Biol 2002; 3: 932-43.
7. Smith HW, Marshall CJ. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 2010; 11: 23-36.
8. Prager GW, Mihaly J, Brunner PM, Koshelnick Y, Hoyer-Hansen G, Binder BR. Urokinase mediates endothelial cell survival via induction of the X-linked inhibitor of apoptosis protein. Blood 2009; 113: 1383-90.
9. Ploug M, Rønne E, Behrendt N, Jensen AL, Blasi F, Danø K. Cellular receptor for urokinase plasminogen activator. Carboxyl-terminal processing and membrane anchoring by glycosyl-phosphatidylinositol. J Biol Chem 1991; 266: 1926-33.
10. Rasch MG, Lund IK, Almasi CE, Hoyer-Hansen G. Intact and cleaved uPAR forms: diagnostic and prognostic value in cancer. Front Biosci 2008; 13: 6752-62.
11. Ploug M, Ellis V. Structure-function relationships in the receptor for urokinase-type plasminogen activator. Comparison to other members of the Ly-6 family and snake venom alpha-neurotoxins. FEBS Lett 1994; 349: 163-8.
12. Selleri C, Montuori N, Ricci P, Visconte V, Baiano A, Carriero MV, Rotoli B, Rossi G, Ragno P. In vivo activity of the cleaved form of soluble urokinase receptor: a new hematopoietic stem/progenitor cell mobilizer. Cancer Res 2006; 66: 10885-990.
13. Resnati M, Guttinger M, Valcamonica S, Sidenius N, Blasi F, Fazioli F. Proteolytic cleavage of the urokinase receptor substitutes for the agonist-induced chemotactic effect. EMBO J 1996; 15: 1572-82.
14. Resnati M, Pallavicini I, Wang JM, Oppenheim J, Serhan CN, Romano M, Blasi F. The fibrinolytic receptor for urokinase activates the G protein-coupled chemotactic receptor FPRL1/LXA4R. Proc Natl Acad Sci USA 2002; 99: 1359-64.
15. Gargiulo L, Longanesi-Cattani I, Bifulco K, Franco P, Raiola R, Campiglia P, Grieco P, Peluso G, Stoppelli MP, Carriero MV. Cross-talk between fMLP and vitronectin receptors triggered by urokinase receptor-derived SRSRY peptide. J Biol Chem 2005; 280: 25225-32.
16. Sidenius N, Blasi F. The urokinase plasminogen activator system in cancer: recent advances and implication for prognosis and therapy. Cancer Metastasis Rev 2003; 22: 205-22.
17. Henic E, Borgfeldt C, Christensen IJ, Casslén B, Høyer-Hansen G. Cleaved forms of the urokinase plasminogen activator receptor in plasma have diagnostic potential and predict postoperative survival in patients with ovarian cancer. Clin Cancer Res 2008; 14: 5785-93.
18. Shariat SF, Roehrborn CG, McConnell JD, Park S, Alam N, Wheeler TM, Slawin KM. Association of the circulating levels of the urokinase system of plasminogen activation with the presence of prostate cancer and invasion, progression, and metastasis. J Clin Oncol 2007; 25: 349-55.
19. Llinas P, Le Du MH, Gårdsvoll H, Danø K, Ploug M, Gilquin B, Stura EA, Ménez A. Crystal structure of the human urokinase plasminogen activator receptor bound to an antagonist peptide. EMBO J 2005; 24: 1655-63.
20. Barinka C, Parry G, Callahan J, Shaw DE, Kuo A, Bdeir K, Cines DB, Mazar A, Lubkowski J. Structural basis of interaction between urokinase-type plasminogen activator and its receptor. J Mol Biol 2006; 363: 482-95.
21. Furlan F, Orlando S, Laudanna C, Resnati M, Basso V, Blasi F, Mondino A. The soluble D2D3(88-274) fragment of the urokinase receptor inhibits monocyte chemotaxis and integrin-dependent cell adhesion. J Cell Sci 2004; 117: 2909-16.
22. Carriero MV, Longanesi-Cattani I, Bifulco K, Maglio O, Lista L, Barbieri A, Votta G, Masucci MT, Arra C, Franco R, De Rosa M, Stoppelli MP, Pavone V. Structure-based design of an urokinase-type plasminogen activator receptor-derived peptide inhibiting cell migration and lung metastasis. Mol Cancer Ther 2009; 9: 2708-17.
23. Arnaoutova I, Kleinman HK. In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat Protoc 2010; 5: 628-35.
24. Masucci MT, Pedersen N, Blasi F. A soluble, ligand binding mutant of the human urokinase plasminogen activator receptor. J Biol Chem 1991; 266: 8655-8.
25. Carriero MV, Franco P, Del Vecchio S, Massa O, Botti G, D'Aiuto G, Stoppelli MP, Salvatore M. Tissue distribution of soluble and receptor-bound urokinase in human breast cancer using a panel of monoclonal antibodies. Cancer Res 1994; 54: 5445-54.
26. Yang S, Graham J, Kahn JW, Schwartz EA, Gerritsen ME. Functional roles for PECAM-1 (CD31) and VE-cadherin (CD144) in tube assembly and lumen formation in three-dimensional collagen gels. Am J Pathol 1999; 155: 887-95.
27. Baroni A, Donnarumma G, Paoletti I, Longanesi-Cattani I, Bifulco K, Tufano MA, Carriero MV. Antimicrobial human beta-defensin-2 stimulates migration, proliferation and tube formation of human umbilical vein endothelial cells. Peptides 2009; 30: 267-72.
28. Montuori N, Carriero MV, Salzano S, Rossi G, Ragno P. The cleavage of the urokinase receptor regulates its multiple functions. J Biol Chem 2002; 277: 46932-9.
29. Carriero MV, Del Vecchio S, Franco P, Potena M, Botti G, Stoppelli MP, Salvatore M. Vitronectin binding to urokinase receptor in human breast cancer. Clin Cancer Res 1997; 3: 1299-308.
30. Guedez L, Rivera AM, Salloum R, Miller ML, Diegmueller JJ, Bungay PM, Stetler-Stevenson WG. Quantitative assessment of angiogenic responses by the directed in vivo angiogenesis assay. Am J Pathol 2003; 162: 1431-9.
31. Perez DM, Karnik SS. Multiple signaling states of G-protein-coupled receptors. Pharmacol Rev 2005; 57: 147-61.
32. Degryse B, Resnati M, Czekay RP, Loskutoff DJ, Blasi F. Domain 2 of the urokinase receptor contains an integrin-interacting epitope with intrinsic signaling activity: generation of a new integrin inhibitor. J Biol Chem 2005; 280: 24792-803.
33. Kjaergaard M, Hansen LV, Jacobsen B, Gardsvoll H, Ploug M. Structure and ligand interactions of the urokinase receptor (uPAR). Front Biosci 2008; 13: 5441-61.
34. Rabiet MJ, Huet E, Boulay F. The N-formyl peptide receptors and the anaphylatoxin C5a receptors: an overview. Biochimie 2007; 89: 1089-106.
35. Somanath PR, Malinin NL, Byzova TV. Cooperation between integrin alphavbeta3 and VEGFR2 in angiogenesis. Angiogenesis 2009; 12: 177-85.
36. Jo M, Thomas KS, Wu L, Gonias SL. Soluble urokinase-type plasminogen activator receptor inhibits cancer cell growth and invasion by direct urokinase-independent effects on cell signaling. J Biol Chem 2003; 278: 46692-8.
37. Jo M, Takimoto S, Montel V, Gonias SL. The urokinase receptor promotes cancer metastasis independently of urokinase-type plasminogen activator in mice. Am J Pathol 2009; 175: 190-200.
38. Carriero MV, Franco P, Vocca I, Alfano D, Longanesi-Cattani I, Bifulco K, Mancini A, Caputi M, Stoppelli MP. Structure, function and antagonists of urokinase-type plasminogen activator. Front Biosci 2009; 14: 3782-94.
39. Bifulco K, Longanesi-Cattani I, Gargiulo L, Maglio O, Cataldi M, De Rosa M, Stoppelli MP, Pavone V, Carriero MV. An urokinase receptor antagonist that inhibits cell migration by blocking the formyl peptide receptor. FEBS Lett 2008; 582: 1141-6.
40. Dranoff G. Cytokines in cancer pathogenesis and cancer therapy. Nat Rev Cancer 2004; 4: 11-22.
41. Chavakis T, Kanse SM, May AE, Preissner KT. Haemostatic factors occupy new territory: the role of the urokinase receptor system and kininogen in inflammation. Biochem Soc Trans 2002; 30: 168-73.