Tissue factor-Akt signaling triggers microvessel formation

Journal of Thrombosis and Haemostasis

Volumn 10, Issue 9, 2012, Pages 1895-1905

  Arderiu, G ^a,b   Pena E ^a,b   Aledo, R ^a,b   Badimon, L ^a,b  

^a CSIC   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Akt; Angiogenesis; Endothelial cells; Tissue factor

Indexed keywords

MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN KINASE B; RAF PROTEIN; SMALL INTERFERING RNA; THROMBOPLASTIN; TRANSCRIPTION FACTOR ETS 1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

CELL LINE; HUMANS; IMMUNOPRECIPITATION; MICROVESSELS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; THROMBOPLASTIN;

EID: 84865745003     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2012.04848.x     Document Type: Article

References (45)

1. Bach RR. Initiation of coagulation by tissue factor. CRC Crit Rev Biochem 1988; 23: 339-68.
2. Bugge TH, Xiao Q, Kombrinck KW, Flick MJ, Holmback K, Danton MJ, Colbert MC, Witte DP, Fujikawa K, Davie EW, Degen JL. Fatal embryonic bleeding events in mice lacking tissue factor, the cell-associated initiator of blood coagulation. Proc Natl Acad Sci USA 1996; 93: 6258-63.
3. Carmeliet P, Mackman N, Moons L, Luther T, Gressens P, Van Vlaenderen I, Demunck H, Kasper M, Breier G, Evrard P, Muller M, Risau W, Edgington T, Collen D. Role of tissue factor in embryonic blood vessel development. Nature 1996; 383: 73-5.
4. Toomey JR, Kratzer KE, Lasky NM, Stanton JJ, Broze GJ Jr. Targeted disruption of the murine tissue factor gene results in embryonic lethality. Blood 1996; 88: 1583-7.
5. Contrino J, Hair G, Kreutzer DL, Rickles FR. In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med 1996; 2: 209-15.
6. Levi M, ten Cate H, Bauer KA, van der Poll T, Edgington TS, Buller HR, van Deventer SJ, Hack CE, ten Cate JW, Rosenberg RD. Inhibition of endotoxin-induced activation of coagulation and fibrinolysis by pentoxifylline or by a monoclonal anti-tissue factor antibody in chimpanzees. J Clin Invest 1994; 93: 114-20.
7. Versteeg HH, Peppelenbosch MP, Spek CA. The pleiotropic effects of tissue factor: a possible role for factor VIIa-induced intracellular signalling? Thromb Haemost 2001; 86: 1353-9.
8. Versteeg HH, Peppelenbosch MP, Spek CA. Tissue factor signal transduction in angiogenesis. Carcinogenesis 2003; 24: 1009-13.
9. Ruf W, Dorfleutner A, Riewald M. Specificity of coagulation factor signaling. J Thromb Haemost 2003; 1: 1495-503, 300[pii].
10. Dorfleutner A, Hintermann E, Tarui T, Takada Y, Ruf W. Cross-talk of integrin alpha3beta1 and tissue factor in cell migration. Mol Biol Cell 2004; 15: 4416-25.
11. Ahamed J, Ruf W. Protease-activated receptor 2-dependent phosphorylation of the tissue factor cytoplasmic domain. J Biol Chem 2004; 279: 23038-44.
12. Belting M, Dorrell MI, Sandgren S, Aguilar E, Ahamed J, Dorfleutner A, Carmeliet P, Mueller BM, Friedlander M, Ruf W. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat Med 2004; 10: 502-9.
13. van den Berg YW, van den Hengel LG, Myers HR, Ayachi O, Jordanova E, Ruf W, Spek CA, Reitsma PH, Bogdanov VY, Versteeg HH. Alternatively spliced tissue factor induces angiogenesis through integrin ligation. Proc Natl Acad Sci USA 2009; 106: 19497-502.
14. Rottingen JA, Enden T, Camerer E, Iversen JG, Prydz H. Binding of human factor VIIa to tissue factor induces cytosolic Ca2+ signals in J82 cells, transfected COS-1 cells, Madin-Darby canine kidney cells and in human endothelial cells induced to synthesize tissue factor. J Biol Chem 1995; 270: 4650-60.
15. Camerer E, Rottingen JA, Iversen JG, Prydz H. Coagulation factors VII and X induce Ca2+ oscillations in Madin-Darby canine kidney cells only when proteolytically active. J Biol Chem 1996; 271: 29034-42.
16. Poulsen LK, Jacobsen N, Sorensen BB, Bergenhem NC, Kelly JD, Foster DC, Thastrup O, Ezban M, Petersen LC. Signal transduction via the mitogen-activated protein kinase pathway induced by binding of coagulation factor VIIa to tissue factor. J Biol Chem 1998; 273: 6228-32.
17. Camerer E, Rottingen JA, Gjernes E, Larsen K, Skartlien AH, Iversen JG, Prydz H. Coagulation factors VIIa and Xa induce cell signaling leading to up-regulation of the egr-1 gene. J Biol Chem 1999; 274: 32225-33.
18. Sorensen BB, Freskgard PO, Nielsen LS, Rao LV, Ezban M, Petersen LC. Factor VIIa-induced p44/42 mitogen-activated protein kinase activation requires the proteolytic activity of factor VIIa and is independent of the tissue factor cytoplasmic domain. J Biol Chem 1999; 274: 21349-54.
19. Versteeg HH, Hoedemaeker I, Diks SH, Stam JC, Spaargaren M, van Bergen En Henegouwen PM, van Deventer SJ, Peppelenbosch MP. Factor VIIa/tissue factor-induced signaling via activation of Src-like kinases, phosphatidylinositol 3-kinase, and Rac. J Biol Chem 2000; 275: 28750-6.
20. Wang P, DeFea KA. Protease-activated receptor-2 simultaneously directs beta-arrestin-1-dependent inhibition and Galphaq-dependent activation of phosphatidylinositol 3-kinase. Biochemistry 2006; 45: 9374-85.
21. Arderiu G, Pena E, Aledo R, Juan-Babot O, Badimon L. Tissue factor regulates microvessel formation and stabilization by induction of chemokine (C-C motif) ligand 2 expression. Arterioscler Thromb Vasc Biol 2011; 31: 2607-15.
22. Arderiu G, Peña E, Aledo R, Espinosa S, Badimon L. Ets-1 transcription is required in tissue factor driven microvessel formation and stabilization. Angiogenesis 2012; DOI: 10.1007/s10456-012-9293-x.
23. Lavenburg KR, Ivey J, Hsu T, Muise-Helmericks RC. Coordinated functions of Akt/PKB and ETS1 in tubule formation. FASEB J 2003; 17: 2278-80.
24. Versteeg HH, Schaffner F, Kerver M, Petersen HH, Ahamed J, Felding-Habermann B, Takada Y, Mueller BM, Ruf W. Inhibition of tissue factor signaling suppresses tumor growth. Blood 2008; 111: 190-9, blood-2007-07-101048 [pii].
25. Nystedt S, Ramakrishnan V, Sundelin J. The proteinase-activated receptor 2 is induced by inflammatory mediators in human endothelial cells. Comparison with the thrombin receptor. J Biol Chem 1996; 271: 14910-5.
26. Pradier A, Ettelaie C. The influence of exogenous tissue factor on the regulators of proliferation and apoptosis in endothelial cells. J Vasc Res 2008; 45: 19-32.
27. Rommel C, Clarke BA, Zimmermann S, Nunez L, Rossman R, Reid K, Moelling K, Yancopoulos GD, Glass DJ. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 1999; 286: 1738-41, 8036 [pii].
28. Zimmermann S, Moelling K. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 1999; 286: 1741-4, 8027 [pii].
29. Zioncheck TF, Roy S, Vehar GA. The cytoplasmic domain of tissue factor is phosphorylated by a protein kinase C-dependent mechanism. J Biol Chem 1992; 267: 3561-4.
30. Hjortoe GM, Petersen LC, Albrektsen T, Sorensen BB, Norby PL, Mandal SK, Pendurthi UR, Rao LV. Tissue factor-factor VIIa-specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated by PAR-2 and results in increased cell migration. Blood 2004; 103: 3029-37.
31. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000; 407: 258-64.
32. Blair RJ, Meng H, Marchese MJ, Ren S, Schwartz LB, Tonnesen MG, Gruber BL. Human mast cells stimulate vascular tube formation. Tryptase is a novel, potent angiogenic factor. J Clin Invest 1997; 99: 2691-700.
33. Milia AF, Salis MB, Stacca T, Pinna A, Madeddu P, Trevisani M, Geppetti P, Emanueli C. Protease-activated receptor-2 stimulates angiogenesis and accelerates hemodynamic recovery in a mouse model of hindlimb ischemia. Circ Res 2002; 91: 346-52.
34. Ott I, Weigand B, Michl R, Seitz I, Sabbari-Erfani N, Neumann FJ, Schomig A. Tissue factor cytoplasmic domain stimulates migration by activation of the GTPase Rac1 and the mitogen-activated protein kinase p38. Circulation 2005; 111: 349-55.
35. Fang J, Gu L, Zhu N, Tang H, Alvarado CS, Zhou M. Tissue factor/FVIIa activates Bcl-2 and prevents doxorubicin-induced apoptosis in neuroblastoma cells. BMC Cancer 2008; 8: 69.
36. Chen J, Somanath PR, Razorenova O, Chen WS, Hay N, Bornstein P, Byzova TV. Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat Med 2005; 11: 1188-96.
37. Somanath PR, Chen J, Byzova TV. Akt1 is necessary for the vascular maturation and angiogenesis during cutaneous wound healing. Angiogenesis 2008; 11: 277-88.
38. Dhillon AS, Meikle S, Yazici Z, Eulitz M, Kolch W. Regulation of Raf-1 activation and signalling by dephosphorylation. EMBO J 2002; 21: 64-71.
39. Gessler F, Voss V, Dutzmann S, Seifert V, Gerlach R, Kogel D. Inhibition of tissue factor/protease-activated receptor-2 signaling limits proliferation, migration and invasion of malignant glioma cells. Neuroscience 2010; 165: 1312-22.
40. Ott I, Fischer EG, Miyagi Y, Mueller BM, Ruf W. A role for tissue factor in cell adhesion and migration mediated by interaction with actin-binding protein 280. J Cell Biol 1998; 140: 1241-53.
41. Melis E, Moons L, De Mol M, Herbert JM, Mackman N, Collen D, Carmeliet P, Dewerchin M. Targeted deletion of the cytosolic domain of tissue factor in mice does not affect development. Biochem Biophys Res Commun 2001; 286: 580-6.
42. Versteeg HH, Sorensen BB, Slofstra SH, Van den Brande JH, Stam JC, van Bergen en Henegouwen PM, Richel DJ, Petersen LC, Peppelenbosch MP. VIIa/tissue factor interaction results in a tissue factor cytoplasmic domain-independent activation of protein synthesis, p70, and p90 S6 kinase phosphorylation. J Biol Chem 2002; 277: 27065-72.
43. Takano S, Tsuboi K, Tomono Y, Mitsui Y, Nose T. Tissue factor, osteopontin, alphavbeta3 integrin expression in microvasculature of gliomas associated with vascular endothelial growth factor expression. Br J Cancer 2000; 82: 1967-73.
44. Zheng DQ, Woodard AS, Tallini G, Languino LR. Substrate specificity of alpha(v)beta(3) integrin-mediated cell migration and phosphatidylinositol 3-kinase/AKT pathway activation. J Biol Chem 2000; 275: 24565-74.
45. Srinivasan R, Ozhegov E, van den Berg YW, Aronow BJ, Franco RS, Palascak MB, Fallon JT, Ruf W, Versteeg HH, Bogdanov VY. Splice variants of tissue factor promote monocyte-endothelial interactions by triggering the expression of cell adhesion molecules via integrin-mediated signaling. J Thromb Haemost 2011; 9: 2087-96.