Independent Anti-Angiogenic Capacities of Coagulation Factors X and Xa

Journal of Cellular Physiology

Volumn 229, Issue 11, 2014, Pages 1673-1680

  Lange, Soledad ^a   Gonzalez, Ibeth ^a   Pinto, Mauricio P ^a   Arce, Maximiliano ^a   Valenzuela, Rodrigo ^a   Aranda, Evelyn ^a   Elliot, Matias ^b   Alvarez, Marjorie ^b   Henriquez, Soledad ^a   Velasquez, Ethel V ^a   Orge, Felipe ^a   Oliva, Barbara ^a   Gonzalez, Pamela ^a   Villalon, Manuel ^a   Cautivo, Kelly M ^c   Kalergis, Alexis M ^c,d,e   Pereira, Karla ^d   Mendoza, Camila ^d   Saez, Claudia ^d   Kato, Sumie ^d   Cuello, Mauricio A ^d   Parborell, Fernanda ^f   Irusta, Griselda ^f   Palma, Veronica ^b   Allende, Miguel L ^b   Owen, Gareth I ^a,e   more..

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c Pontificia Universidad Católica de Chile   (Chile)

^d PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^e Biomedical Research Consortium (BMRC) Chile   (Chile)

^f INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING INHIBITOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; RECOMBINANT BLOOD CLOTTING FACTOR X; RIVAROXABAN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL DEATH; CELL MIGRATION; CELL VIABILITY; CHORIOALLANTOIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CHICK EMBRYO; FACTOR X; FACTOR XA; HELMINTH PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTOR, PAR-1; ZEBRAFISH;

EID: 84904893895     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24612     Document Type: Article

References (51)

1. Al-Ani B, Saifeddine M, Wijesuriya SJ, Hollenberg MD. 2002. Modified proteinase-activated receptor-1 and -2 derived peptides inhibit proteinase-activated receptor-2 activation by trypsin. J Pharmacol Exp Ther 300:702-708.
2. Aranda E, Owen GI. 2009. A semi-quantitative assay to screen for angiogenic compounds and compounds with angiogenic potential using the EA. hy926 endothelial cell line. Biol Res 42:377-389.
3. Bae JS, Yang L, Rezaie AR. 2010. Factor X/Xa elicits protective signaling responses in endothelial cells directly via PAR-2 and indirectly via endothelial protein C receptor-dependent recruitment of PAR-1. J Biol Chem 285:34803-34812.
4. Bergum PW, Cruikshank A, Maki SL, Kelly CR, Ruf W, Vlasuk GP. 2001. Role of zymogen and activated factor X as scaffolds for the inhibition of the blood coagulation factor VIIa-tissue factor complex by recombinant nematode anticoagulant protein c2. J Biol Chem 276:10063-10071.
5. Bohm SK, Kong W, Bromme D, Smeekens SP, Anderson DC, Connolly A, Kahn M, Nelken NA, Coughlin SR, Payan DG, Bunnett NW. 1996. Molecular cloning, expression and potential functions of the human proteinase-activated receptor-2. Biochem J 314:1009-1016.
6. Borensztajn KS, Spek CA. 2008. Protease-activated receptors, apoptosis and tumor growth. Pathophysiol Haemost Thromb 36:137-147.
7. Borensztajn K, Aberson H, Peppelenbosch MP, Spek CA. 2009a. FXa-induced intracellular signaling links coagulation to neoangiogenesis: Potential implications for fibrosis. Biochim Biophys Acta 1793:798-805.
8. Borensztajn K, Bijlsma MF, Reitsma PH, Peppelenbosch MP, Spek CA. 2009b. Coagulation factor Xa inhibits cancer cell migration via protease-activated receptor-1 activation. Thromb Res 124:219-225.
9. Browder T, Folkman J, Pirie-Shepherd S. 2000. The hemostatic system as a regulator of angiogenesis. J Biol Chem 275:1521-1524.
10. Camerer E, Rottingen JA, Gjernes E, Larsen K, Skartlien AH, Iversen JG, Prydz H. 1999. Coagulation factors VIIa and Xa induce cell signaling leading to up-regulation of the egr-1 gene. J Biol Chem 274:32225-32233.
11. Chan B, Merchan JR, Kale S, Sukhatme VP. 2003. Antiangiogenic property of human thrombin. Microvasc Res 66:1-14.
12. Connolly AJ, Ishihara H, Kahn ML, Farese RV, Jr., Coughlin SR. 1996. Role of the thrombin receptor in development and evidence for a second receptor. Nature 381:516-519.
13. Coughlin SR. 2000. Thrombin signalling and protease-activated receptors. Nature 407:258-264.
14. Dewerchin M, Liang Z, Moons L, Carmeliet P, Castellino FJ, Collen D, Rosen ED. 2000. Blood coagulation factor X deficiency causes partial embryonic lethality and fatal neonatal bleeding in mice. Thromb Haemost 83:185-190.
15. Diaz J, Aranda E, Henriquez S, Quezada M, Espinoza E, Bravo ML, Oliva B, Lange S, Villalon M, Jones M, Brosens JJ, Kato S, Cuello MA, Knutson TP, Lange CA, Leyton L, Owen GI. 2012. Progesterone promotes focal adhesion formation and migration in breast cancer cells through induction of protease-activated receptor-1. J Endocrinol 214:165-175.
16. Dow JK, deVere White RW. 2000. Fibroblast growth factor 2: Its structure and property, paracrine function, tumor angiogenesis, and prostate-related mitogenic and oncogenic functions. Urology 55:800-806.
17. Edgell CJ, McDonald CC, Graham JB. 1983. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci USA 80:3734-3737.
18. Feistritzer C, Lenta R, Riewald M. 2005. Protease-activated receptors-1 and -2 can mediate endothelial barrier protection: Role in factor Xa signaling. J Thromb Haemost 3:2798-2805.
19. Furie B, Furie BC. 1988. The molecular basis of blood coagulation. Cell 53:505-518.
20. Girolami A, Ruzzon E, Tezza F, Scandellari R, Scapin M, Scarparo P. 2008. Congenital FX deficiency combined with other clotting defects or with other abnormalities: A critical evaluation of the literature. Haemophilia 14:323-328.
21. Gulseth MP, Michaud J, Nutescu EA. 2008. Rivaroxaban: An oral direct inhibitor of factor Xa. Am J Health Syst Pharm 65:1520-1529.
22. Haralabopoulos GC, Grant DS, Kleinman HK, Maragoudakis ME. 1997. Thrombin promotes endothelial cell alignment in Matrigel in vitro and angiogenesis in vivo. Am J Physiol 273:C239-C245.
23. Herbert J, Bono F, Herault J, Avril C, Dol F, Mares A, Schaeffer P. 1998. Effector protease receptor 1 mediates the mitogenic activity of factor Xa for vascular smooth muscle cells in vitro and in vivo. J Clin Investig 101:993-1000.
24. Hollenberg MD, Yang SG, Laniyonu AA, Moore GJ, Saifeddine M. 1992. Action of thrombin receptor polypeptide in gastric smooth muscle: Identification of a core pentapeptide retaining full thrombin-mimetic intrinsic activity. Mol Pharmacol 42:186-191.
25. Isogai S, Horiguchi M, Weinstein BM. 2001. The vascular anatomy of the developing zebrafish: An atlas of embryonic and early larval development. Dev Biol 230:278-301.
26. Jaffe EA, Nachman RL, Becker CG, Minick CR. 1973. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Investig 52:2745-2756.
27. Kato S, Pinto M, Carvajal A, Espinoza N, Monso C, Sadarangani A, Villalon M, Brosens JJ, White JO, Richer JK, Horwitz KB, Owen GI. 2005. Progesterone increases tissue factor gene expression, procoagulant activity, and invasion in the breast cancer cell line ZR-75-1. J Clin Endocrinol Metab 90:1181-1188.
28. Kato S, Sadarangani A, Lange S, Villalon M, Branes J, Brosens JJ, Owen GI, Cuello M. 2007. The oestrogen metabolite 2-methoxyoestradiol alone or in combination with tumour necrosis factor-related apoptosis-inducing ligand mediates apoptosis in cancerous but not healthy cells of the human endometrium. Endocr Relat Cancer 14:351-368.
29. Kurz H, Fehr J, Nitschke R, Burkhardt H. 2008. Pericytes in the mature chorioallantoic membrane capillary plexus contain desmin and alpha-smooth muscle actin: Relevance for non-sprouting angiogenesis. Histochem Cell Biol 130:1027-1040.
30. Lawson ND, Weinstein BM. 2002. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307-318.
31. Lee AY, Vlasuk GP. 2003. Recombinant nematode anticoagulant protein c2 and other inhibitors targeting blood coagulation factor VIIa/tissue factor. J Intern Med 254:313-321.
32. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. 2001. Proteinase-activated receptors. Pharmacol Rev 53:245-282.
33. McLaughlin JN, Shen L, Holinstat M, Brooks JD, Dibenedetto E, Hamm HE. 2005. Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. J Biol Chem 280:25048-25059.
34. Nico B, Ennas MG, Crivellato E, Frontino A, Mangieri D, De Giorgis M, Roncali L, Ribatti D. 2004. Desmin-positive pericytes in the chick embryo chorioallantoic membrane in response to fibroblast growth factor-2. Microvasc Res 68:13-19.
35. O'Brien PJ, Molino M, Kahn M, Brass LF. 2001. Protease activated receptors: Theme and variations. Oncogene 20:1570-1581.
36. Ossovskaya VS, Bunnett NW. 2004. Protease-activated receptors: Contribution to physiology and disease. Physiol Rev 84:579-621.
37. Quezada M, Alvarez M, Pena OA, Henriquez S, d'Alencon CA, Lange S, Oliva B, Owen GI, Allende ML. 2013. Antiangiogenic, antimigratory and antiinflammatory effects of 2-methoxyestradiol in zebrafish larvae. Comp Biochem Physiol Toxicol Pharmacol 157:141-149.
38. Rao LV, Pendurthi UR. 2005. Tissue factor-factor VIIa signaling. Arterioscler Thromb Vasc Biol 25:47-56.
39. Riewald M, Kravchenko VV, Petrovan RJ, O'Brien PJ, Brass LF, Ulevitch RJ, Ruf W. 2001. Gene induction by coagulation factor Xa is mediated by activation of protease-activated receptor 1. Blood 97:3109-3116.
40. Robinson RS, Woad KJ, Hammond AJ, Laird M, Hunter MG, Mann GE. 2009. Angiogenesis and vascular function in the ovary. Reproduction 138:869-881.
41. Rosen ED. 2002. Gene targeting in hemostasis. Factor X. Front Biosci 7:d1915-d1925.
42. Rupprecht HJ, Blank R. 2010. Clinical pharmacology of direct and indirect factor Xa inhibitors. Drugs 70:2153-2170.
43. Santoro MM, Pesce G, Stainier DY. 2009. Characterization of vascular mural cells during zebrafish development. Mech Dev 126:638-649.
44. Schuepbach RA, Riewald M. 2010. Coagulation factor Xa cleaves protease-activated receptor-1 and mediates signaling dependent on binding to the endothelial protein C receptor. J Thromb Haemost 8:379-388.
45. Senden NH, Jeunhomme TM, Heemskerk JW, Wagenvoord R. 1998. Van't Veer C, Hemker HC, Buurman WA.. Factor Xa induces cytokine production and expression of adhesion molecules by human umbilical vein endothelial cells. J Immunol 161:4318-4324.
46. Serbedzija GN, Flynn E, Willett CE. 1999. Zebrafish angiogenesis: A new model for drug screening. Angiogenesis 3:353-359.
47. Tsigkos S, Koutsilieris M, Papapetropoulos A. 2003. Angiopoietins in angiogenesis and beyond. Expert Opin Investig Drugs 12:933-941.
48. Vassallo RR, Jr., Kieber-Emmons T, Cichowski K, Brass LF. 1992. Structure-function relationships in the activation of platelet thrombin receptors by receptor-derived peptides. J Biol Chem 267:6081-6085.
49. Veikkola T, Karkkainen M, Claesson-Welsh L, Alitalo K. 2000. Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Res 60:203-212.
50. Versteeg HH, Peppelenbosch MP, Spek CA. 2003. Tissue factor signal transduction in angiogenesis. Carcinogenesis 24:1009-1013.
51. Wang B, Pearson T, Manning G, Donnelly R. 2010. In vitro study of thrombin on tubule formation and regulators of angiogenesis. Clin Appl Thromb Hemost 16:674-678.