Journal of Surgical Research
Volume 169, Issue 2 , Pages 319-327 , August 2011

Factor Xa Induces Tissue Factor Expression in Endothelial Cells by P44/42 MAPK and NF-κB-Dependent Pathways

  • Rong Jiang, M.D., Ph.D.

      Affiliations

    • Cardiothoracic Research Laboratory, Division of Cardiothoracic Surgery, Carlyle Fraser Heart Center, Emory University Hospital Midtown, Atlanta, Georgia
  • ,
  • Ning-Ping Wang, M.D.

      Affiliations

    • Department of Biomedical Sciences, Mercer University School of Medicine (Savannah Campus), Atlanta, Georgia
  • ,
  • Kenichi A. Tanaka, M.D.

      Affiliations

    • Department of Anesthesiology, Emory University, Atlanta, Georgia
  • ,
  • Jerrold H. Levy, M.D.

      Affiliations

    • Department of Anesthesiology, Emory University, Atlanta, Georgia
  • ,
  • Robert A. Guyton, M.D.

      Affiliations

    • Cardiothoracic Research Laboratory, Division of Cardiothoracic Surgery, Carlyle Fraser Heart Center, Emory University Hospital Midtown, Atlanta, Georgia
  • ,
  • Zhi-Qing Zhao, Ph.D.

      Affiliations

    • Department of Biomedical Sciences, Mercer University School of Medicine (Savannah Campus), Atlanta, Georgia
  • ,
  • Jakob Vinten-Johansen, Ph.D.

      Affiliations

    • Cardiothoracic Research Laboratory, Division of Cardiothoracic Surgery, Carlyle Fraser Heart Center, Emory University Hospital Midtown, Atlanta, Georgia
    • Corresponding Author InformationTo whom correspondence and reprint requests should be addressed at Cardiothoracic Research Laboratory, Carlyle Fraser Heart Center, 550 Peachtree Street NE, Atlanta, GA 30308-2225.

Received 1 September 2009

References 

  1. Shimizu T, Nishihira J, Watanabe H, et al. Macrophage migration inhibitory factor is induced by thrombin and factor Xa in endothelial cells. J Biol Chem. 2004;279:13729
  2. Bachli EB, Pech CM, Johnson KM, et al. Factor Xa and thrombin, but not factor VIIa, elicit specific cellular responses in dermal fibroblasts. J Thromb Haemost. 2003;1:1935
  3. Hollenstein UM, Pernerstorfer T, Homoncik M, et al. Effect of factor X inhibition on coagulation activation and cytokine induction in human systemic inflammation. J Infect Disease. 2002;186:1270
  4. Liu Y, Pelekanakis K, Woolkalis MJ. Thrombin and tumor necrosis factor a synergistically stimulate tissue factor expression in human endothelial cells. J Biol Chem. 2004;279:36142
  5. Iba T, Kidokoro A, Fukunaga M, et al. Factor Xa-inhibitor (DX-9065a) modulates the leukocyte-endothelial cell interaction in endotoxemic rat. Shock. 2002;17:159
  6. Akahane K, Okamoto K, Kikuchi M, et al. Inhibition of factor Xa suppresses the expression of tissue factor in human monocytes and lipopolysaccharide-induced endotoxemia in rats. Surgery. 2001;130:809
  7. Herault JP, Bono F, Avril C, et al. Activation of human vascular endothelial cells by factor Xa: Effect of specific inhibitors. Biochem Pharmacol. 1999;57:603
  8. McLean K, Schirm S, Johns A, et al. FXa-induced responses in vascular wall cells are PAR-mediated and inhibited by ZK-807834. Thromb Res. 2001;103:281
  9. Senden NHM, Jeunhomme TMAA, Heemskerk JWM, et al. Factor Xa induces cytokine production and expression of adhesion molecules by human umbilical vein endothelial cells. J Immunol. 1998;161:4318
  10. Buschi G, Seitz I, Steppich B, et al. Coagulation factor Xa stimulates interleukin-8 release in endothelial cells and mononuclear leukocytes implications in acute myocardial infarction. Arterioscler Thromb Vasc Biol. 2005;25:1
  11. Jaffe EA, Nechman RL, Becker CG, et al. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest. 1973;52:2745
  12. Nishibe T, Parry G, Ishida A, et al. Oncostatin M promotes biphasic tissue factor expression in smooth muscle cells: Evidence for Erk-1/2 activation. Blood. 2001;97:692
  13. Oeth P, Parry GC, Mackman N. Regulation of the tissue factor gene in human monocytic cells: Role of AP-1, NF-κB/Rel, and Sp1 proteins in uninduced and lipopolysaccharide-induced expression. Arterioscler Thromb Vasc Biol. 1997;17:365
  14. Blum S, Issbruker K, Willuweit A, et al. An inhibitory role of the phosphatidylinositol 3-kinase-signaling pathway in vascular endothelial growth factor-induced tissue factor expression. J Biol Chem. 2001;276:33428
  15. Matsumoto Y, Kawai Y, Watanabe K, et al. Fluid shear stress attenuates tumor necrosis factor-a-induced tissue factor expression in cultured human endothelial cells. Blood. 1998;91:4164
  16. Krishnaswamy S, Walker RK. Contribution of the prothrombin fragment 2 domain to the function of factor Va in the prothrombinase complex. Biochemistry. 1997;36:3319
  17. Ghosh S, Karin M. Missing pieces in the NF-κB puzzle. Cell. 2002;109:S81
  18. Boyle EM, Verrier ED, Spiess BD. Endothelial cell injury in cardiovascular surgery: The procoagulant response. Ann Thorac Surg. 1996;62:1549
  19. Pruefer D, Makowski J, Dahm M, et al. Aprotinin inhibits leukocyte-endothelial cell interactions after hemorrhage and reperfusion. Ann Thorac Surg. 2003;75:210
  20. Pruefer D, Buerke U, Khalili M, et al. Cardioprotective effects of the serine protease inhibitor aprotinin after regional ischemia and reperfusion on the beating heart. J Thorac Cardiovasc Surg. 2002;124:942
  21. Reeves JG, Jiang R, Mykytenko J, et al. Inhibition of serine protease activity at reperfusion reduces postischemic injury in a closed-chest model of acute myocardial infarction. JACC. 2006;47:170A
  22. Kubes P, Jutila M, Payne D. Therapeutic potential of inhibiting leukocyte rolling in ischemia/reperfusion. J Clin Invest. 1995;95:2510
  23. Ley K. Molecular mechanisms of leukocyte recruitment in the inflammatory process. Cardiovasc Res. 1996;32:733
  24. Kranzhöfer R, Clinton SK, Ishii K, et al. Thrombin potently stimulates cytokine production in human vascular smooth muscle cells but not in mononuclear phagocytes. Circ Res. 1996;79:286
  25. Nicholson AC, Nachman RL, Altieri DC, et al. Effector cell protease receptor-1 is a vascular receptor for coagulation factor Xa. J Biol Chem. 1996;271:28407
  26. Eto M, Kozai T, Cosentino F, et al. Statin prevents tissue factor expression in human endothelial cells role of Rho/Rho-kinase and Akt pathways. Circulation. 2002;105:1756
  27. Mackman N. Regulation of the tissue factor gene. FASEB. 1995;9:883
  28. Parry GC, Mackman N. Transcriptional regulation of tissue factor expression in human endothelial cells. Arterioscler Thromb Vasc Biol. 1995;15:612
  29. Parry GC, Mackman N. A set of inducible genes expressed by activated human monocytic and endothelial cells contain kappa B-like sites that specifically bind c-Rel-p65 heterodimers. J Biol Chem. 1994;269:20823
  30. Houston P, Dickson MC, Ludbrook V, et al. Fluid shear stress induction of the tissue factor promoter in vitro and in vivo is mediated by Egr-1. Arteriosclerosis Thromb Vasc Biol. 1999;19:281
  31. Hausenloy DJ, Tsang A, Yellon DM. The reperfusion injury salvage kinase pathway: A common target for both ischemic preconditioning and postconditioning. TCM. 2005;15:69
  32. Tsang A, Hausenloy DJ, Mocanu MM, et al. Postconditioning: A form of “modified reperfusion” protects the myocardium by activating the phosphatidylinositol 3-kinase-Akt pathway. Circ Res. 2004;95:230
  33. Darling CE, Jiang R, Maynard M, et al. Postconditioning via stuttering reperfusion limits myocardial infarct size in rabbit hearts: Role of ERK1/2. Am J Physiol (Heart Circ Physiol). 2005;289:H1618
  34. Riewald M, Kravchenko VV, Petrovan RJ, et al. Gene induction by coagulation factor Xa is mediated by activation of protease-activated receptor 1. Blood. 2001;97:3109
  35. Bono F, Schaeffer P, Herault JP, et al. Factor Xa activates endothelial cells by a receptor cascade between EPR-1 and PAR-2. Arterioscl Thromb Vasc Biol. 2000;20:E107
  36. Daubie V, Cauwenberghs S, Senden NH, et al. Factor Xa and thrombin evoke additive calcium and proinflammatory responses in endothelial cells subjected to coagulation. Biochim Biophys Acta. 2006;1763:860
  37. Moons AHM, Levi M, Peters RJG. Tissue factor and coronary artery disease. Cardiovasc Res. 2002;53:313
  38. Reganon E, Vila V, Martinez-Sales V, et al. Inflammation, fibrinogen and thrombin generation in patients with previous myocardial infarction. Haematologica. 2002;87:740
  39. Roldan V, Marin F, Fernandez P, et al. Tissue factor/tissue factor pathway inhibitor system and long-term prognosis after acute myocardial infarction. Int J Cardiol. 2001;78:115

PII: S0022-4804(10)00093-4

doi: 10.1016/j.jss.2010.01.041

Journal of Surgical Research
Volume 169, Issue 2 , Pages 319-327 , August 2011