Thrombosis Research
Volume 125 , Pages S57-S59 , April 2010

Interdependent biological systems, multi-functional molecules: The evolving role of tissue factor pathway inhibitor beyond anti-coagulation

  • Eric W. Holroyd
    • ,
  • Robert D. Simari

      Affiliations

    • Corresponding Author InformationCorresponding author. Mayo Clinic, Division of Cardiovascular Diseases, 200 First Street SW, Rochester, Minnesota, 55905, USA. Tel.: +1 507 284 3727; fax: +1 507 538 6418.

References 

  1. Davidson CJ, Tuddenham EG, McVey JH. 450 million years of hemostasis. J Thromb Haemost. 2003 Jul;1(7):1487–1494
  2. Broze G, Warren L, Novotny W, Higuchi D, Girard J, Miletich J. The lipoprotein-associated coagulation inhibitor that inhibits factor Xa: insight into its possible mechanism of action. Blood. 1988;71:335–343
  3. Girard T, Warren L, Novotny W, Likert K, Brown S, Miletich J. G.J. Broze J. Functional significance of the Kunitz-type inhibitory domains of lipoprotein-associated coagulation inhibitor. Nature. 1989;338:518–520
  4. Vincent JL. Infection/inflammation and hemostasis. Curr Hematol Rep. 2003 Sep;2(5):407–410
  5. Schoenmakers SH, Reitsma PH, Spek CA. Blood coagulation factors as inflammatory mediators. Blood Cells Mol Dis. Jan-Feb 2005;34(1):30–37
  6. Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis. Am J Pathol. May 1989;134(5):1087–1097
  7. Rivers RP, Hathaway WE, Weston WL. The endotoxin-induced coagulant activity of human monocytes. Br J Haematol. 1975 Jul;30(3):311–316
  8. Prydz H, Allison AC, Schorlemmer HU. Further link between complement activation and blood coagulation. Nature. 1977 Nov 10;270(5633):173–174
  9. Versteeg HH, Peppelenbosch MP, Spek CA. The pleiotropic effects of tissue factor: a possible role for factor VIIa-induced intracellular signalling?. Thromb Haemost. 2001 Dec;86(6):1353–1359
  10. Ruf W, Dorfleutner A, Riewald M. Specificity of coagulation factor signaling. J Thromb Haemost. 2003 Jul;1(7):1495–1503
  11. Pawlinski R, Pedersen B, Schabbauer G, Tencati M, Holscher T, Boisvert W, et al. Role of tissue factor and protease-activated receptors in a mouse model of endotoxemia. Blood. 2004 Feb 15;103(4):1342–1347
  12. Taylor FB, Chang A, Ruf W, Morrissey JH, Hinshaw L, Catlett R, et al. Lethal E. coli septic shock is prevented by blocking tissue factor with monoclonal antibody. Circ Shock. Mar 1991;33(3):127–134
  13. Opal SM, Palardy JE, Parejo NA, Creasey AA. The activity of tissue factor pathway inhibitor in experimental models of superantigen-induced shock and polymicrobial intra-abdominal sepsis. Crit Care Med. 2001 Jan;29(1):13–17
  14. Carr C, Bild GS, Chang AC, Peer GT, Palmier MO, Frazier RB, et al. Recombinant E. coli-derived tissue factor pathway inhibitor reduces coagulopathic and lethal effects in the baboon gram-negative model of septic shock. Circ Shock. Nov 1994;44(3):126–137
  15. Abraham E, Reinhart K, Opal S, Demeyer I, Doig C, Rodriguez AL, et al. Efficacy and safety of tifacogin (recombinant tissue factor pathway inhibitor) in severe sepsis: a randomized controlled trial. JAMA. 2003 Jul 9;290(2):238–247
  16. Ohkura N, Enjyoji K-I, Kamikubo Y-I, Kato H. A novel degradation pathway of tissue factor pathway inhibitor: incorporation into fibrin clot and degradation by thrombin. Blood. 1997;90:1883–1892
  17. Schirm S, Liu X, Jennings LL, Jedrzejewski P, Dai Y, Hardy S. Fragmented tissue factor pathway inhibitor (TFPI) and TFPI C-terminal peptides eliminate serum-resistant Escherichia coli from blood cultures. J Infect Dis. 2009 Jun 15;199(12):1807–1815
  18. Ruf W, Fischer EG, Huang HY, Miyagi Y, Ott I, Riewald M, et al. Diverse functions of protease receptor tissue factor in inflammation and metastasis. Immunol Res. 2000;21(2–3):289–292
  19. Mueller B, Ruf W. Requirement for binding of catalytically active factor VIIa in tissue factor-dependent experimental metastasis. J Clin Invest. 1998;101:1372–1378
  20. Contrino J, Hair G, Kreutzer D, Rickles F. In situ detection of tissue factor in vascular endothelial cells: Correlation with the malignant phenotype of human breast disease. Nature Med. 1996;2:209–215
  21. Uusitalo-Jarvinen H, Kurokawa T, Mueller BM, Andrade-Gordon P, Friedlander M, Ruf W. Role of protease activated receptor 1 and 2 signaling in hypoxia-induced angiogenesis. Arterioscler Thromb Vasc Biol. 2007 Jun;27(6):1456–1462
  22. Versteeg HH, Schaffner F, Kerver M, Petersen HH, Ahamed J, Felding-Habermann B, et al. Inhibition of tissue factor signaling suppresses tumor growth. Blood. 2008 Jan 1;111(1):190–199
  23. Belting M, Dorrell MI, Sandgren S, Aguilar E, Ahamed J, Dorfleutner A, et al. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat Med. 2004 May;10(5):502–509
  24. Ahamed J, Belting M, Ruf W. Regulation of tissue factor-induced signaling by endogenous and recombinant tissue factor pathway inhibitor 1. Blood. Mar 15 2005;105(6):2384–2391
  25. Hembrough TA, Swartz GM, Papathanassiu A, Vlasuk GP, Rote WE, Green SJ, et al. Tissue factor/factor VIIa inhibitors block angiogenesis and tumor growth through a nonhemostatic mechanism. Cancer Res. 2003 Jun 1;63(11):2997–3000
  26. Hembrough TA, Ruiz JF, Papathanassiu AE, Green SJ, Strickland DK. Tissue factor pathway inhibitor inhibits endothelial cell proliferation via association with the very low density lipoprotein receptor. J Biol Chem. 2001;276:12241–12248
  27. Hembrough TA, Ruiz JF, Swerdlow BM, Swartz GM, Hammers HJ, Zhang L, et al. Identification and characterization of a very low density lipoprotein receptor-binding peptide from tissue factor pathway inhibitor that has antitumor and antiangiogenic activity. Blood. May 1 2004;103(9):3374–33802004
  28. Bajaj MS, Birktoft JJ, Steer SA, Bajaj SP. Structure and biology of tissue factor pathway inhibitor. Thromb Haemost. 2001 Oct;86(4):959–972
  29. Provencal M, Michaud M, Beaulieu E, Ratel D, Rivard GE, Gingras D, et al. Tissue factor pathway inhibitor (TFPI) interferes with endothelial cell migration by inhibition of both the Erk pathway and focal adhesion proteins. Thromb Haemost. 2008 Mar;99(3):576–585
  30. Channon KM. The Endothelium and the Pathogenesis of Atherosclerosis. Medicine. 2002;30(4):54–58
  31. Moreno PR, Purushothaman KR, Fuster V, Echeverri D, Truszczynska H, Sharma SK, et al. Plaque neovascularization is increased in ruptured therosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation. 2004 Oct 5;110(14):2032–2038
  32. Wun TC, Kretzmer KK, Girard TJ, Miletich JP, Broze GJ. Cloning and characterization of a cDNA coding for the lipoprotein-associated coagulation inhibitor shows that it consists of three tandem Kunitz-type inhibitory domains. J Biol Chem. 1988 May 5;263(13):6001–6004
  33. Novotny W, Girard T, Miletich J, Broze G. Purification and characterization of the lipoprotein-associated coagulation inhibitor from human plasma. J Biol Chem. 1989;264:18832–18837
  34. Warshawsky I, GJ Broze J, Schwartz A. The low density lipoprotein receptor-related protein mediates the cellular degradation of tissue factor pathway inhibitor. Proc Natl Acad Sci USA. 1994;91:6664–6668
  35. Narita M, Bu G, Olins G, Higuchi D, Herz J. GJ Broze J, Schwartz A. Two receptor systems are involved in the plasma clearance of tissue factor pathway inhibitor in vivo. J Biol Chem. 1995;270(42):24800–24804
  36. Horie S, Hiraishi S, Hamuro T, Kamikubo Y, Matsuda J. Oxidized low-density lipoprotein associates strongly with carboxy-terminal domain of tissue factor pathway inhibitor and reduces the catalytic activity of the protein. Thromb Haemost. 2002 Jan;87(1):80–85
  37. Ohkura N, Hiraishi S, Itabe H, Hamuro T, Kamikubo Y, Takano T, et al. Oxidized phospholipids in oxidized low-density lipoprotein reduce the activity of tissue factor pathway inhibitor through association with its carboxy-terminal region. Antioxid Redox Signal. 2004 Aug;6(4):705–712
  38. Singh R, Pan S, Mueske CS, Witt T, Kleppe LS, Peterson TE, et al. Role for tissue factor pathway in murine model of vascular remodeling. Circ Res. 2001 Jul 6;89(1):71–76
  39. Pan S, Kleppe LS, Witt TA, Mueske CS, Simari RD. The effect of vascular smooth muscle cell-targeted expression of tissue factor pathway inhibitor in a murine model of arterial thrombosis. Thromb Haemost. 2004 Sep;92(3):495–502
  40. Westrick RJ, Bodary PF, Xu Z, Shen YC, Broze GJ, Eitzman DT. Deficiency of tissue factor pathway inhibitor promotes atherosclerosis and thrombosis in mice. Circulation. 2001 Jun 26;103(25):3044–3046
  41. Singh R, Pan S, Mueske CS, Witt TA, Kleppe LS, Peterson TE, et al. Tissue factor pathway inhibitor deficiency enhances neointimal proliferation and formation in a murine model of vascular remodeling. Thromb Haemost. 2003;89:747–751
  42. Pan S, White TA, Witt TA, Chiriac A, Mueske CS, Simari RD. Vascular-directed tissue factor pathway inhibitor overexpression regulates plasma cholesterol and reduces atherosclerotic plaque development. Circ Res. Sep 25 2009;105(7):713–7208 p following 20

PII: S0049-3848(10)00092-7

doi: 10.1016/j.thromres.2010.01.039

Thrombosis Research
Volume 125 , Pages S57-S59 , April 2010

Article Tools