Neutrophil activation by the tissue factor/Factor VIIa/PAR2 axis mediates fetal death in a mouse model of antiphospholipid syndrome

Journal of Clinical Investigation

Volumn 118, Issue 10, 2008, Pages 3453-3461

  Redecha, Patricia ^a   Franzke, Claus Werner ^a   Ruf, Wolfram ^b   Mackman, Nigel ^c   Girardi, Guillermina ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 7A; PHOSPHOLIPID ANTIBODY; PRAVASTATIN; PROTEINASE ACTIVATED RECEPTOR 2; SIMVASTATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPHOSPHOLIPID SYNDROME; ARTICLE; BLOOD CLOTTING; CELL DAMAGE; CONTROLLED STUDY; CYTOPLASM; FEMALE; FETUS DEATH; GENE DELETION; LEUKOCYTE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE INJURY;

ANIMALS; ANTIBODIES, ANTIPHOSPHOLIPID; ANTIPHOSPHOLIPID SYNDROME; DISEASE MODELS, ANIMAL; FACTOR VIIA; FEMALE; FETAL DEATH; GENE DELETION; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULIN G; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL ACTIVATION; NEUTROPHILS; PHAGOCYTOSIS; PREGNANCY; REACTIVE OXYGEN SPECIES; RECEPTOR, PAR-1; RECEPTOR, PAR-2; RESPIRATORY BURST; SIGNAL TRANSDUCTION; SIMVASTATIN; THROMBOPLASTIN;

EID: 55849112296     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI36089     Document Type: Article

References (54)

1. Redecha, P., et al. 2007. Tissue factor: a link between C5a and neutrophil activation in antiphospholipid antibody induced fetal injury. Blood. 110:2423-2431.
2. Monroe, D.M., and Key, N.S. 2007. The tissue factor-factor VIIa complex: procoagulant activity, regulation, and multitasking. J. Thromb. Haemost. 5:1097-1105.
3. Strukova, S. 1006. Blood coagulation-dependent inflammation. Coagulation-dependent inflammation and inflammation-dependent thrombosis. Front. Biosci. 11:59-80.
4. Camerer, E., Huang, W., Coughlin, S.R. 2000. Tissue factor- and factor X-dependent activation of protease-activated receptor 2 by factor VIIa. Proc. Natl. Acad. Sci. U. S. A. 97:5255-5260.
5. Ruf, W., Dorfleutner, A., and Riewald, M. 2003. Specificity of coagulation factor signaling. J. Thromb. Haemost. 1:1495-1503.
6. Lindner, J.R., et al. 2000. Delayed onset of inflammation in protease-activated receptor-2-deficient mice. J. Immunol. 165:6504-6510.
7. Zimmerman, B.J., et al. 1994. Thrombin receptor peptide-mediated leukocyte rolling in rat mesenteric venules: roles of P-selectin and sialyl Lewis X. Am. J. Physiol. 267:H1049-H1053.
8. Erlich, J.H., et al. 2000. Inhibition of the tissue factor-thrombin pathway limits infarct size after myocardial ischemia-reperfusion injury by reducing inflammation. Am. J. Pathol. 157:1849-1862.
9. Sevastos, J., et al. 2007. Tissue factor deficiency and PAR-1 deficiency are protective against renal ischemia reperfusion injury. Blood. 109:577-583.
10. Stone, S., et al. 2006. The placental bed in pregnancies complicated by primary antiphospholipid syndrome. Placenta. 27:457-467.
11. Holers, V.M., et al. 2003. Complement C3 activation is required for antiphospholipid antibody-induced fetal loss. J. Exp. Med. 195:211-220.
12. Girardi, G., et al. 2004. Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J. Clin. Invest. 112:1644-1654.
13. Girardi, G., Redecha, P., and Salmon, J.E. 2004. Heparin prevents antiphospholipid antibody-induced fetal loss by inhibiting complement activation. Nat. Med. 10:1222-1226.
14. Versteeg, H.H. 2008. Inhibition of tissue factor signaling suppresses tumor growth. Blood. 111:190-199.
15. Pawlinski, R., et al. 2007. Role of cardiac myocyte tissue factor in heart hemostasis. J. Thromb. Haemost. 5:1693-1700.
16. Ahamed, J., et al. 2007. Regulation of macrophage procoagulant responses by the tissue factor cytoplasmic domain in endotoxemia. Blood. 109:5251-5259.
17. Takemoto, M., and Liao, J.K. 2001. Pleiotropic effects of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Arterioscler. Thromb. Vasc. Biol. 21:1712-1719.
18. Wei, J.L., Cui, H.M., and Ma, C.Y. 2007. Simvastatin inhibits tissue factor and plasminogen activator inhibitor-1 secretion by peripheral blood mononuclear cells in patients with primary nephrotic syndrome. Eur. J. Med. Res. 12:216-221.
19. Pierangeli, S.S., and Ferrara, D.E. 2005. More on: fluvastatin inhibits up-regulation of tissue factor expression by antiphospholipid antibodies on endothelial cells. J. Thromb. Haemost. 3:1112-1113.
20. Kunieda, Y., et al. 2003. HMG CoA reductase inhibitor suppresses the expression of tissue factor and plasminogen activator inhibitor-1 induced by angiotensin II in cultured rat aortic endothelial cells. Thromb. Res. 110:227-234.
21. Volanakis, J.E., and Frank, M. 1998. The human complement system in health and disease. Dekker. New York, New York, USA. 672 pp.
22. Lambris, J.D. 1990. The third component of complement: chemistry and biology. Springer Verlag. Berlin, Germany. 251 pp.
23. Sun, X., et al. 1999. Role of decay-accelerating factor in regulating complement activation on the erythrocyte surface as revealed by gene targeting. Proc. Natl. Acad. Sci. U. S. A. 96:628-633.
24. Mason, J.C., et al. 2002. Statin-induced expression of decay-accelerating factor protects vascular endothelium against complement-mediated injury. Circ. Res. 91:696-703.
25. Edison, R.J., and Muenke, M. 2005. Mechanistic and epidemiologic considerations in the evaluation of adverse birth outcomes following gestational exposure to statins. Am. J. Med. Genet. A. 135:230-231.
26. Rosenson, R., and Tangney, C. 1998. Antiatherosclerotic properties of statins. JAMA. 279:1643-1650.
27. Kubes, P., Suzuki, M., and Granger, D.N. 1991. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. U. S. A. 88:4651-4655.
28. Bunnett, N.W. 2006. Protease-activated receptors: how proteases signal to cells to cause inflammation and pain. Semin. Thromb. Hemost. 32:39-48.
29. Versteeg, H.H., and Ruf, W. 2006. Emerging insights in tissue factor-dependent signaling events. Semin. Thromb. Hemost. 32:24-32.
30. Nakamura, S., Imamura, T., and Okamoto, K. 2004. Tissue factor in neutrophils: yes. J. Thromb. Haemost. 2:214-217.
31. Østerud, B. 2004. Tissue factor in neutrophils: no. J. Thromb. Haemost. 2:218-220.
32. Ritis, K., et al. 2006. A novel C5a receptor-tissue factor cross-talk in neutrophils links innate immunity to coagulation pathways. J. Immunol. 177:4794-4802.
33. Howells, G.L., et al. 1997. Proteinase-activated receptor-2: expression by human neutrophils. J. Cell Sci. 110:881-887.
34. Shpacovitch, V.M., et al. 2007. Agonists of proteinase-activated receptor-2 affect transendothelial migration and apoptosis of human neutrophils. Exp. Dermatol. 16:799-806.
35. Moraes, T.J., et al. 2008. Role of PAR2 in murine pulmonary pseudomonal infection. Am. J. Physiol. Lung Cell Mol. Physiol. 294:L368-L377.
36. Fischer, E.G., Ruf, W., and Mueller, B.M. 1995. Tissue factor-initiated thrombin generation activates the signaling thrombin receptor on malignant melanoma cells. Cancer Res. 55:1629-1632.
37. Mueller, B.M., Reisfeld, R.A., Edgington, T.S., and Ruf, W. 1992. Expression of tissue factor by melanoma cells promotes efficient hematogenous metastasis. Proc. Natl. Acad. Sci. U. S. A. 89:11832-11836.
38. Yang, Y.H., et al. 2004. Reduction in arthritis severity and modulation of immune function in tissue factor cytoplasmic domain mutant mice. Am. J. Pathol. 164:109-117.
39. Uusitalo-Jarvinen, H., et al. 2007. Role of protease activated receptor 1 and 2 signaling in hypoxia-induced angiogenesis. Arterioscler. Thromb. Vasc. Biol. 27:1456-1462.
40. O'Brien, P.J. 2003. Thrombin receptors and protease-activated receptor-2 in human placentation: receptor activation mediates extravillous trophoblast invasion in vitro. Am. J. Pathol. 163:1245-1254.
41. Isermann, B., et al. 2003. The thrombomodulin-protein C system is essential for the maintenance of pregnancy. Nat. Med. 9:331-337.
42. Paraskevas, K.I., Tzovaras, A.A., Briana, D.D., and Mikhailidis, D.P. 2007. Emerging indications for statins: a pluripotent family of agents with several potential applications. Curr. Pharm. Des. 13:3622-3636.
43. Aberg, M., Wickström, M., and Siegbahn, A. 2008. Simvastatin induces apoptosis in human breast cancer cells in a NFkappaB-dependent manner and abolishes the anti-apoptotic signaling of TF/FVIIa and TF/FVIIa/FXa. Thromb. Res. 122:191-202.
44. Broz, P., et al. 2008. Inhibition of macrophage phagocytotic activity by a receptor-targeted polymer vesicle-based drug delivery formulation of pravastatin. J. Cardiovasc. Pharmacol. 51:246-252.
45. Pollack, P.S., et al. 2005. Pregnancy outcomes after maternal exposure to simvastatin and lovastatin. Birth Defects Res. A Clin. Mol. Teratol. 73:888-896.
46. Elahi, M.M., et al. 2008. Statin treatment in hypercholesterolemic pregnant mice reduces cardiovascular risk factors in their offspring. Hypertension. 51:939-944.
47. Wagner, B.K., et al. 2008. Large-scale chemical dissection of mitochondrial function. Nat Biotechnol. 26:343-351.
48. Cudmore, M., et al. 2007. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation. 115:1789-1797.
49. Connolly, A.J., Suh, D.Y., Hunt, T.K., and Coughlin, S.R. 1997. Mice lacking the thrombin receptor, PAR1, have normal skin wound healing. Am. J. Pathol. 151:1199-1204.
50. Melis, E., et al. 2001. Targeted deletion of the cytosolic domain of tissue factor in mice does not affect development. Biochem. Biophys. Res. Commun. 286:580-586.
51. Ahamed, J., et al. 2006. Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc. Natl. Acad. Sci. U. S. A. 103:13932-13937.
52. Huang, M., et al. 1998. The mechanism of an inhibitory antibody on TF-initiated blood coagulation revealed by the crystal structures of human tissue factor, Fab 5G9 and TF.G9 complex. J. Mol. Biol. 275:873-894.
53. Mueller, B.M., Reisfeld, R.A., Edgington, T.S., and Ruf, W. 1992. Expression of tissue factor by melanoma cells promotes efficient hematogenous metastasis. Proc. Natl. Acad. Sci. U. S. A. 89:11832-11836.
54. Ruf, W., and Edgington, T.S. 1991. An anti-tissue factor monoclonal antibody which inhibits TF.VIIa complex is a potent anticoagulant in plasma. Thromb. Haemost. 66:529-533.