Role of tissue factor in thrombosis in antiphospholipid antibody syndrome

Lupus

Volumn 19, Issue 4, 2010, Pages 370-378

  Boles, J ^a   MacKman, N ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Antiphospholipid syndrome; Coagulation; DIC; Thrombosis; Tissue factor

Indexed keywords

BETA2 GLYCOPROTEIN 1; BLOOD CLOTTING FACTOR 7A; BLOOD CLOTTING FACTOR 7A INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MONOCLONAL ANTIBODY; PHOSPHOLIPID ANTIBODY; PRAVASTATIN; RECOMBINANT TISSUE FACTOR PATHWAY INHIBITOR; THROMBOPLASTIN; TOLL LIKE RECEPTOR 4; WARFARIN;

ANTIPHOSPHOLIPID SYNDROME; AORTA THROMBOSIS; ARTERY THROMBOSIS; CORONARY ARTERY THROMBOSIS; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE MARKER; DISEASE MODEL; DISSEMINATED INTRAVASCULAR CLOTTING; DRUG MECHANISM; ENDOTHELIUM INJURY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RISK FACTOR; SEPTIC SHOCK; THROMBOSIS; THROMBOTIC THROMBOCYTOPENIC PURPURA; VASCULAR DISEASE; VEIN THROMBOSIS;

ANIMALS; ANTIBODIES, ANTIPHOSPHOLIPID; ANTIPHOSPHOLIPID SYNDROME; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MICE; PREGNANCY; PREGNANCY COMPLICATIONS; THROMBOPLASTIN; THROMBOSIS;

EID: 77951210466     PISSN: 09612033     EISSN: None     Source Type: Journal    
DOI: 10.1177/0961203309360810     Document Type: Review

References (107)

1. Broze GJ Jr, Leykam JE, Schwartz BD, Miletich JP Purification of human brain tissue factor. J Biol Chem 1985 ; 260: 10917-10920. (Pubitemid 16253239)
2. Spicer EK, Horton R., Bloem L., et al. Isolation of cDNA clones coding for human tissue factor: primary structure of the protein and cDNA. Proc Natl Acad Sci U S A 1987 ; 84: 5148-5152. (Pubitemid 17119118)
3. Morrissey JH, Fakhrai H., Edgington TS Molecular cloning of the cDNA for tissue factor, the cellular receptor for the initiation of the coagulation protease cascade. Cell 1987 ; 50: 129-135.
4. Mackman N., Morrissey JH, Fowler B., Edgington TS Complete sequence of the human tissue factor gene, a highly regulated cellular receptor that initiates the coagulation protease cascade. Biochemistry 1989 ; 28: 1755-1762. (Pubitemid 19072050)
5. Banner DW, DArcy A., Chene C., et al. The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 1996 ; 380: 41-46. (Pubitemid 26076234)
6. Komiyama Y., Pedersen AH, Kisiel W. Proteolytic activation of human factors IX and X by recombinant human factor VIIa: effects of calcium, phospholipids, and tissue factor. Biochemistry 1990 ; 29: 9418-9425. (Pubitemid 20329079)
7. Mackman N. Regulation of the tissue factor gene. FASEB J 1995 ; 9: 883-889.
8. Osterud B., Bjorklid E. Sources of tissue factor. Semin Thromb Hemost 2006 ; 32: 11-23. (Pubitemid 43297432)
9. 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 1989 ; 134: 1087-1097.
10. Butenas S., Bouchard BA, Brummel-Ziedins KE, Parhami- Seren B., Mann KG Tissue factor activity in whole blood. Blood 2005 ; 105: 2764-2770. (Pubitemid 40446267)
11. Giesen PL, Rauch U., Bohrmann B., et al. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci U S A 1999 ; 96: 2311-2315. (Pubitemid 29117911)
12. Nemerson Y. A different view of thrombosis. Blood Coagul Fibrinolysis 2000 ; 11 (Suppl 1). S1 - S2. (Pubitemid 30368693)
13. Mackman N. Alternatively spliced tissue factor - one cut too many? Thromb Haemost 2007 ; 97: 5-8.
14. Hoffman M., Whinna HC, Monroe DM Circulating tissue factor accumulates in thrombi, but not in hemostatic plugs. J Thromb Haemost 2006 ; 4: 2092-2093. (Pubitemid 44226805)
15. Fleck RA, Rao LV, Rapaport SI, Varki N. Localization of human tissue factor antigen by immunostaining with monospecific, polyclonal anti-human tissue factor antibody. Thromb Res 1990 ; 59: 421-437. (Pubitemid 20143748)
16. Flossel C., Luther T., Muller M., Albrecht S., Kasper M. Immunohistochemical detection of tissue factor (TF) on paraffin sections of routinely fixed human tissue. Histochemistry 1994 ; 101: 449-453. (Pubitemid 2103038)
17. Mackman N., Sawdey MS, Keeton MR, Loskutoff DJ Murine tissue factor gene expression in vivo. Tissue and cell specificity and regulation by lipopolysaccharide. Am J Pathol 1993 ; 143: 76-84. (Pubitemid 24058162)
18. Erlich J., Parry GC, Fearns C., et al. Tissue factor is required for uterine hemostasis and maintenance of the placental labyrinth during gestation. Proc Natl Acad Sci U S A 1999 ; 96: 8138-8143. (Pubitemid 29328421)
19. Eddleston M., de la Torre JC, Oldstone MB, Loskutoff DJ, Edgington TS, Mackman N. Astrocytes are the primary source of tissue factor in the murine central nervous system. A role for astrocytes in cerebral hemostasis. J Clin Invest 1993 ; 92: 349-358. (Pubitemid 23209016)
20. Mackman N. Tissue-specific hemostasis in mice. Arterioscler Thromb Vasc Biol 2005 ; 25: 2273-2281.
21. Snyder LA, Rudnick KA, Tawadros R., et al. Expression of human tissue factor under the control of the mouse tissue factor promoter mediates normal hemostasis in knock-in mice. J Thromb Haemost 2008 ; 6: 306-314.
22. Carmeliet P., Mackman N., Moons L., et al. Role of tissue factor in embryonic blood vessel development. Nature 1996 ; 383: 73-75. (Pubitemid 26296462)
23. Bugge TH, Xiao Q., Kombrinck KW, et al. Fatal embryonic bleeding events in mice lacking tissue factor, the cell-associated initiator of blood coagulation. Proc Natl Acad Sci U S A 1996 ; 93: 6258-6263. (Pubitemid 26230292)
24. 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: 1583-1587. (Pubitemid 26307052)
25. Mackman N., Tilley RE, Key NS Role of the extrinsic pathway of blood coagulation in hemostasis and thrombosis. Arterioscler Thromb Vasc Biol 2007 ; 27: 1687-1693.
26. Morel O., Toti F., Hugel B., et al. Procoagulant microparticles: disrupting the vascular homeostasis equation? Arterioscler Thromb Vasc Biol 2006 ; 26: 2594-2604.
27. Pawlinski R., Pedersen B., Schabbauer G., et al. Role of tissue factor and protease-activated receptors in a mouse model of endotoxemia. Blood 2004 ; 103: 1342-1347. (Pubitemid 38168646)
28. Zillmann A., Luther T., Muller I., et al. Platelet-associated tissue factor contributes to the collagen-triggered activation of blood coagulation. Biochem Biophys Res Commun 2001 ; 281: 603-609. (Pubitemid 32928197)
29. Panes O., Matus V., Saez CG, Quiroga T., Pereira J., Mezzano D. Human platelets synthesize and express functional tissue factor. Blood 2007 ; 109: 5242-5250. (Pubitemid 46890544)
30. Schwertz H., Tolley ND, Foulks JM, et al. Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenicity of human platelets. J Exp Med 2006 ; 203: 2433-2440. (Pubitemid 44664613)
31. Del Conde I., Shrimpton CN, Thiagarajan P., Lopez JA Tissue-factor- bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005 ; 106: 1604-1611. (Pubitemid 41208572)
32. Maugeri N., Brambilla M., Camera M., et al. Human polymorphonuclear leukocytes produce and express functional tissue factor upon stimulation. J Thromb Haemost 2006 ; 4: 1323-1330. (Pubitemid 43756712)
33. Moosbauer C., Morgenstern E., Cuvelier SL, et al. Eosinophils are a major intravascular location for tissue factor storage and exposure. Blood 2007 ; 109: 995-1002. (Pubitemid 46220644)
34. Ritis K., Doumas M., Mastellos D., et al. A novel C5a receptor-tissue factor cross-talk in neutrophils links innate immunity to coagulation pathways. J Immunol 2006 ; 177: 4794-4802. (Pubitemid 44469814)
35. Egorina EM, Sovershaev MA, Olsen JO, Osterud B. Granulocytes do not express but acquire monocyte-derived tissue factor in whole blood: evidence for a direct transfer. Blood 2008 ; 111: 1208-1216. (Pubitemid 351213402)
36. Bach RR Tissue factor encryption. Arterioscler Thromb Vasc Biol 2006 ; 26: 456-461.
37. Chen VM, Ahamed J., Versteeg HH, Berndt MC, Ruf W., Hogg PJ Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry 2006 ; 45: 12020-12028. (Pubitemid 44497827)
38. Bach RR, Monroe D. What is wrong with the allosteric disulfide bond hypothesis ? Arterioscler Thromb Vasc Biol 2009 ; 29: 1997-1998.
39. Speidel CM, Thornton JD, Meng YY, Eisenberg PR, Edgington TS, Abendschein DR Procoagulant activity on injured arteries and associated thrombi is mediated primarily by the complex of tissue factor and factor VIIa. Coron Artery Dis 1996 ; 7: 57-62.
40. Pawashe AB, Golino P., Ambrosio G., et al. A monoclonal antibody against rabbit tissue factor inhibits thrombus formation in stenotic injured rabbit carotid arteries. Circ Res 1994 ; 74: 56-63. (Pubitemid 24976837)
41. Roque M., Reis ED, Fuster V., et al. Inhibition of tissue factor reduces thrombus formation and intimal hyperplasia after porcine coronary angioplasty. J Am Coll Cardiol 2000 ; 36: 2303-2310.
42. Day SM, Reeve JL, Pedersen B., et al. Macrovascular thrombosis is driven by tissue factor derived primarily from the blood vessel wall. Blood 2005 ; 105: 192-198. (Pubitemid 40053082)
43. Wang L., Miller C., Swarthout RF, Rao M., Mackman N., Taubman MB Vascular smooth muscle-derived tissue factor is critical for arterial thrombosis after ferric chloride-induced injury. Blood 2009 ; 113: 705-713.
44. Esmon CT Basic mechanisms and pathogenesis of venous thrombosis. Blood Rev 2009 ; 23: 225-229.
45. Himber J., Kling D., Fallon JT, Nemerson Y., Riederer MA In situ localization of tissue factor in human thrombi. Blood 2002 ; 99: 4249-4250. (Pubitemid 35332082)
46. Kamikura Y., Wada H., Nobori T., et al. Elevated levels of leukocyte tissue factor mRNA in patients with venous thromboembolism. Thromb Res 2005 ; 116: 307-312. (Pubitemid 40994913)
47. Biro E., Sturk-Maquelin KN, Vogel GM, et al. Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost 2003 ; 1: 2561-2568.
48. Tesselaar ME, Romijn FP, Van Der Linden IK, Prins FA, Bertina RM, Osanto S. Microparticle-associated tissue factor activity: a link between cancer and thrombosis? J Thromb Haemost 2007 ; 5: 520-527. (Pubitemid 46680685)
49. Tesselaar ME, Romijn FP, van der Linden IK, Bertina RM, Osanto S. Microparticle-associated tissue factor activity in cancer patients with and without thrombosis. J Thromb Haemost 2009 ; 7: 1421-1423.
50. Manly DA, Wang J., Glover SL, et al. Increased microparticle tissue factor activity in cancer patients with venous thromboembolism. Thromb Res 2009 ; epub ahead or print.
51. Khorana AA, Francis CW, Menzies KE, et al. Plasma tissue factor may be predictive of venous thromboembolism in pancreatic cancer. J Thromb Haemost 2008 ; 6: 1983-1985.
52. Yu JL, May L., Lhotak V., et al. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood 2005 ; 105: 1734-1741. (Pubitemid 40223697)
53. Davila M., Amirkhosravi A., Coll E., et al. Tissue factor-bearing microparticles derived from tumor cells: impact on coagulation activation. J Thromb Haemost 2008 ; 6: 1517-1524.
54. Levi M. Current understanding of disseminated intravascular coagulation. Br J Haematol 2004 ; 124: 567-576. (Pubitemid 38297089)
55. Sase T., Wada H., Nishioka J., et al. Measurement of tissue factor messenger RNA levels in leukocytes from patients in hypercoagulable state caused by several underlying diseases. Thromb Haemost 2003 ; 89: 660-665. (Pubitemid 36456963)
56. Franco RF, de Jonge E., Dekkers PE, et al. The in vivo kinetics of tissue factor messenger RNA expression during human endotoxemia: relationship with activation of coagulation. Blood 2000 ; 96: 554-559. (Pubitemid 30463375)
57. Aras O., Shet A., Bach RR, et al. Induction of microparticle- and cell-associated intravascular tissue factor in human endotoxemia. Blood 2004 ; 103: 4545-4553. (Pubitemid 38745982)
58. Taylor FB Jr, Chang A., Ruf W., et al. Lethal E. coli septic shock is prevented by blocking tissue factor with monoclonal antibody. Circ Shock 1991 ; 33: 127-134.
59. Carr C., Bild GS, Chang AC, 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 1994 ; 44: 126-137.
60. Taylor FB, Chang AC, Peer G., Li A., Ezban M., Hedner U. Active site inhibited factor VIIa (DEGR VIIa) attenuates the coagulant and interleukin-6 and -8, but not tumor necrosis factor, responses of the baboon to LD100 Escherichia coli. Blood 1998 ; 91: 1609-1615. (Pubitemid 28110325)
61. Levi M., ten Cate H., Bauer KA, et al. 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: 114-120. (Pubitemid 24030827)
62. Biemond BJ, Levi M., ten Cate H., et al. Complete inhibition of endotoxin-induced coagulation activation in chimpanzees with a monoclonal Fab fragment against factor VII/VIIa. Thromb Haemost 1995 ; 73: 223-230.
63. Warr TA, Rao LV, Rapaport SI Disseminated intravascular coagulation in rabbits induced by administration of endotoxin or tissue factor: effect of anti-tissue factor antibodies and measurement of plasma extrinsic pathway inhibitor activity. Blood 1990 ; 75: 1481-1489.
64. van der Poll T. Tissue factor as an initiator of coagulation and inflammation in the lung. Crit Care 2008 ; 12 (Suppl 6). S3.
65. Niessen F., Schaffner F., Furlan-Freguia C., et al. Dendritic cell PAR1-S1P3 signalling couples coagulation and inflammation. Nature 2008 ; 452: 654-658. (Pubitemid 351483355)
66. Andrews BS, Rehemtulla A., Fowler BJ, Edgington TS, Mackman N. Conservation of tissue factor primary sequence among three mammalian species. Gene 1991 ; 98: 265-269.
67. Petersen LC, Norby PL, Branner S., et al. Characterization of recombinant murine factor VIIa and recombinant murine tissue factor: a human-murine species compatibility study. Thromb Res 2005 ; 116: 75-85.
68. Parry GC, Erlich JH, Carmeliet P., Luther T., Mackman N. Low levels of tissue factor are compatible with development and hemostasis in mice. J Clin Invest 1998 ; 101: 560-569. (Pubitemid 28084238)
69. Pedersen B., Holscher T., Sato Y., Pawlinski R., Mackman N. A balance between tissue factor and tissue factor pathway inhibitor is required for embryonic development and hemostasis in adult mice. Blood 2005 ; 105: 2777-2782. (Pubitemid 40446269)
70. Pawlinski R., Tencati M., Holscher T., et al. Role of cardiac myocyte tissue factor in heart hemostasis. J Thromb Haemost 2007 ; 5: 1693-1700. (Pubitemid 47091413)
71. Osterud B., Olsen JO, Bjorklid E. What is blood borne tissue factor? Thromb Res 2009 ; 124: 640-641. (Pubitemid 351888882)
72. Redecha P., Tilley R., Tencati M., et al. Tissue factor: a link between C5a and neutrophil activation in antiphospholipid antibody induced fetal injury. Blood 2007 ; 110: 2423-2431. (Pubitemid 47523163)
73. Ginsburg KS, Liang MH, Newcomer L., et al. Anticardiolipin antibodies and the risk for ischemic stroke and venous thrombosis. Ann Intern Med 1992 ; 117: 997-1002.
74. Blank M., Cohen J., Toder V., Shoenfeld Y. Induction of anti-phospholipid syndrome in naive mice with mouse lupus monoclonal and human polyclonal anti-cardiolipin antibodies. Proc Natl Acad Sci U S A 1991 ; 88: 3069-3073. (Pubitemid 21916560)
75. Pierangeli SS, Barker JH, Stikovac D., et al. Effect of human IgG antiphospholipid antibodies on an in vivo thrombosis model in mice. Thromb Haemost 1994 ; 71: 670-674. (Pubitemid 2108697)
76. Reverter JC, Tassies D., Font J., et al. Hypercoagulable state in patients with antiphospholipid syndrome is related to high induced tissue factor expression on monocytes and to low free proteins. Arterioscler Thromb Vasc Biol 1996 ; 16: 1319-1326.
77. Cuadrado MJ, Lopez-Pedrera C., Khamashta MA, et al. Thrombosis in primary antiphospholipid syndrome: a pivotal role for monocyte tissue factor expression. Arthritis Rheum 1997 ; 40: 834-841.
78. Dobado-Berrios PM, Lopez-Pedrera C., Velasco F., Aguirre MA, Torres A., Cuadrado MJ Increased levels of tissue factor mRNA in mononuclear blood cells of patients with primary antiphospholipid syndrome. Thromb Haemost 1999 ; 82: 1578-1582.
79. de Prost D., Ollivier V., Ternisien C., Chollet-Martin S. Increased monocyte procoagulant activity independent of the lupus anticoagulant in patients with systemic lupus erythematosus. Thromb Haemost 1990 ; 64: 216-221. (Pubitemid 20351868)
80. Nojima J., Masuda Y., Iwatani Y., et al. Tissue factor expression on monocytes induced by anti-phospholipid antibodies as a strong risk factor for thromboembolic complications in SLE patients. Biochem Biophys Res Commun 2008 ; 365: 195-200. (Pubitemid 350102473)
81. Kornberg A., Blank M., Kaufman S., Shoenfeld Y. Induction of tissue factor-like activity in monocytes by anti-cardiolipin antibodies. J Immunol 1994 ; 153: 1328-1332. (Pubitemid 24228525)
82. Amengual O., Atsumi T., Khamashta MA, Hughes GR The role of the tissue factor pathway in the hypercoagulable state in patients with the antiphospholipid syndrome. Thromb Haemost 1998 ; 79: 276-281. (Pubitemid 28065869)
83. Reverter JC, Tassies D., Font J., et al. Effects of human monoclonal anticardiolipin antibodies on platelet function and on tissue factor expression on monocytes. Arthritis Rheum 1998 ; 41: 1420-1427.
84. Zhou H., Wolberg AS, Roubey RA Characterization of monocyte tissue factor activity induced by IgG antiphospholipid antibodies and inhibition by dilazep. Blood 2004 ; 104: 2353-2358. (Pubitemid 39331833)
85. Zhou BY, He JJ Proliferation inhibition of astrocytes, neurons, and non-glial cells by intracellularly expressed human immunodeficiency virus type 1 (HIV-1) Tat protein. Neurosci Lett 2004 ; 359: 155-158.
86. Lopez-Pedrera C., Buendia P., Barbarroja N., Siendones E., Velasco F., Cuadrado MJ Antiphospholipid-mediated thrombosis: interplay between anticardiolipin antibodies and vascular cells. Clin Appl Thromb Hemost 2006 ; 12: 41-45. (Pubitemid 43221570)
87. Ma K., Simantov R., Zhang JC, Silverstein R., Hajjar KA, McCrae KR High affinity binding of beta 2-glycoprotein I to human endothelial cells is mediated by annexin II. J Biol Chem 2000 ; 275: 15541-15548. (Pubitemid 30337288)
88. Zhang J., McCrae KR Annexin A2 mediates endothelial cell activation by antiphospholipid/anti-beta2 glycoprotein I antibodies. Blood 2005 ; 105: 1964-1969. (Pubitemid 40731779)
89. Pennings MT, van Lummel M., Derksen RH, et al. Interaction of beta2-glycoprotein I with members of the low density lipoprotein receptor family. J Thromb Haemost 2006 ; 4: 1680-1690. (Pubitemid 44144793)
90. Pierangeli SS, Vega-Ostertag ME, Raschi E., et al. Toll-like receptor and antiphospholipid mediated thrombosis: in vivo studies. Ann Rheum Dis 2007 ; 66: 1327-1333. (Pubitemid 47492476)
91. Raschi E., Testoni C., Bosisio D., et al. Role of the MyD88 transduction signaling pathway in endothelial activation by antiphospholipid antibodies. Blood 2003 ; 101: 3495-3500. (Pubitemid 36857933)
92. Sorice M., Longo A., Capozzi A., et al. Anti-beta2-glycoprotein I antibodies induce monocyte release of tumor necrosis factor alpha and tissue factor by signal transduction pathways involving lipid rafts. Arthritis Rheum 2007 ; 56: 2687-2697. (Pubitemid 47237287)
93. Montiel-Manzano G., Romay-Penabad Z., Papalardo de Martinez E., et al. In vivo effects of an inhibitor of nuclear factor-kappa B on thrombogenic properties of antiphospholipid antibodies. Ann N Y Acad Sci 2007 ; 1108: 540-553. (Pubitemid 47528768)
94. Bohgaki M., Atsumi T., Yamashita Y., et al. The p38 mitogen-activated protein kinase (MAPK) pathway mediates induction of the tissue factor gene in monocytes stimulated with human monoclonal anti-beta2Glycoprotein I antibodies. Int Immunol 2004 ; 16: 1633-1641. (Pubitemid 39480782)
95. Yasuda S., Bohgaki M., Atsumi T., Koike T. Pathogenesis of antiphospholipid antibodies: impairment of fibrinolysis and monocyte activation via the p38 mitogen-activated protein kinase pathway. Immunobiology 2005 ; 210: 775-780. (Pubitemid 41683862)
96. Aronovich R., Gurwitz D., Kloog Y., Chapman J. Antiphospholipid antibodies, thrombin and LPS activate brain endothelial cells and Ras-dependent pathways through distinct mechanisms. Immunobiology 2005 ; 210: 781-788. (Pubitemid 41683863)
97. Lopez-Pedrera C., Buendia P., Cuadrado MJ, et al. Antiphospholipid antibodies from patients with the antiphospholipid syndrome induce monocyte tissue factor expression through the simultaneous activation of NF-kappaB/Rel proteins via the p38 mitogen-activated protein kinase pathway, and of the MEK-1/ERK pathway. Arthritis Rheum 2006 ; 54: 301-311. (Pubitemid 43122214)
98. Vega-Ostertag ME, Ferrara DE, Romay-Penabad Z., et al. Role of p38 mitogen-activated protein kinase in antiphospholipid antibody-mediated thrombosis and endothelial cell activation. J Thromb Haemost 2007 ; 5: 1828-1834. (Pubitemid 47288938)
99. Lopez-Pedrera C., Buendia P., Aguirre MA, Velasco F., Cuadrado MJ Antiphospholipid syndrome and tissue factor: a thrombotic couple. Lupus 2006 ; 15: 161-166.
100. Kinev AV, Roubey RA Tissue factor in the antiphospholipid syndrome. Lupus 2008 ; 17: 952-958.
101. Girardi G., Berman J., Redecha P., et al. Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J Clin Invest 2003 ; 112: 1644-1654. (Pubitemid 38063722)
102. Redecha P., Franzke CW, Ruf W., Mackman N., Girardi G. Neutrophil activation by the tissue factor/Factor VIIa/PAR2 axis mediates fetal death in a mouse model of antiphospholipid syndrome. J Clin Invest 2008 ; 118: 3453-3461.
103. Girardi G., Mackman N. Tissue factor in antiphospholipid antibody-induced pregnancy loss: a pro-inflammatory molecule. Lupus 2008 ; 17: 931-936.
104. Seshan SV, Franzke CW, Redecha P., Monestier M., Mackman N., Girardi G. Role of tissue factor in a mouse model of thrombotic microangiopathy induced by antiphospholipid antibodies. Blood 2009 ; 114: 1675-1683.
105. Steiner S., Speidl WS, Pleiner J., et al. Simvastatin blunts endotoxin-induced tissue factor in vivo. Circulation 2005 ; 111: 1841-1846. (Pubitemid 40525151)
106. Meroni PL, Raschi E., Testoni C., et al. Statins prevent endothelial cell activation induced by antiphospholipid (anti-beta2-glycoprotein I) antibodies: effect on the proadhesive and proinflammatory phenotype. Arthritis Rheum 2001 ; 44: 2870-2878. (Pubitemid 34016207)
107. Ferrara DE, Swerlick R., Casper K., et al. Fluvastatin inhibits up-regulation of tissue factor expression by antiphospholipid antibodies on endothelial cells. J Thromb Haemost 2004 ; 2: 1558-1563.