Sources of Tissue Factor

ABSTRACT

Tissue factor (TF) exhibits a distinct nonuniform tissue distribution. Thus, high levels are found in highly vascularized organs such as the lung, brain, and placenta; intermediate levels in the heart, kidney, intestine, testes, and uterus; and low levels in the spleen, thymus, and liver. Several cell types are known to express TF constitutively, such as astrocytes in the brain, epithelial cells enveloping organs and body surfaces, adventitial fibroblasts and pericytes, and cardial myocytes in the heart. Smooth muscle cells in the media of the vessel wall and monocytes/macrophages contain small amounts of TF, which is enhanced substantially upon activation of the cells. Endothelial cells probably do not express TF. The popular concept of TF serving predominantly as a hemostatic envelope encapsulating the vascular bed has been challenged recently by the observation that blood of healthy individuals may form TF-induced thrombi under conditions entailing shear stress and activated platelets, corroborating the notion of blood-borne TF. Accordingly, small amounts of decrypted TF activity is detected in calcium ionophore-stimulated monocytes, and microparticles from plasma of healthy subjects possess TF-like activity subject to partial inactivation by anti-TF antibody. In addition to microparticles, plasma TF also comprises the soluble alternatively spliced human TF and truncated TF, both of which probably require factor VIIa to be physiologically active. Although it has been suggested that activated platelets possess active TF, the notion of TF as an integral platelet component is contested by more recent data. Rather, platelets may be very important in decrypting monocyte TF activity in a process entailing transfer of TF to activated platelets.

Tissue factor, TF - blood-borne TF - monocytes - platelets

REFERENCES

• 1 Morawitz P. Die Chemie der Blutgerinnung.  Ergeb Physiol. 1905;  4 307-416
• 2 Owren P A. Parahaemophilia, haemorrhagic diathesis due to the absence of a previously unknown clotting factor.  Lancet. 1947;  1 446-448
• 3 Alexander B, Goldstein R, Landwehr G, Cook C D. Congenital SPCA deficiency: a hitherto unrecognised defect with hemorrhage rectified by serum and serum fractions.  J Clin Invest. 1951;  30 596-608
• 4 Koller F. Experiments on a new clotting factor.  Acta Haematol. 1951;  6 1
• 5 Aggeler P M, White S G, Glendening M D, Page E W, Leake T B, Bates G. Plasma thromboplastin component (PTC) deficiency: a new disease resembling hemophilia.  Proc Soc Exp Biol Med. 1952;  79 692-694
• 6 Biggs R, Douglas A S, Macfarlane R G et al.. Christmas disease: a condition previously mistaken for hemophilia.  Br Med J. 1952;  2 1378-1382
• 7 Telfer T P, Denson K W, Wright D RA. “New” coagulation defect.  Br J Haematol. 1956;  2 308-316
• 8 Coon R W, Stewart W B, Flynn J E. Fed Proc. 1954;  35 426
• 9 Hjort P F. Intermediate reactions in the coagulation of blood with tissue thromboplastin.  Scand J Clin Lab Invest. 1957;  9(suppl 27) 1-183
• 10 Macfarlane R G. An enzyme cascade in the blood clotting mechanism and its function as a biochemical amplifier.  Nature. 1964;  202 498-499
• 11 Davie E W, Ratnoff O D. Water fall sequence for intrinsic blood clotting.  Science. 1964;  245 1310-1312
• 12 Nemerson Y. The reaction between bovine brain tissue factor and factors VII and X.  Biochemistry. 1966;  5 601-608
• 13 Østerud B, Rapaport S I. Activation of factor IX by the reaction product of tissue factor and factor VII: additional pathway for initiating blood coagulation.  Proc Natl Acad Sci U S A. 1977;  74 5260-5264
• 14 Bach R, Gentry R, Nemerson Y. Factor VII binding to tissue factor in reconstituted phospholipid vesicles: induction of cooperativity by phosphatidylserine.  Biochemistry. 1986;  25 4007-4020
• 15 Sabharwal A K, Birktoft J J, Gorka J, Wildgoose P, Petersen L C, Bajaj S P. High affinity Ca(2+)-binding site in the serine protease domain of human factor VIIa and its role in tissue factor binding and development of catalytic activity.  J Biol Chem. 1995;  270 15523-15530
• 16 Ruf W, Rehemtulla A, Morrissey J H, Edgington T S. Phospholipid-independent and -dependent interactions required for tissue factor receptor and cofactor function.  J Biol Chem. 1991;  266 2158-2166
• 17 Østerud B. The role of phospholipids in the expression of factor VII activity.  Thromb Haemost. 1991;  65 940 , (abst 872)
• 18 Broze G J, Majerus P W. Purification and properties of human coagulation factor VII.  J Biol Chem. 1980;  255 1242-1247
• 19 Bajaj S P, Rapaport S I, Brown S F. Isolation and characterization of human factor VII. Activation of factor VII by factor Xa.  J Biol Chem. 1981;  256 253-259
• 20 Davie E W, Fujikawa K, Kisiel W. The coagulation cascade: initiation, maintenance, and regulation.  Biochemistry. 1991;  30 10363-10370
• 21 Neuenschwander P F, Morrissey J H. Deletion of the membrane anchoring region of tissue factor abolishes autoactivation of factor VII but not cofactor function. Analysis of a mutant with a selective deficiency in activity.  J Biol Chem. 1992;  267 14477-14482
• 22 Higashi S, Nishimura H, Fujii S, Takada K, Iwanaga S. Tissue factor potentiates the factor VIIa-catalyzed hydrolysis of an ester substrate.  J Biol Chem. 1992;  267 17990-17996
• 23 Lawson J H, Butenas S, Mann K G. The evaluation of complex-dependent alterations in human factor VIIa.  J Biol Chem. 1992;  267 4834-4843
• 24 Ruf W, Kalnik M W, Lund-Hansen T, Edgington T S. Characterization of factor VII association with tissue factor in solution. High and low affinity calcium binding sites in factor VII contribute to functionally distinct interactions.  J Biol Chem. 1991;  266 15719-15725
• 25 Fiore M M, Neuenschwander P F, Morrissey J H. An unusual antibody that blocks tissue factor/factor VIIa function by inhibiting cleavage only of macromolecular substrates.  Blood. 1992;  80 3127-3134
• 26 Neuenschwander P F, Fiore M M, Morrissey J H. Factor VII autoactivation proceeds via interaction of distinct protease-cofactor and zymogen-cofactor complexes. Implications of a two-dimensional enzyme kinetic mechanism.  J Biol Chem. 1993;  268 21489-21492
• 27 Edgington T S, Mackman N, Brand K, Ruf W. The structural biology of expression and function of tissue factor.  Thromb Haemost. 1991;  66 67-79
• 28 Krishnaswamy S, Field K A, Edgington T S, Morrissey J H, Mann K G. Role of the membrane surface in the activation of human coagulation factor X.  J Biol Chem. 1992;  267 26110-26120
• 29 Fiore M M, Neuenschwander P F, Morrissey J H. The biochemical basis for the apparent defect of soluble mutant tissue factor in enhancing the proteolytic activities of factor VIIa.  J Biol Chem. 1994;  269 143-149
• 30 Astrup T. Assay and content of tissue thromboplastin in different organs.  Thromb Diath Haemorrh. 1965;  14 401-416
• 31 Drake T A, Morrissey J H, Edgington T S. Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis.  Am J Pathol. 1989;  134 1087-1097
• 32 Giesen P L, Rauch U, Bohrmann B et al.. Blood-borne tissue factor: another view of thrombosis.  Proc Natl Acad Sci USA. 1999;  96 2311-2315
• 33 Camerer E, Kolsto A B, Prydz H. Cell biology of tissue factor, the principal initiator of blood coagulation.  Thromb Res. 1996;  81 1-41
• 34 Wilcox J N, Smith K M, Schwartz S M, Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque.  Proc Natl Acad Sci U S A. 1989;  86 2839-2843
• 35 Solberg S, Østerud B, Larsen T, Sorlie D. Lack of ability to synthesize tissue factor by endothelial cells in intact human saphenous veins.  Blood Coagul Fibrinolysis. 1990;  1 595-600
• 36 Østerud B, Tindall A, Brox J H, Olsen J O. Thromboplastin content in the vessel walls of different arteries and organs of rabbits.  Thromb Res. 1986;  42 323-329
• 37 Erlich J, Fearns C, Mathison J, Ulevitch R J, Mackman N. Lipopolysaccharide induction of tissue factor expression in rabbits.  Infect Immun. 1999;  67 2540-2546
• 38 Semeraro N, Triggiani R, Montemurro P, Cavallo L G, Colucci M. Enhanced endothelial tissue factor but normal thrombomodulin in endotoxin-treated rabbits.  Thromb Res. 1993;  71 479-486
• 39 Drake T A, Cheng J, Chang A, Taylor Jr F B. Expression of tissue factor, thrombomodulin, and E-selectin in baboons with lethal Escherichia coli sepsis. [Published erratum in Am J Pathol 1993;143(2):649].  Am J Pathol. 1993;  142 1458-1470
• 40 Shet A S, Aras O, Gupta K et al.. Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes.  Blood. 2003;  102 2678-2683
• 41 Solovey A, Kollander R, Shet A et al.. Endothelial cell expression of tissue factor in sickle mice is augmented by hypoxia/reoxygenation and inhibited by lovastatin.  Blood. 2004;  104 840-846
• 42 Del Conde I, Shrimpton C N, Thiagarajan P, Lopez J A. Tissue factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation.  Blood. 2005;  106 1604-1611
• 43 Fleck R A, Rao L V, Rapaport S I, Varki N. Localization of human tissue factor antigen by immunostaining with monospecific, polyclonal anti-human tissue factor antibody. [Corrected and republished article originally printed in Thromb Res 1990;57(5):765-781].  Thromb Res. 1990;  59 421-437
• 44 Jang Y, Guzman L A, Lincoff A M et al.. Influence of blockade at specific levels of the coagulation cascade on restenosis in a rabbit atherosclerotic femoral artery injury model.  Circulation. 1995;  92 3041-3050
• 45 Oltrona L, Speidel C M, Recchia D, Wickline S A, Eisenberg P R, Abendschein D R. Inhibition of tissue factor-mediated coagulation markedly attenuates stenosis after balloon-induced arterial injury in minipigs.  Circulation. 1997;  96 646-652
• 46 Bach R R. Initiation of coagulation by tissue factor.  CRC Crit Rev Biochem. 1988;  23 339-368
• 47 Mackman N, Sawdey M S, Keeton M R, Loskutoff D J. Murine tissue factor gene expression in vivo. Tissue and cell specificity and regulation by lipopolysaccharide.  Am J Pathol. 1993;  143 76-84
• 48 Eddleston M, de la Torre J C, Oldstone M B, Loskutoff D J, Edgington T S, 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
• 49 Hartzell S, Ryder K, Lanahan A, Lau L F, Nathan D. A growth factor-responsive gene of murine BALB/c 3T3 cells encodes a protein homologous to human tissue factor.  Mol Cell Biol. 1989;  9 2567-2573
• 50 Faulk W P, Labarrere C A, Carson S D. Tissue factor: identification and characterization of cell types in human placentae.  Blood. 1990;  76 86-96
• 51 Mallat Z, Hugel B, Ohan J, Leseche G, Freyssinet J M, Tedgui A. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity.  Circulation. 1999;  99 348-353
• 52 Nieuwland R, Berckmans R J, McGregor S et al.. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis.  Blood. 2000;  95 930-935
• 53 Satta N, Toti F, Feugeas O et al.. Monocyte vesiculation is a possible mechanism for dissemination of membrane-associated procoagulant activities and adhesion molecules after stimulation by lipopolysaccharide.  J Immunol. 1994;  153 3245-3255
• 54 Misumi K, Ogawa H, Yasue H et al.. Circadian variation in plasma levels of free-form tissue factor pathway inhibitor antigen in patients with coronary spastic angina.  Jpn Circ J. 1998;  62 419-424
• 55 Suefuji H, Ogawa H, Yasue H et al.. Increased plasma tissue factor levels in acute myocardial infarction.  Am Heart J. 1997;  134 253-259
• 56 Rivers R P, Hathaway W E, Weston W L. The endotoxin-induced coagulant activity of human monocytes.  Br J Haematol. 1975;  30 311-316
• 57 Bach R R, Moldow C F. Mechanism of tissue factor activation on HL-60 cells.  Blood. 1997;  89 3270-3276
• 58 Butenas S, Bouchard B A, Brummel-Ziedins K E, Parhami-Seren B, Mann K G. Tissue factor activity in whole blood.  Blood. 2005;  105 2764-2770
• 59 Egorina E M, Sovershaev M A, Bjorkoy G et al.. Intracellular and surface distribution of monocyte tissue factor. Application to intersubject variability.  Arterioscler Thromb Vasc Biol. 2005;  25 1493-1498
• 60 Østerud B. The high responder phenomenon: enhancement of LPS induced tissue factor activity in monocytes by platelets and granulocytes.  Platelets. 1995;  6 119-125
• 61 Østerud B, Due Jr J. Blood coagulation in patients with benign and malignant tumours before and after surgery. Special reference to thromboplastin generation in monocytes.  Scand J Haematol. 1984;  32 258-264
• 62 Østerud B, Rapaport S I, Lavine K K. Factor V activity of platelets: evidence for an activated factor V molecule and for a platelet activator.  Blood. 1977;  49 819-834
• 63 Rao L V, Rapaport S I. The effect of platelets upon factor Xa-catalyzed activation of factor VII in vitro.  Blood. 1988;  72 396-401
• 64 Niemetz J, Marcus A J. The stimulatory effect of platelets and platelet membranes on the procoagulant activity of leukocytes.  J Clin Invest. 1974;  54 1437-1443
• 65 Lorenzet R, Niemetz J, Marcus A J, Broekman M J. Enhancement of mononuclear procoagulant activity by platelet 12-hydroxyeicosatetraenoic acid.  J Clin Invest. 1986;  78 418-423
• 66 Pinder P B, Hunt J A, Zacharski L R. In vitro stimulation of monocyte tissue factor activity by autologous platelets.  Am J Hematol. 1985;  19 317-325
• 67 Østerud B, Olsen J O, Wilsgard L. The role of arachidonic acid release and lipoxygenase pathway in lipopolysaccharide-induced thromboplastin activity in monocytes.  Blood Coagul Fibrinolysis. 1990;  1 41-46
• 68 Halvorsen H, Olsen J O, Østerud B. Granulocytes enhance LPS-induced tissue factor activity in monocytes via an interaction with platelets.  J Leukoc Biol. 1993;  54 275-282
• 69 Østerud B. Platelet activating factor enhancement of lipopolysaccharide-induced tissue factor activity in monocytes: requirement of platelets and granulocytes.  J Leukoc Biol. 1992;  51 462-465
• 70 Selak M A, Chignard M, Smith J B. Cathepsin G is a strong platelet agonist released by neutrophils.  Biochem J. 1988;  251 293-299
• 71 Halvorsen H, Østerud B. Cellular interactions in lipopolysaccharide induced tissue factor activity in monocytes: the mandatory role of cathepsin GIn: Sixma JJ XIIIth Congress of the International Society on Thrombosis and Haemostasis.  Thromb Haemost. 1991;  65 701 (abst 166)
• 72 Østerud B, Rao L V, Olsen J O. Induction of tissue factor expression in whole blood: lack of evidence for the presence of tissue factor expression in granulocytes.  [In process citation] Thromb Haemost. 2000;  83 861-867
• 73 Eilertsen K E, Østerud B. The central role of thromboxane and platelet activating factor receptors in ex vivo regulation of endotoxin-induced monocyte tissue factor activity in human whole blood.  J Endotoxin Res. 2002;  8 285-293
• 74 Eilertsen K E, Østerud B. Tissue factor: (patho)physiology and cellular biology.  Blood Coagul Fibrinolysis. 2004;  15 521-538
• 75 Østerud B, Bjorklid E. The production and availability of tissue thromboplastin in cellular populations of whole blood exposed to various concentrations of endotoxin. An assay for detection of endotoxin.  Scand J Haematol. 1982;  29 175-184
• 76 Schecter A D, Rollins B J, Zhang Y J et al.. Tissue factor is induced by monocyte chemoattractant protein-1 in human aortic smooth muscle and THP-1 cells.  J Biol Chem. 1997;  272 28568-28573
• 77 Nemerson Y, Giesen P L. Some thoughts about localization and expression of tissue factor.  Blood Coagul Fibrinolysis. 1998;  9(suppl 1) S45-S47
• 78 Fibach E, Treves A, Korenberg A, Rachmilewitz E A. In vitro generation of procoagulant activity by leukemic promyelocytes in response to cytotoxic drugs.  Am J Hematol. 1985;  20 257-265
• 79 Bouchard B A, Shatos M A, Tracy P B. Human brain pericytes differentially regulate expression of procoagulant enzyme complexes comprising the extrinsic pathway of blood coagulation.  Arterioscler Thromb Vasc Biol. 1997;  17 1-9
• 80 Bach R, Rifkin D B. Expression of tissue factor procoagulant activity: regulation by cytosolic calcium.  Proc Natl Acad Sci USA. 1990;  87 6995-6999
• 81 Wolberg A S, Monroe D M, Roberts H R, Hoffman M R. Tissue factor de-encryption: ionophore treatment induces changes in tissue factor activity by phosphatidylserine-dependent and -independent mechanisms.  Blood Coagul Fibrinolysis. 1999;  10 201-210
• 82 Breimo E S, Østerud B. Generation of TF-rich microparticles in an ex vivo whole blood model.  Blood Coagul Fibrinolysis. 2005;  16 399-405
• 83 Satta N, Toti F, Feugeas O et al.. Monocyte vesiculation is a possible mechanism for dissemination of membrane-associated procoagulant activities and adhesion molecules after stimulation by lipopolysaccharide.  J Immunol. 1994;  153 3245-3255
• 84 Hrachovinova I, Cambien B, Hafezi-Moghadam A et al.. Interaction of P-selectin and PSGL-1 generates microparticles that correct hemostasis in a mouse model of hemophilia A.  Nat Med. 2003;  9 1020-1025
• 85 Falati S, Liu Q, Gross P et al.. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin.  J Exp Med. 2003;  197 1585-1598
• 86 Murk J L, Stoorvogel W, Kleijmeer M J, Geuze H J. The plasticity of multivesicular bodies and the regulation of antigen presentation.  Semin Cell Dev Biol. 2002;  13 303-311
• 87 Raposo G, Nijman H W, Stoorvogel W et al.. B lymphocytes secrete antigen-presenting vesicles.  J Exp Med. 1996;  183 1161-1172
• 88 Combes V, Simon A C, Grau G E et al.. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant.  J Clin Invest. 1999;  104 93-102
• 89 Berckmans R J, Neiuwland R, Boing A N, Romijn F P, Hack C E, Sturk A. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation.  Thromb Haemost. 2001;  85 639-646
• 90 Mallat Z, Benamer H, Hugel B et al.. Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes.  Circulation. 2000;  101 841-843
• 91 Bernal-Mizrachi L, Jy W, Jimenez J J et al.. High levels of circulating endothelial microparticles in patients with acute coronary syndromes.  Am Heart J. 2003;  145 962-970
• 92 Katopodis J N, Kolodny L, Jy W et al.. Platelet microparticles and calcium homeostasis in acute coronary ischemias.  Am J Hematol. 1997;  54 95-101
• 93 VanWijk M J, Nieuwland R, Boer K, van der Post J A, VanBavel E, Sturk A. Microparticle subpopulations are increased in preeclampsia: possible involvement in vascular dysfunction?.  Am J Obstet Gynecol. 2002;  187 450-456
• 94 Jimenez J J, Jy W, Mauro L M, Horstman L L, Soderland C, Ahn Y S. Endothelial microparticles released in thrombotic thrombocytopenic purpura express von Willebrand factor and markers of endothelial activation.  Br J Haematol. 2003;  123 896-902
• 95 Dignat-George F, Camoin-Jau L, Sabatier F et al.. Endothelial microparticles: a potential contribution to the thrombotic complications of the antiphospholipid syndrome.  Thromb Haemost. 2004;  91 667-673
• 96 Lee Y J, Jy W, Horstman L L et al.. Elevated platelet microparticles in transient ischemic attacks, lacunar infarcts, and multiinfarct dementias.  Thromb Res. 1993;  72 295-304
• 97 Warkentin T E, Hayward C P, Boshkov L K et al.. Sera from patients with heparin-induced thrombocytopenia generate platelet-derived microparticles with procoagulant activity: an explanation for the thrombotic complications of heparin-induced thrombocytopenia.  Blood. 1994;  84 3691-3699
• 98 Lee Y J, Jy W, Horstman L L et al.. Elevated platelet microparticles in transient ischemic attacks, lacunar infarcts, and multiinfarct dementias.  Thromb Res. 1993;  72 295-304
• 99 Holme P A, Orvim U, Hamers M J et al.. Shear-induced platelet activation and platelet microparticle formation at blood flow conditions as in arteries with a severe stenosis.  Arterioscler Thromb Vasc Biol. 1997;  17 646-653
• 100 Sandberg H, Bode A P, Dombrose F A, Hoechli M, Lentz B R. Expression of coagulant activity in human platelets: release of membranous vesicles providing platelet factor 1 and platelet factor 3.  Thromb Res. 1985;  39 63-79
• 101 Sims P J, Faioni E M, Wiedmer T, Shattil S J. Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity.  J Biol Chem. 1988;  263 18205-18212
• 102 Pasquet J M, Toti F, Nurden A T, Dachary-Prigent J. Procoagulant activity and active calpain in platelet-derived microparticles.  Thromb Res. 1996;  82 509-522
• 103 Jy W, Mao W W, Horstman L, Tao J, Ahn Y S. Platelet microparticles bind, activate and aggregate neutrophils in vitro.  Blood Cells Mol Dis. 1995;  21 217-231
• 104 George J N, Pickett E B, Saucerman S et al.. Platelet surface glycoproteins. Studies on resting and activated platelets and platelet membrane microparticles in normal subjects, and observations in patients during adult respiratory distress syndrome and cardiac surgery.  J Clin Invest. 1986;  78 340-348
• 105 Abrams C S, Ellison N, Budzynski A Z, Shattil S J. Direct detection of activated platelets and platelet-derived microparticles in humans.  Blood. 1990;  75 128-138
• 106 Nomura S, Yanabu M, Miyake T et al.. Relationship of microparticles with beta 2-glycoprotein I and P-selectin positivity to anticardiolipin antibodies in immune thrombocytopenic purpura.  Ann Hematol. 1995;  70 25-30
• 107 Jy W, Horstman L L, Wang F, Duncan R C, Ahn Y S. Platelet factor 3 in plasma fractions: its relation to microparticle size and thromboses.  Thromb Res. 1995;  80 471-482
• 108 Zeiger F, Stephan S, Hoheisel G, Pfeiffer D, Ruehlmann C, Koksch M. P-Selectin expression, platelet aggregates, and platelet-derived microparticle formation are increased in peripheral arterial disease.  Blood Coagul Fibrinolysis. 2000;  11 723-728
• 109 Rauch U, Bonderman D, Bohrmann B et al.. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor.  Blood. 2000;  96 170-175
• 110 Carson S D, Perry G A, Pirruccello S J. Fibroblast tissue factor: calcium and ionophore induce shape changes, release of membrane vesicles, and redistribution of tissue factor antigen in addition to increased procoagulant activity.  Blood. 1994;  84 526-534
• 111 Kagawa H, Komiyama Y, Nakamura S et al.. Expression of functional tissue factor on small vesicles of lipopolysaccharide-stimulated human vascular endothelial cells.  Thromb Res. 1998;  91 297-304
• 112 Mallat Z, Tedgui A. Current perspective on the role of apoptosis in atherothrombotic disease.  Circ Res. 2001;  88 998-1003
• 113 Nieuwland R, Berckmans R J, Rotteveel-Eijkman R C et al.. Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant.  Circulation. 1997;  96 3534-3541
• 114 Schecter A D, Spirn B, Rossikhina M et al.. Release of active tissue factor by human arterial smooth muscle cells.  Circ Res. 2000;  87 126-132
• 115 Chou J, Mackman N, Merrill-Skoloff G, Pedersen B, Furie B C, Furie B. Hematopoietic cell-derived microparticle tissue factor contributes to fibrin formation during thrombus propagation.  Blood. 2004;  104 3190-3197
• 116 Day S M, Reeve J L, Pedersen B et al.. Macrovascular thrombosis is driven by tissue factor derived primarily from the blood vessel wall.  Blood. 2005;  105 192-198
• 117 Jin M, Drwal G, Bourgeois T, Saltz J, Wu H M. Distinct proteome features of plasma microparticles.  Proteomics. 2005;  5 1940-1952
• 118 Sambola A, Osende J, Hathcock J et al.. Role of risk factors in the modulation of tissue factor activity and blood thrombogenicity.  Circulation. 2003;  107 973-977
• 119 Bogdanov V Y, Balasubramanian V, Hathcock J, Vele O, Lieb M, Nemerson Y. Alternatively spliced human tissue factor: a circulating, soluble, thrombogenic protein.  Nat Med. 2003;  9 458-462
• 120 Takahashi H, Satoh N, Wada K, Takakuwa E, Seki Y, Shibata A. Tissue factor in plasma of patients with disseminated intravascular coagulation.  Am J Hematol. 1994;  46 333-337
• 121 Asakura H, Kamikubo Y, Goto A et al.. Role of tissue factor in disseminated intravascular coagulation.  Thromb Res. 1995;  80 217-224
• 122 Østerud B. Tissue factor in neutrophils. No.  J Thromb Haemost. 2003;  2 218-220
• 123 Nakamura S, Imamura T, Okamoto K. Tissue factor in neutrophils: yes.  J Thromb Haemost. 2004;  2 214-217
• 124 Higure A, Okamoto K, Hirata K et al.. Macrophages and neutrophils infiltrating into the liver are responsible for tissue factor expression in a rabbit model of acute obstructive cholangitis.  Thromb Haemost. 1996;  75 791-795
• 125 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
• 126 Muller I, Klocke A, Alex M et al.. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets.  FASEB J. 2003;  17 476-478
• 127 Siddiqui F A, Desai H, Amirkhosravi A, Amaya M, Francis J L. The presence and release of tissue factor from human platelets.  Platelets. 2002;  13 247-253
• 128 Camera M, Frigerio M, Toschi V et al.. Platelet activation induces cell-surface immunoreactive tissue factor expression, which is modulated differently by antiplatelet drugs.  Arterioscler Thromb Vasc Biol. 2003;  23 1690-1696
• 129 So A K, Varisco P A, Kemkes-Matthes B et al.. Arthritis is linked to local and systemic activation of coagulation and fibrinolysis pathways.  J Thromb Haemost. 2003;  1 2510-2515
• 130 Bogdanov Y, Hathcock J, Nemerson Y. Active tissue factor in blood.  Nat Med. 2004;  10 1155-1156