Download PDF
Semin Thromb Hemost 2015; 41(07): 708-717
DOI: 10.1055/s-0035-1564045
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Role of Tissue Factor in the Coagulation Network

Giovanni Cimmino
1   Division of Cardiology, Department of Cardio-Thoracic Sciences, Second University of Naples, Naples, Italy
,
Giovanni Ciccarelli
1   Division of Cardiology, Department of Cardio-Thoracic Sciences, Second University of Naples, Naples, Italy
,
Paolo Golino
1   Division of Cardiology, Department of Cardio-Thoracic Sciences, Second University of Naples, Naples, Italy
› Author Affiliations
Further Information

Publication History

Publication Date:
26 September 2015 (online)

    Permissions and Reprints

Abstract

It is generally accepted that the initial event in coagulation and intravascular thrombus formation is the exposure of the flowing blood to cell-surface protein, such as tissue factor (TF). Vascular injury and/or atherosclerotic plaque complication is responsible for this exposure, leading to clinical manifestations such as acute coronary syndromes. For many years, TF has been considered one of the major determinants of plaque-related thrombosis. However, the discoveries of different pools of TF that circulates in the blood as cell-associated TF, microparticles bound, and as soluble form have changed this dogma. Recent evidence suggests that an increased circulating TF activity may potentiate the initial thrombogenic stimulus related to vessel wall–associated TF, leading to the formation of larger and/or more stable thrombus and thus more severe clinical manifestations. Different pathological conditions, such as inflammatory status, enhance TF expression and activity. Conversely, TF upregulation may facilitate inflammation by formation of proinflammatory fibrin fragments and coagulation proteases generation, including FVIIa, FXa, and thrombin. Furthermore, the biology of TF has become more complex by the demonstration that, apart from its known effects on blood coagulation, it is involved in intracellular signaling, proliferation, angiogenesis, and tumor metastasis.

Keywords

coagulation cascade - tissue factor - thrombus formation - atherothrombosis
 

  • References

  • 1 Toschi V, Gallo R, Lettino M , et al. Tissue factor modulates the thrombogenicity of human atherosclerotic plaques. Circulation 1997; 95 (3) 594-599
    CrossrefPubMedGoogle Scholar
  • 2 Cimmino G, D'Amico C, Vaccaro V, D'Anna M, Golino P. The missing link between atherosclerosis, inflammation and thrombosis: is it tissue factor?. Expert Rev Cardiovasc Ther 2011; 9 (4) 517-523
    CrossrefPubMedGoogle Scholar
  • 3 Cimmino G, Golino P, Badimon JJ. Pathophysiological role of blood-borne tissue factor: should the old paradigm be revisited?. Intern Emerg Med 2011; 6 (1) 29-34
    PubMedGoogle Scholar
  • 4 Cirillo P, Calì G, Golino P , et al. Tissue factor binding of activated factor VII triggers smooth muscle cell proliferation via extracellular signal-regulated kinase activation. Circulation 2004; 109 (23) 2911-2916
    CrossrefPubMedGoogle Scholar
  • 5 van den Berg YW, Versteeg HH. Alternatively spliced tissue factor. A crippled protein in coagulation or a key player in non-haemostatic processes?. Hamostaseologie 2010; 30 (3) 144-149
    PubMedGoogle Scholar
  • 6 van den Berg YW, van den Hengel LG, Myers HR , et al. Alternatively spliced tissue factor induces angiogenesis through integrin ligation. Proc Natl Acad Sci U S A 2009; 106 (46) 19497-19502
    CrossrefPubMedGoogle Scholar
  • 7 Chu AJ. Tissue factor, blood coagulation, and beyond: an overview. Int J Inflamm 2011; 2011: 367284
    PubMedGoogle Scholar
  • 8 Bächli E. History of tissue factor. Br J Haematol 2000; 110 (2) 248-255
    CrossrefPubMedGoogle Scholar
  • 9 Davie EW. A brief historical review of the waterfall/cascade of blood coagulation. J Biol Chem 2003; 278 (51) 50819-50832
    CrossrefPubMedGoogle Scholar
  • 10 Beck EA. The chemistry of blood coagulation: a summary by Paul Morawitz (1905). Thromb Haemost 1977; 37 (3) 376-379
    PubMedGoogle Scholar
  • 11 Horne RM. The action of calcium, strontium and barium salts in preventing coagulation of the blood. J Physiol 1896; 19 (4) 356-371
    CrossrefPubMedGoogle Scholar
  • 12 Hjort PF. Intermediate reactions in the coagulation of blood with tissue thromboplastin; convertin, accelerin, prothrombinase. Scand J Clin Lab Invest 1957; 9 (Suppl. 27) 1-183
    CrossrefPubMedGoogle Scholar
  • 13 Quick AJ. The one-stage prothrombin time determination. Its history and interpretation. Chemotherapia (Basel) 1961; 3: 313-320
    CrossrefPubMedGoogle Scholar
  • 14 Nemerson Y. The reaction between bovine brain tissue factor and factors VII and X. Biochemistry 1966; 5 (2) 601-608
    CrossrefPubMedGoogle Scholar
  • 15 Broze Jr GJ, Leykam JE, Schwartz BD, Miletich JP. Purification of human brain tissue factor. J Biol Chem 1985; 260 (20) 10917-10920
    PubMedGoogle Scholar
  • 16 Fisher KL, Gorman CM, Vehar GA, O'Brien DP, Lawn RM. Cloning and expression of human tissue factor cDNA. Thromb Res 1987; 48 (1) 89-99
    CrossrefPubMedGoogle Scholar
  • 17 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 (1) 129-135
    CrossrefPubMedGoogle Scholar
  • 18 Scarpati EM, Wen D, Broze Jr GJ , et al. Human tissue factor: cDNA sequence and chromosome localization of the gene. Biochemistry 1987; 26 (17) 5234-5238
    CrossrefPubMedGoogle Scholar
  • 19 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 (15) 5148-5152
    CrossrefPubMedGoogle Scholar
  • 20 Bazan JF. Structural design and molecular evolution of a cytokine receptor superfamily. Proc Natl Acad Sci U S A 1990; 87 (18) 6934-6938
    CrossrefPubMedGoogle Scholar
  • 21 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 (4) 1755-1762
    CrossrefPubMedGoogle Scholar
  • 22 Paborsky LR, Caras IW, Fisher KL, Gorman CM. Lipid association, but not the transmembrane domain, is required for tissue factor activity. Substitution of the transmembrane domain with a phosphatidylinositol anchor. J Biol Chem 1991; 266 (32) 21911-21916
    PubMedGoogle Scholar
  • 23 Sharma L, Melis E, Hickey MJ , et al. The cytoplasmic domain of tissue factor contributes to leukocyte recruitment and death in endotoxemia. Am J Pathol 2004; 165 (1) 331-340
    CrossrefPubMedGoogle Scholar
  • 24 Paborsky LR, Tate KM, Harris RJ , et al. Purification of recombinant human tissue factor. Biochemistry 1989; 28 (20) 8072-8077
    CrossrefPubMedGoogle Scholar
  • 25 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 (5) 1087-1097
    PubMedGoogle Scholar
  • 26 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 (2) 421-437
    CrossrefPubMedGoogle Scholar
  • 27 Broze Jr GJ, Majerus PW. Purification and properties of human coagulation factor VII. J Biol Chem 1980; 255 (4) 1242-1247
    PubMedGoogle Scholar
  • 28 Gladhaug A, Prydz H. Purification of the coagulation factors VII and X from human serum. Some properties of factor VII. Biochim Biophys Acta 1970; 215 (1) 105-111
    CrossrefPubMedGoogle Scholar
  • 29 Vadivel K, Bajaj SP. Structural biology of factor VIIa/tissue factor initiated coagulation. Front Biosci (Landmark Ed) 2012; 17: 2476-2494
    CrossrefPubMedGoogle Scholar
  • 30 Radcliffe R, Nemerson Y. Activation and control of factor VII by activated factor X and thrombin. Isolation and characterization of a single chain form of factor VII. J Biol Chem 1975; 250 (2) 388-395
    PubMedGoogle Scholar
  • 31 Rao LV, Bajaj SP, Rapaport SI. Activation of human factor VII during clotting in vitro. Blood 1985; 65 (1) 218-226
    PubMedGoogle Scholar
  • 32 Sabharwal AK, Birktoft JJ, Gorka J, Wildgoose P, Petersen LC, Bajaj SP. 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 (26) 15523-15530
    CrossrefPubMedGoogle Scholar
  • 33 Irie A, Takahashi S, Katayama Y, Ito K, Miyake Y. Human urinary prokallikrein: rapid purification and model activation by trypsin. Biochem Int 1986; 13 (2) 375-382
    PubMedGoogle Scholar
  • 34 Ruf W, Rehemtulla A, Morrissey JH, Edgington TS. Phospholipid-independent and -dependent interactions required for tissue factor receptor and cofactor function. J Biol Chem 1991; 266 (4) 2158-2166
    PubMedGoogle Scholar
  • 35 Fiore MM, Neuenschwander PF, Morrissey JH. 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 (1) 143-149
    PubMedGoogle Scholar
  • 36 Zhong D, Bajaj MS, Schmidt AE, Bajaj SP. The N-terminal epidermal growth factor-like domain in factor IX and factor X represents an important recognition motif for binding to tissue factor. J Biol Chem 2002; 277 (5) 3622-3631
    CrossrefPubMedGoogle Scholar
  • 37 Wilkinson FH, Ahmad SS, Walsh PN. The factor IXa second epidermal growth factor (EGF2) domain mediates platelet binding and assembly of the factor X activating complex. J Biol Chem 2002; 277 (8) 5734-5741
    CrossrefPubMedGoogle Scholar
  • 38 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 (5) 2311-2315
    CrossrefPubMedGoogle Scholar
  • 39 Østerud B, Bjørklid E. Sources of tissue factor. Semin Thromb Hemost 2006; 32 (1) 11-23
    Article in Thieme ConnectPubMedGoogle Scholar
  • 40 Brambilla M, Camera M, Colnago D , et al. Tissue factor in patients with acute coronary syndromes: expression in platelets, leukocytes, and platelet-leukocyte aggregates. Arterioscler Thromb Vasc Biol 2008; 28 (5) 947-953
    CrossrefPubMedGoogle Scholar
  • 41 Lechner D, Weltermann A. Circulating tissue factor-exposing microparticles. Thromb Res 2008; 122 (Suppl. 01) S47-S54
    CrossrefPubMedGoogle Scholar
  • 42 Bogdanov VY, Balasubramanian V, Hathcock J, Vele O, Lieb M, Nemerson Y. Alternatively spliced human tissue factor: a circulating, soluble, thrombogenic protein. Nat Med 2003; 9 (4) 458-462
    Google Scholar
  • 43 Rivers RP, Hathaway WE, Weston WL. The endotoxin-induced coagulant activity of human monocytes. Br J Haematol 1975; 30 (3) 311-316
    CrossrefPubMedGoogle Scholar
  • 44 Maugeri N, Brambilla M, Camera M , et al. Human polymorphonuclear leukocytes produce and express functional tissue factor upon stimulation. J Thromb Haemost 2006; 4 (6) 1323-1330
    CrossrefPubMedGoogle Scholar
  • 45 Sovershaev MA, Lind KF, Devold H , et al. No evidence for the presence of tissue factor in high-purity preparations of immunologically isolated eosinophils. J Thromb Haemost 2008; 6 (10) 1742-1749
    CrossrefPubMedGoogle Scholar
  • 46 Darbousset R, Thomas GM, Mezouar S , et al. Tissue factor-positive neutrophils bind to injured endothelial wall and initiate thrombus formation. Blood 2012; 120 (10) 2133-2143
    CrossrefPubMedGoogle Scholar
  • 47 Egorina EM, Sovershaev MA, Olsen JO, Østerud B. Granulocytes do not express but acquire monocyte-derived tissue factor in whole blood: evidence for a direct transfer. Blood 2008; 111 (3) 1208-1216
    CrossrefPubMedGoogle Scholar
  • 48 Bouchard BA, Mann KG, Butenas S. No evidence for tissue factor on platelets. Blood 2010; 116 (5) 854-855
    CrossrefPubMedGoogle Scholar
  • 49 Camera M, Brambilla M, Toschi V, Tremoli E. Tissue factor expression on platelets is a dynamic event. Blood 2010; 116 (23) 5076-5077
    CrossrefPubMedGoogle Scholar
  • 50 Zillmann A, Luther T, Müller I , et al. Platelet-associated tissue factor contributes to the collagen-triggered activation of blood coagulation. Biochem Biophys Res Commun 2001; 281 (2) 603-609
    CrossrefPubMedGoogle Scholar
  • 51 Weyrich AS, Lindemann S, Tolley ND , et al. Change in protein phenotype without a nucleus: translational control in platelets. Semin Thromb Hemost 2004; 30 (4) 491-498
    Article in Thieme ConnectPubMedGoogle Scholar
  • 52 Mezzano D, Panes O. Regulation of platelet-expressed tissue factor. J Thromb Haemost 2009; 7 (Suppl. 02) Abstract AS-MO-041
    PubMedGoogle Scholar
  • 53 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 (9) 1690-1696
    CrossrefPubMedGoogle Scholar
  • 54 Camera M, Brambilla M, Facchinetti L , et al. Tissue factor and atherosclerosis: not only vessel wall-derived TF, but also platelet-associated TF. Thromb Res 2012; 129 (3) 279-284
    CrossrefPubMedGoogle Scholar
  • 55 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 (11) 2433-2440
    CrossrefPubMedGoogle Scholar
  • 56 Rauch U, Nemerson Y. Circulating tissue factor and thrombosis. Curr Opin Hematol 2000; 7 (5) 273-277
    CrossrefPubMedGoogle Scholar
  • 57 Cimmino GBG, Conte S, Pellegrino G , et al. Expression of Functional Tissue Factor in Activated T-Lymphocytes: A Contribution to Thrombosis? ACC Scientific Session; 2014
    PubMed
  • 58 Chargaff E, West R. The biological significance of the thromboplastic protein of blood. J Biol Chem 1946; 166 (1) 189-197
    PubMedGoogle Scholar
  • 59 Biró 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 (12) 2561-2568
    CrossrefPubMedGoogle Scholar
  • 60 Davizon P, López JA. Microparticles and thrombotic disease. Curr Opin Hematol 2009; 16 (5) 334-341
    CrossrefPubMedGoogle Scholar
  • 61 Reininger AJ, Bernlochner I, Penz SM , et al. A 2-step mechanism of arterial thrombus formation induced by human atherosclerotic plaques. J Am Coll Cardiol 2010; 55 (11) 1147-1158
    CrossrefPubMedGoogle Scholar
  • 62 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 (1) 192-198
    CrossrefPubMedGoogle Scholar
  • 63 Balasubramanian V, Grabowski E, Bini A, Nemerson Y. Platelets, circulating tissue factor, and fibrin colocalize in ex vivo thrombi: real-time fluorescence images of thrombus formation and propagation under defined flow conditions. Blood 2002; 100 (8) 2787-2792
    CrossrefPubMedGoogle Scholar
  • 64 Bach RR. Tissue factor encryption. Arterioscler Thromb Vasc Biol 2006; 26 (3) 456-461
    CrossrefPubMedGoogle Scholar
  • 65 Ploplis VA, Edgington TS, Fair DS. Initiation of the extrinsic pathway of coagulation. Association of factor VIIa with a cell line expressing tissue factor. J Biol Chem 1987; 262 (20) 9503-9508
    PubMedGoogle Scholar
  • 66 Sakai T, Lund-Hansen T, Paborsky L, Pedersen AH, Kisiel W. Binding of human factors VII and VIIa to a human bladder carcinoma cell line (J82). Implications for the initiation of the extrinsic pathway of blood coagulation. J Biol Chem 1989; 264 (17) 9980-9988
    PubMedGoogle Scholar
  • 67 Le DT, Rapaport SI, Rao LV. Relations between factor VIIa binding and expression of factor VIIa/tissue factor catalytic activity on cell surfaces. J Biol Chem 1992; 267 (22) 15447-15454
    PubMedGoogle Scholar
  • 68 Henriksson CE, Klingenberg O, Hellum M , et al. Calcium ionophore-induced de-encryption of tissue factor in monocytes is associated with extensive cell death. Thromb Res 2007; 119 (5) 621-630
    CrossrefPubMedGoogle Scholar
  • 69 Mallat Z, Hugel B, Ohan J, Lesèche G, Freyssinet JM, Tedgui A. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity. Circulation 1999; 99 (3) 348-353
    CrossrefPubMedGoogle Scholar
  • 70 Leroyer AS, Isobe H, Lesèche G , et al. Cellular origins and thrombogenic activity of microparticles isolated from human atherosclerotic plaques. J Am Coll Cardiol 2007; 49 (7) 772-777
    CrossrefPubMedGoogle Scholar
  • 71 Berckmans RJ, Nieuwland R, Böing AN, Romijn FP, Hack CE, Sturk A. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost 2001; 85 (4) 639-646
    PubMedGoogle Scholar
  • 72 Giannarelli C, Alique M, Rodriguez DT , et al. Alternatively spliced tissue factor promotes plaque angiogenesis through the activation of hypoxia-inducible factor-1α and vascular endothelial growth factor signaling. Circulation 2014; 130 (15) 1274-1286
    CrossrefPubMedGoogle Scholar
  • 73 Bogdanov VY, Cimmino G, Tardos JG, Tunstead JR, Badimon JJ. Assessment of plasma tissue factor activity in patients presenting with coronary artery disease: limitations of a commercial assay. J Thromb Haemost 2009; 7 (5) 894-897
    CrossrefPubMedGoogle Scholar
  • 74 Cimmino G , et al. Decreased blood-borne tissue factor activity in patients presenting with acute coronary syndrome: should the old paradigm be revisited?. Circulation 2010; 122: A19396
    PubMedGoogle Scholar
  • 75 Broze Jr GJ. The rediscovery and isolation of TFPI. J Thromb Haemost 2003; 1 (8) 1671-1675
    CrossrefPubMedGoogle Scholar
  • 76 Broze Jr GJ, Girard TJ. Tissue factor pathway inhibitor: structure-function. Front Biosci (Landmark Ed) 2012; 17: 262-280
    CrossrefPubMedGoogle Scholar
  • 77 Golino P, Ragni M, Cimmino G, Forte L. Role of tissue factor pathway inhibitor in the regulation of tissue factor-dependent blood coagulation. Cardiovasc Drug Rev 2002; 20 (1) 67-80
    PubMedGoogle Scholar
  • 78 Girard TJ, Warren LA, Novotny WF , et al. Functional significance of the Kunitz-type inhibitory domains of lipoprotein-associated coagulation inhibitor. Nature 1989; 338 (6215) 518-520
    Google Scholar
  • 79 Wesselschmidt R, Likert K, Girard T, Wun TC, Broze Jr GJ. Tissue factor pathway inhibitor: the carboxy-terminus is required for optimal inhibition of factor Xa. Blood 1992; 79 (8) 2004-2010
    PubMedGoogle Scholar
  • 80 Wesselschmidt R, Likert K, Huang Z, MacPhail L, Broze Jr GJ. Structural requirements for tissue factor pathway inhibitor interactions with factor Xa and heparin. Blood Coagul Fibrinolysis 1993; 4 (5) 661-669
    CrossrefPubMedGoogle Scholar
  • 81 Piro O, Broze Jr GJ. Role for the Kunitz-3 domain of tissue factor pathway inhibitor-alpha in cell surface binding. Circulation 2004; 110 (23) 3567-3572
    Google Scholar
  • 82 Baugh RJ, Broze Jr GJ, Krishnaswamy S. Regulation of extrinsic pathway factor Xa formation by tissue factor pathway inhibitor. J Biol Chem 1998; 273 (8) 4378-4386
    CrossrefPubMedGoogle Scholar
  • 83 Lesnik P, Vonica A, Guérin M, Moreau M, Chapman MJ. Anticoagulant activity of tissue factor pathway inhibitor in human plasma is preferentially associated with dense subspecies of LDL and HDL and with Lp(a). Arterioscler Thromb 1993; 13 (7) 1066-1075
    CrossrefPubMedGoogle Scholar
  • 84 Novotny WF, Girard TJ, Miletich JP, Broze Jr GJ. Purification and characterization of the lipoprotein-associated coagulation inhibitor from human plasma. J Biol Chem 1989; 264 (31) 18832-18837
    Google Scholar
  • 85 Novotny WF, Girard TJ, Miletich JP, Broze Jr GJ. Platelets secrete a coagulation inhibitor functionally and antigenically similar to the lipoprotein associated coagulation inhibitor. Blood 1988; 72 (6) 2020-2025
    Google Scholar
  • 86 Sandset PM, Abildgaard U, Larsen ML. Heparin induces release of extrinsic coagulation pathway inhibitor (EPI). Thromb Res 1988; 50 (6) 803-813
    CrossrefPubMedGoogle Scholar
  • 87 Ellery PE, Hardy K, Oostryck R, Adams MJ. Further insight into the heparin-releasable and glycosylphosphatidylinositol-lipid—anchored forms of tissue factor pathway inhibitor. Clin Appl Thromb Hemost 2008; 14 (3) 267-278
    CrossrefPubMedGoogle Scholar
  • 88 Golino P, Cimmino G. Targeting tissue factor as an antithrombotic strategy. Semin Vasc Med 2003; 3 (2) 205-214
    Article in Thieme ConnectPubMedGoogle Scholar
  • 89 Ragni M, Golino P, Cirillo P , et al. Endogenous tissue factor pathway inhibitor modulates thrombus formation in an in vivo model of rabbit carotid artery stenosis and endothelial injury. Circulation 2000; 102 (1) 113-117
    CrossrefPubMedGoogle Scholar
  • 90 Haskel EJ, Torr SR, Day KC , et al. Prevention of arterial reocclusion after thrombolysis with recombinant lipoprotein-associated coagulation inhibitor. Circulation 1991; 84 (2) 821-827
    CrossrefPubMedGoogle Scholar
  • 91 Oltrona L, Speidel CM, Recchia D, Wickline SA, Eisenberg PR, Abendschein DR. Inhibition of tissue factor-mediated coagulation markedly attenuates stenosis after balloon-induced arterial injury in minipigs. Circulation 1997; 96 (2) 646-652
    CrossrefPubMedGoogle Scholar
  • 92 Golino P, Cirillo P, Calabro' P , et al. Expression of exogenous tissue factor pathway inhibitor in vivo suppresses thrombus formation in injured rabbit carotid arteries. J Am Coll Cardiol 2001; 38 (2) 569-576
    CrossrefPubMedGoogle Scholar
  • 93 Versteeg HH, Spek CA, Peppelenbosch MP, Richel DJ. Tissue factor and cancer metastasis: the role of intracellular and extracellular signaling pathways. Mol Med 2004; 10 (1–6) 6-11
    CrossrefPubMedGoogle Scholar
  • 94 Antoniak S, Pawlinski R, Mackman N. Protease-activated receptors and myocardial infarction. IUBMB Life 2011; 63 (6) 383-389
    CrossrefPubMedGoogle Scholar
  • 95 Borissoff JI, Spronk HM, ten Cate H. The hemostatic system as a modulator of atherosclerosis. N Engl J Med 2011; 364 (18) 1746-1760
    CrossrefPubMedGoogle Scholar
  • 96 Pyo RT, Sato Y, Mackman N, Taubman MB. Mice deficient in tissue factor demonstrate attenuated intimal hyperplasia in response to vascular injury and decreased smooth muscle cell migration. Thromb Haemost 2004; 92 (3) 451-458
    PubMedGoogle Scholar
  • 97 Demetz G, Seitz I, Stein A , et al. Tissue Factor-Factor VIIa complex induces cytokine expression in coronary artery smooth muscle cells. Atherosclerosis 2010; 212 (2) 466-471
    CrossrefPubMedGoogle Scholar
  • 98 Ardissino D, Merlini PA, Ariëns R, Coppola R, Bramucci E, Mannucci PM. Tissue-factor antigen and activity in human coronary atherosclerotic plaques. Lancet 1997; 349 (9054) 769-771
    CrossrefPubMedGoogle Scholar
  • 99 Hutter R, Valdiviezo C, Sauter BV , et al. Caspase-3 and tissue factor expression in lipid-rich plaque macrophages: evidence for apoptosis as link between inflammation and atherothrombosis. Circulation 2004; 109 (16) 2001-2008
    CrossrefPubMedGoogle Scholar
  • 100 Cirillo P, Golino P, Calabrò P , et al. C-reactive protein induces tissue factor expression and promotes smooth muscle and endothelial cell proliferation. Cardiovasc Res 2005; 68 (1) 47-55
    CrossrefPubMedGoogle Scholar
  • 101 Cirillo P, Angri V, De Rosa S , et al. Pro-atherothrombotic effects of leptin in human coronary endothelial cells. Thromb Haemost 2010; 103 (5) 1065-1075
    Article in Thieme ConnectPubMedGoogle Scholar
  • 102 Cirillo P, Ziviello F, Pellegrino G , et al. The adipokine apelin-13 induces expression of prothrombotic tissue factor. Thromb Haemost 2015; 113 (2) 363-372
    PubMedGoogle Scholar