37
Views
1
CrossRef citations to date
0
Altmetric
ORIGINAL ARTICLE

Role of Tissue Factor in Cancer

, &
Pages 53-62 | Published online: 11 Jun 2009

REFERENCES

  • Spicer E. K., Horton R., Bloem L., Bach R., Williams K. R., Guha A., Kraus J., Lin T. C., Nemerson Y., Konigsberg W. H. Isolation of cDNA clones coding for human tissue factor: primary structure of the protein and cDNA. Proc Natl Acad Sci USA 1987; 84(15)5148–5152
  • Morrissey J. H., Fakhrai H., Edgington T. S. 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
  • Scarpati E. M., Wen D., Broze G. J., Jr., Miletich J. P., Flandermeyer R. R., Siegel N. R., Sadler J. E. Human tissue factor: cDNA sequence and chromosome localization of the gene. Biochemistry 1987; 26(17)5234–5238
  • Fisher K. L., Gorman C. M., Vehar G. A., O'Brien D. P., Lawn R. M. Cloning and expression of human tissue factor cDNA. Thromb Res 1987; 48(1)89–99
  • 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(4)458–462
  • Chand H. S., Ness S. A., Kisiel W. Identification of a novel human tissue factor splice variant that is upregulated in tumor cells. Int J Cancer 2006; 118(7)1713–1720
  • Edgington T. S., Mackman N., Brand K., Ruf W. The structural biology of expression and function of tissue factor. Thromb Haemost 1991; 66(1)67–79
  • Taubman M. B., Marmur J. D., Rosenfield C. L., Guha A., Nichtberger S., Nemerson Y. Agonist-mediated tissue factor expression in cultured vascular smooth muscle cells. Role of Ca2+ mobilization and protein kinase C activation. J Clin Invest 1993; 91(2)547–552
  • Cui M. Z., Parry G. C., Edgington T. S., Mackman N. Regulation of tissue factor gene expression in epithelial cells. Induction by serum and phorbol 12-myristate 13-acetate. Arterioscler Thromb 1994; 14(5)807–814
  • Mackman N. Regulation of the tissue factor gene. Faseb J 1995; 9(10)883–889
  • Eilertsen K. E., Osterud B. Tissue factor: (patho)physiology and cellular biology. Blood Coagul Fibrinolysis 2004; 15(7)521–538
  • Bugge T. H., Xiao Q., Kombrinck K. W., Flick M. J., Holmback K., Danton M. J., Colbert M. C., Witte D. P., Fujikawa K., Davie E. W., Degen J. L. Fatal embryonic bleeding events in mice lacking tissue factor, the cell-associated initiator of blood coagulation. Proc Natl Acad Sci USA 1996; 93(13)6258–6263
  • Toomey J. R., Kratzer K. E., Lasky N. M., Stanton J. J., Broze G. J., Jr. Targeted disruption of the murine tissue factor gene results in embryonic lethality. Blood 1996; 88(5)1583–1587
  • Carmeliet P., Mackman N., Moons L., Luther T., Gressens P., Van Vlaenderen I., Demunck H., Kasper M., Breier G., Evrard P., Muller M., Risau W., Edgington T., Collen D. Role of tissue factor in embryonic blood vessel development. Nature 1996; 383(6595)73–75
  • Osterud 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 USA 1977; 74(12)5260–5264
  • Nemerson Y. Tissue factor and hemostasis. Blood 1988; 71(1)1–8
  • Komiyama Y., Pedersen A. H., 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(40)9418–9425
  • Mackman N., Tilley R. E., Key N. S. Role of the extrinsic pathway of blood coagulation in hemostasis and thrombosis. Arterioscler Thromb Vasc Biol 2007; 27(8)1687–1693
  • Belting M., Ahamed J., Ruf W. Signaling of the tissue factor coagulation pathway in angiogenesis and cancer. Arterioscler Thromb Vasc Biol 2005; 25(8)1545–1550
  • Ruf W. Tissue factor and PAR signaling in tumor progression. Thromb Res 2007; 120(Suppl. 2)S7–S12
  • 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(5)1087–1097
  • 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. Thromb Res 1990; 59(2)421–437
  • Contrino J., Hair G., Kreutzer D. L., Rickles F. R. In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nature Med 1996; 2(2)209–215
  • Shoji M., Hancock W. W., Abe K., Micko C., Casper K. A., Baine R. M., Wilcox J. N., Danave I., Dillehay D. L., Matthews E., Contrino J., Morrissey J. H., Gordon S., Edgington T. S., Kudryk B., Kreutzer D. L., Rickles F. R. Activation of coagulation and angiogenesis in cancer: immunohistochemical localization in situ of clotting proteins and vascular endothelial growth factor in human cancer. Am J Pathol 1998; 152(2)399–411
  • 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(4)247–253
  • Biro E., Sturk-Maquelin K. N., Vogel G. M., Meuleman D. G., Smit M. J., Hack C. E., Sturk A., Nieuwland R. Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost 2003; 1(12)2561–2568
  • Sturk-Maquelin K. N., Nieuwland R., Romijn F. P., Eijsman L., Hack C. E., Sturk A. Pro- and non-coagulant forms of non-cell-bound tissue factor in vivo. J Thromb Haemost 2003; 1(9)1920–1926
  • Muller I., Klocke A., Alex M., Kotzsch M., Luther T., Morgenstern E., Zieseniss S., Zahler S., Preissner K., Engelmann B. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. Faseb J 2003; 17(3)476–478
  • Takano S., Tsuboi K., Tomono Y., Mitsui Y., Nose T. Tissue factor, osteopontin, alphavbeta3 integrin expression in microvasculature of gliomas associated with vascular endothelial growth factor expression. Br J Cancer 2000; 82(12)1967–1973
  • Guan M., Jin J., Su B., Liu W. W., Lu Y. Tissue factor expression and angiogenesis in human glioma. Clin Biochemistry 2002; 35(4)321–325
  • Vrana J. A., Stang M. T., Grande J. P., Getz M. J. Expression of tissue factor in tumor stroma correlates with progression to invasive human breast cancer: paracrine regulation by carcinoma cell-derived members of the transforming growth factor beta family. Cancer Res 1996; 56(21)5063–5070
  • Ueno T., Toi M., Koike M., Nakamura S., Tominaga T. Tissue factor expression in breast cancer tissues: its correlation with prognosis and plasma concentration. Br J Cancer 2000; 83(2)164–170
  • Koomagi R., Volm M. Tissue-factor expression in human non-small-cell lung carcinoma measured by immunohistochemistry: correlation between tissue factor and angiogenesis. Int J Cancer 1998; 79(1)19–22
  • Sawada M., Miyake S., Ohdama S., Matsubara O., Masuda S., Yakumaru K., Yoshizawa Y. Expression of tissue factor in non-small-cell lung cancers and its relationship to metastasis. Br J Cancer 1999; 79(3–4)472–477
  • Rauch U., Antoniak S., Boots M., Schulze K., Goldin-Lang P., Stein H., Schultheiss H. P., Coupland S. E. Association of tissue-factor upregulation in squamous-cell carcinoma of the lung with increased tissue factor in circulating blood. Lancet Oncol 2005; 6(4)254
  • Hair G. A., Padula S., Zeff R., Schmeizl M., Contrino J., Kreutzer D. L., de Moerloose P., Boyd A. W., Stanley I., Burgess A. W., Rickles F. R. Tissue factor expression in human leukemic cells. Leukemia Res 1996; 20(1)1–11
  • Lopez-Pedrera C., Barbarroja N., Dorado G., Siendones E., Velasco F. Tissue factor as an effector of angiogenesis and tumor progression in hematological malignancies. Leukemia 2006; 20(8)1331–1340
  • Kataoka H., Uchino H., Asada Y., Hatakeyama K., Nabeshima K., Sumiyoshi A., Koono M. Analysis of tissue factor and tissue factor pathway inhibitor expression in human colorectal carcinoma cell lines and metastatic sublines to the liver. Int J Cancer 1997; 72(5)878–884
  • Shigemori C., Wada H., Matsumoto K., Shiku H., Nakamura S., Suzuki H. Tissue factor expression and metastatic potential of colorectal cancer. Thrombosis and Haemostasis 1998; 80(6)894–898
  • Seto S., Onodera H., Kaido T., Yoshikawa A., Ishigami S., Arii S., Imamura M. Tissue factor expression in human colorectal carcinoma: correlation with hepatic metastasis and impact on prognosis. Cancer 2000; 88(2)295–301
  • Nakasaki T., Wada H., Shigemori C., Miki C., Gabazza E. C., Nobori T., Nakamura S., Shiku H. Expression of tissue factor and vascular endothelial growth factor is associated with angiogenesis in colorectal cancer. Am J Hematol 2002; 69(4)247–254
  • Poon R. T., Lau C. P., Ho J. W., Yu W. C., Fan S. T., Wong J. Tissue factor expression correlates with tumor angiogenesis and invasiveness in human hepatocellular carcinoma. Clin Cancer Res 2003; 9(14)5339–5345
  • Kageshita T., Funasaka Y., Ichihashi M., Wakamatsu K., Ito S., Ono T. Tissue factor expression and serum level in patients with melanoma does not correlate with disease progression. Pigment cell research/sponsored by the European Society for Pigment Cell Research and the International Pigment Cell Society 2001; 14(3)195–200
  • Depasquale I., Thompson W. D. Prognosis in human melanoma: PAR-1 expression is superior to other coagulation components and VEGF. Histopathology 2008; 52(4)500–509
  • Abdulkadir S. A., Carvalhal G. F., Kaleem Z., Kisiel W., Humphrey P. A., Catalona W. J., Milbrandt J. Tissue factor expression and angiogenesis in human prostate carcinoma. Hum Pathol 2000; 31(4)443–447
  • Ohta S., Wada H., Nakazaki T., Maeda Y., Nobori T., Shiku H., Nakamura S., Nagakawa O., Furuya Y., Fuse H. Expression of tissue factor is associated with clinical features and angiogenesis in prostate cancer. Anticancer Res 2002; 22(5)2991–2996
  • Akashi T., Furuya Y., Ohta S., Fuse H. Tissue factor expression and prognosis in patients with metastatic prostate cancer. Urology 2003; 62(6)1078–1082
  • Forster Y., Meye A., Albrecht S., Kotzsch M., Fussel S., Wirth M. P., Schwenzer B. Tissue specific expression and serum levels of human tissue factor in patients with urological cancer. Cancer Lett 2003; 193(1)65–73
  • Kakkar A. K., Lemoine N. R., Scully M. F., Tebbutt S., Williamson R. C. Tissue factor expression correlates with histological grade in human pancreatic cancer. Br J Surg 1995; 82(8)1101–1104
  • Ueda C., Hirohata Y., Kihara Y., Nakamura H., Abe S., Akahane K., Okamoto K., Itoh H., Otsuki M. Pancreatic cancer complicated by disseminated intravascular coagulation associated with production of tissue factor. J Gastroenterol 2001; 36(12)848–850
  • Nitori N., Ino Y., Nakanishi Y., Yamada T., Honda K., Yanagihara K., Kosuge T., Kanai Y., Kitajima M., Hirohashi S. Prognostic significance of tissue factor in pancreatic ductal adenocarcinoma. Clin Cancer Res 2005; 11(7)2531–2539
  • Khorana A. A., Ahrendt S. A., Ryan C. K., Francis C. W., Hruban R. H., Hu Y. C., Hostetter G., Harvey J., Taubman M. B. Tissue factor expression, angiogenesis, and thrombosis in pancreatic cancer. Clin Cancer Res 2007; 13(10)2870–2875
  • Han L. Y., Landen C. N., Jr., Kamat A. A., Lopez A., Bender D. P., Mueller P., Schmandt R., Gershenson D. M., Sood A. K. Preoperative serum tissue factor levels are an independent prognostic factor in patients with ovarian carcinoma. J Clin Oncol 2006; 24(5)755–761
  • Patry G., Hovington H., Larue H., Harel F., Fradet Y., Lacombe L. Tissue factor expression correlates with disease-specific survival in patients with node-negative muscle-invasive bladder cancer. Int J Cancer 2008; 122(7)1592–1597
  • Kaushal V., Mukunyadzi P., Siegel E. R., Dennis R. A., Johnson D. E., Kohli M. Expression of tissue factor in prostate cancer correlates with malignant phenotype. Appl Immunohistochem Mol Morphol 2008; 16(1)1–6
  • Chand H. S., Kisiel W. Quantitative real-time reverse transcription polymerase chain reaction analysis of a novel tissue factor splice variant in select human solid tumors. J Thromb Haemost 2007; 5(3)640–641
  • Hobbs J. E., Zakarija A., Cundiff D. L., Doll J. A., Hymen E., Cornwell M., Crawford S. E., Liu N., Signaevsky M., Soff G. A. Alternatively spliced human tissue factor promotes tumor growth and angiogenesis in a pancreatic cancer tumor model. Thromb Res 2007; 120(Suppl. 2)S13–S21
  • Khorana A. A. Malignancy, thrombosis and Trousseau: the case for an eponym. J Thromb Haemost 2003; 1(12)2463–2465
  • Otten H. M., Prins M. H. Venous thromboembolism and occult malignancy. Thromb Res 2001; 102(6)V187–V194
  • Maynard J. R., Dreyer B. E., Stemerman M. B., Pitlick F. A. Tissue-factor coagulant activity of cultured human endothelial and smooth muscle cells and fibroblasts. Blood 1977; 50(3)387–396
  • Colucci M., Balconi G., Lorenzet R., Pietra A., Locati D., Donati M. B., Semeraro N. Cultured human endothelial cells generate tissue factor in response to endotoxin. J Clin Invest 1983; 71(6)1893–1896
  • Bevilacqua M. P., Pober J. S., Majeau G. R., Cotran R. S., Gimbrone M. A., Jr. Interleukin 1 (IL-1) induces biosynthesis and cell surface expression of procoagulant activity in human vascular endothelial cells. J Exp Med 1984; 160(2)618–623
  • Bevilacqua M. P., Pober J. S., Majeau G. R., Fiers W., Cotran R. S., Gimbrone M. A., Jr. Recombinant tumor necrosis factor induces procoagulant activity in cultured human vascular endothelium: characterization and comparison with the actions of interleukin 1. Proc Natl Acad Sci USA 1986; 83(12)4533–4537
  • Tannenbaum S. H., Finko R., Cines D. B. Antibody and immune complexes induce tissue factor production by human endothelial cells. J Immunol 1986; 137(5)1532–1537
  • Szotowski B., Antoniak S., Poller W., Schultheiss H. P., Rauch U. Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res 2005; 96(12)1233–1239
  • Bona R., Lee E., Rickles F. Tissue factor apoprotein: intracellular transport and expression in shed membrane vesicles. Thromb Res 1987; 48(4)487–500
  • Conkling P. R., Greenberg C. S., Weinberg J. B. Tumor necrosis factor induces tissue factor-like activity in human leukemia cell line U937 and peripheral blood monocytes. Blood 1988; 72(1)128–133
  • Drake T. A., Ruf W., Morrissey J. H., Edgington T. S. Functional tissue factor is entirely cell surface expressed on lipopolysaccharide-stimulated human blood monocytes and a constitutively tissue factor-producing neoplastic cell line. J Cell Biol 1989; 109(1)389–395
  • Cermak J., Key N. S., Bach R. R., Balla J., Jacob H. S., Vercellotti G. M. C-reactive protein induces human peripheral blood monocytes to synthesize tissue factor. Blood 1993; 82(2)513–520
  • Schwager I., Jungi T. W. Effect of human recombinant cytokines on the induction of macrophage procoagulant activity. Blood 1994; 83(1)152–160
  • Del Prete G., De Carli M., Lammel R. M., D'Elios M. M., Daniel K. C., Giusti B., Abbate R., Romagnani S. Th1 and Th2 T-helper cells exert opposite regulatory effects on procoagulant activity and tissue factor production by human monocytes. Blood 1995; 86(1)250–257
  • Gouault Heilmann M., Chardon E., Sultan C., Josso F. The procoagulant factor of leukaemic promyelocytes: demonstration of immunologic cross reactivity with human brain tissue factor. Br J Haematol 1975; 30(2)151–158
  • Dvorak H. F., Quay S. C., Orenstein N. S., Dvorak A. M., Hahn P., Bitzer A. M., Carvalho A. C. Tumor shedding and coagulation. Science (New York, N. Y.) 1981; 212(4497)923–924
  • Dvorak H. F., Van DeWater L., Bitzer A. M., Dvorak A. M., Anderson D., Harvey V. S., Bach R., Davis G. L., DeWolf W., Carvalho A. C. Procoagulant activity associated with plasma membrane vesicles shed by cultured tumor cells. Cancer Res 1983; 43(9)4434–4442
  • Wada H., Nagano T., Tomeoku M., Kuto M., Karitani Y., Deguchi K., Shirakawa S. Coagulant and fibrinolytic activities in the leukemic cell lysates. Thromb Res 1983; 30(4)315–322
  • Bastida E., Ordinas A., Escolar G., Jamieson G. A. Tissue factor in microvesicles shed from U87MG human glioblastoma cells induces coagulation, platelet aggregation, and thrombogenesis. Blood 1984; 64(1)177–184
  • Cozzolino F., Torcia M., Miliani A., Carossino A. M., Giordani R., Cinotti S., Filimberti E., Saccardi R., Bernabei P., Guidi G., et al. Potential role of interleukin-1 as the trigger for diffuse intravascular coagulation in acute nonlymphoblastic leukemia. Am J Med 1988; 84(2)240–250
  • Tanaka M. Induction of tissue factor-like activity of human monoblastic leukemia cell line by tumor necrosis factor-alpha. Thromb Res 1989; 56(2)201–211
  • Mueller B. M., Reisfeld R. A., Edgington T. S., Ruf W. Expression of tissue factor by melanoma cells promotes efficient hematogenous metastasis. Proc Natl Acad Sci USA 1992; 89(24)11832–11836
  • Zucchella M., Pacchiarini L., Meloni F., Ballabio P., Saporiti A., Brocchieri A., Grignani G. Effect of interferon alpha, interferon gamma and tumor necrosis factor on the procoagulant activity of human cancer cells. Haematologica 1993; 78(5)282–286
  • Dolo V., Adobati E., Canevari S., Picone M. A., Vittorelli M. L. Membrane vesicles shed into the extracellular medium by human breast carcinoma cells carry tumor-associated surface antigens. Clin Exp Metastasis 1995; 13(4)277–286
  • Kim C. W., Lee H. M., Lee T. H., Kang C., Kleinman H. K., Gho Y. S. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res 2002; 62(21)6312–6317
  • Yu J. L., Rak J. W. Shedding of tissue factor (TF)-containing microparticles rather than alternatively spliced TF is the main source of TF activity released from human cancer cells. J Thromb Haemost 2004; 2(11)2065–2067
  • Rong Y., Post D. E., Pieper R. O., Durden D. L., Van Meir E. G., Brat D. J. PTEN and hypoxia regulate tissue factor expression and plasma coagulation by glioblastoma. Cancer Res 2005; 65(4)1406–1413
  • Kakkar A. K., DeRuvo N., Chinswangwatanakul V., Tebbutt S., Williamson R. C. Extrinsic-pathway activation in cancer with high factor VIIa and tissue factor. Lancet 1995; 346(8981)1004–1005
  • Tesselaar M. E., Romijn F. P., Van Der Linden I. K., Prins F. A., Bertina R. M., Osanto S. Microparticle-associated tissue factor activity: a link between cancer and thrombosis?. J Thromb Haemost 2007; 5(3)520–527
  • Langer F., Chun F. K., Amirkhosravi A., Friedrich M., Leuenroth S., Eifrig B., Bokemeyer C., Francis J. L. Plasma tissue factor antigen in localized prostate cancer: distribution, clinical significance and correlation with haemostatic activation markers. Thromb Haemost 2007; 97(3)464–470
  • Camera M., Frigerio M., Toschi V., Brambilla M., Rossi F., Cottell D. C., Maderna P., Parolari A., Bonzi R., De Vincenti O., Tremoli E. 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
  • Key N. S., Slungaard A., Dandelet L., Nelson S. C., Moertel C., Styles L. A., Kuypers F. A., Bach R. R. Whole blood tissue factor procoagulant activity is elevated in patients with sickle cell disease. Blood 1998; 91(11)4216–4223
  • Giesen P. L., Rauch U., Bohrmann B., Kling D., Roque M., Fallon J. T., Badimon J. J., Himber J., Riederer M. A., Nemerson Y. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci USA 1999; 96(5)2311–2315
  • Falati S., Gross P., Merrill-Skoloff G., Furie B. C., Furie B. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med 2002; 8(10)1175–1181
  • Celi A., Merrill-Skoloff G., Gross P., Falati S., Sim D. S., Flaumenhaft R., Furie B. C., Furie B. Thrombus formation: direct real-time observation and digital analysis of thrombus assembly in a living mouse by confocal and widefield intravital microscopy. J Thromb Haemost 2003; 1(1)60–68
  • Falati S., Liu Q., Gross P., Merrill-Skoloff G., Chou J., Vandendries E., Celi A., Croce K., Furie B. C., Furie B. 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(11)1585–1598
  • 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(10)3190–3197
  • Day S. M., Reeve J. L., Pedersen B., Farris D. M., Myers D. D., Im M., Wakefield T. W., Mackman N., Fay W. P. Macrovascular thrombosis is driven by tissue factor derived primarily from the blood vessel wall. Blood 2005; 105(1)192–198
  • Uno K., Homma S., Satoh T., Nakanishi K., Abe D., Matsumoto K., Oki A., Tsunoda H., Yamaguchi I., Nagasawa T., Yoshikawa H., Aonuma K. Tissue factor expression as a possible determinant of thromboembolism in ovarian cancer. Br J Cancer 2007; 96(2)290–295
  • Kamikura Y., Wada H., Nobori T., Kobayashi T., Sase T., Nishikawa M., Ishikura K., Yamada N., Abe Y., Nishioka J., Nakano T., Shiku H. Elevated levels of leukocyte tissue factor mRNA in patients with venous thromboembolism. Thromb Res 2005; 116(4)307–312
  • Goldenberg N., Kahn S. R., Solymoss S. Markers of coagulation and angiogenesis in cancer-associated venous thromboembolism. J Clin Oncol 2003; 21(22)4194–4199
  • Zioncheck T. F., Roy S., Vehar G. A. The cytoplasmic domain of tissue factor is phosphorylated by a protein kinase C-dependent mechanism. J Biol Chem 1992; 267(6)3561–3564
  • Ahamed J., Belting M., Ruf W. Regulation of tissue factor-induced signaling by endogenous and recombinant tissue factor pathway inhibitor 1. Blood 2005; 105(6)2384–2391
  • Ahamed J., Ruf W. Protease-activated receptor 2-dependent phosphorylation of the tissue factor cytoplasmic domain. J Biol Chem 2004; 279(22)23038–23044
  • Muller M., Albrecht S., Golfert F., Hofer A., Funk R. H., Magdolen V., Flossel C., Luther T. Localization of tissue factor in actin-filament-rich membrane areas of epithelial cells. Exp Cell Res 1999; 248(1)136–147
  • Ott I., Fischer E. G., Miyagi Y., Mueller B. M., Ruf W. A role for tissue factor in cell adhesion and migration mediated by interaction with actin-binding protein 280. J Cell Biol 1998; 140(5)1241–1253
  • Dorfleutner A., Hintermann E., Tarui T., Takada Y., Ruf W. Cross-talk of integrin alpha3beta1 and tissue factor in cell migration. Mol Biol Cell 2004; 15(10)4416–4425
  • Ott I., Weigand B., Michl R., Seitz I., Sabbari-Erfani N., Neumann F. J., Schomig A. Tissue factor cytoplasmic domain stimulates migration by activation of the GTPase Rac1 and the mitogen-activated protein kinase p38. Circulation 2005; 111(3)349–355
  • Abe K., Shoji M., Chen J., Bierhaus A., Danave I., Micko C., Casper K., Dillehay D. L., Nawroth P. P., Rickles F. R. Regulation of vascular endothelial growth factor production and angiogenesis by the cytoplasmic tail of tissue factor. Proc Natl Acad Sci USA 1999; 96(15)8663–8668
  • Bromberg M. E., Bailly M. A., Konigsberg W. H. Role of protease-activated receptor 1 in tumor metastasis promoted by tissue factor. Thromb Haemost 2001; 86(5)1210–1214
  • Bromberg M. E., Konigsberg W. H., Madison J. F., Pawashe A., Garen A. Tissue factor promotes melanoma metastasis by a pathway independent of blood coagulation. Proc Natl Acad Sci USA 1995; 92(18)8205–8209
  • Bromberg M. E., Sundaram R., Homer R. J., Garen A., Konigsberg W. H. Role of tissue factor in metastasis: functions of the cytoplasmic and extracellular domains of the molecule. Thromb Haemost 1999; 82(1)88–92
  • Hembrough T. A., Swartz G. M., Papathanassiu A., Vlasuk G. P., Rote W. E., Green S. J., Pribluda V. S. Tissue factor/factor VIIa inhibitors block angiogenesis and tumor growth through a nonhemostatic mechanism. Cancer Res 2003; 63(11)2997–3000
  • Mueller B. M., Ruf W. Requirement for binding of catalytically active factor VIIa in tissue factor-dependent experimental metastasis. J Clin Invest 1998; 101(7)1372–1378
  • Ngo C. V., Picha K., McCabe F., Millar H., Tawadros R., Tam S. H., Nakada M. T., Anderson G. M. CNTO 859, a humanized anti-tissue factor monoclonal antibody, is a potent inhibitor of breast cancer metastasis and tumor growth in xenograft models. Int J Cancer 2007; 120(6)1261–1267
  • Amarzguioui M., Peng Q., Wiiger M. T., Vasovic V., Babaie E., Holen T., Nesland J. M., Prydz H. Ex vivo and in vivo delivery of anti-tissue factor short interfering RNA inhibits mouse pulmonary metastasis of B16 melanoma cells. Clin Cancer Res 2006; 12(13)4055–4061
  • Zhang Y., Deng Y., Luther T., Muller M., Ziegler R., Waldherr R., Stern D. M., Nawroth P. P. Tissue factor controls the balance of angiogenic and antiangiogenic properties of tumor cells in mice. J Clin Invest 1994; 94(3)1320–1327
  • Belting M., Dorrell M. I., Sandgren S., Aguilar E., Ahamed J., Dorfleutner A., Carmeliet P., Mueller B. M., Friedlander M., Ruf W. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat Med 2004; 10(5)502–509
  • Versteeg H. H., Schaffner F., Kerver M., Petersen H. H., Ahamed J., Felding-Habermann B., Takada Y., Mueller B. M., Ruf W. Inhibition of tissue factor signaling suppresses tumor growth. Blood 2008; 111(1)190–199
  • Palumbo J. S., Talmage K. E., Massari J. V., La Jeunesse C. M., Flick M. J., Kombrinck K. W., Hu Z., Barney K. A., Degen J. L. Tumor cell-associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell-dependent and-independent mechanisms. Blood 2007; 110(1)133–141
  • Toomey J. R., Kratzer K. E., Lasky N. M., Broze G. J., Jr. Effect of tissue factor deficiency on mouse and tumor development. Proc Natl Acad Sci USA 1997; 94(13)6922–6926
  • Parry G. C., Erlich J. H., Carmeliet P., Luther T., Mackman N. Low levels of tissue factor are compatible with development and hemostasis in mice. J Clin Invest 1998; 101(3)560–569
  • Milsom C., Yu J., May L., Meehan B., Magnus N., Al-Nedawi K., Luyendyk J., Weitz J., Klement P., Broze G., Mackman N., Rak J. The role of tumor-and host-related tissue factor pools in oncogene-driven tumor progression. Thromb Res 2007; 120(Suppl. 2)S82–S91
  • Sorensen B. B., Freskgard P. O., Nielsen L. S., Rao L. V., Ezban M., Petersen L. C. Factor VIIa-induced p44/42 mitogen-activated protein kinase activation requires the proteolytic activity of factor VIIa and is independent of the tissue factor cytoplasmic domain. J Biol Chem 1999; 274(30)21349–21354
  • Camerer E., Rottingen J. A., Gjernes E., Larsen K., Skartlien A. H., Iversen J. G., Prydz H. Coagulation factors VIIa and Xa induce cell signaling leading to up-regulation of the egr-1 gene. J Biol Chem 1999; 274(45)32225–32233
  • Petersen L. C., Freskgard P., Ezban M. Tissue factor-dependent factor VIIa signaling. Trends Cardiovasc Med 2000; 10(2)47–52
  • Bono F., Schaeffer P., Herault J. P., Michaux C., Nestor A. L., Guillemot J. C., Herbert J. M. Factor Xa activates endothelial cells by a receptor cascade between EPR-1 and PAR-2. Arterioscler Thromb Vasc Biol 2000; 20(11)E107–E112
  • Camerer E., Huang W., Coughlin S. R. Tissue factor- and factor X-dependent activation of protease-activated receptor 2 by factor VIIa. Proc Natl Acad Sci USA 2000; 97(10)5255–5260
  • Hjortoe G. M., Petersen L. C., Albrektsen T., Sorensen B. B., Norby P. L., Mandal S. K., Pendurthi U. R., Rao L. V. Tissue factor-factor VIIa-specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated by PAR-2 and results in increased cell migration. Blood 2004; 103(8)3029–3037
  • Petersen L. C., Thastrup O., Hagel G., Sorensen B. B., Freskgard P. O., Rao L. V., Ezban M. Exclusion of known protease-activated receptors in factor VIIa-induced signal transduction. Thromb Haemost 2000; 83(4)571–576
  • Siegbahn A., Johnell M., Rorsman C., Ezban M., Heldin C. H., Ronnstrand L. Binding of factor VIIa to tissue factor on human fibroblasts leads to activation of phospholipase C and enhanced PDGF-BB-stimulated chemotaxis. Blood 2000; 96(10)3452–3458
  • Cunningham M. A., Romas P., Hutchinson P., Holdsworth S. R., Tipping P. G. Tissue factor and factor VIIa receptor/ligand interactions induce proinflammatory effects in macrophages. Blood 1999; 94(10)3413–3420
  • Poulsen L. K., Jacobsen N., Sorensen B. B., Bergenhem N. C., Kelly J. D., Foster D. C., Thastrup O., Ezban M., Petersen L. C. Signal transduction via the mitogen-activated protein kinase pathway induced by binding of coagulation factor VIIa to tissue factor. J Biol Chem 1998; 273(11)6228–6232
  • Versteeg H. H., Hoedemaeker I., Diks S. H., Stam J. C., Spaargaren M., van Bergen En Henegouwen P. M., van Deventer S. J., Peppelenbosch M. P. Factor VIIa/tissue factor-induced signaling via activation of Src-like kinases, phosphatidylinositol 3-kinase, and Rac. J Biol Chem 2000; 275(37)28750–28756
  • Versteeg H. H., Spek C. A., Slofstra S. H., Diks S. H., Richel D. J., Peppelenbosch M. P. FVIIa:TF induces cell survival via G12/G13-dependent Jak/STAT activation and BclXL production. Circ Res 2004; 94(8)1032–1040
  • Riewald M., Kravchenko V. V., Petrovan R. J., O'Brien P. J., Brass L. F., Ulevitch R. J., Ruf W. Gene induction by coagulation factor Xa is mediated by activation of protease-activated receptor 1. Blood 2001; 97(10)3109–3116
  • Riewald M., Ruf W. Mechanistic coupling of protease signaling and initiation of coagulation by tissue factor. Proc Natl Acad Sci USA 2001; 98(14)7742–7747
  • Jiang X., Bailly M. A., Panetti T. S., Cappello M., Konigsberg W. H., Bromberg M. E. Formation of tissue factor-factor VIIa-factor Xa complex promotes cellular signaling and migration of human breast cancer cells. J Thromb Haemost 2004; 2(1)93–101
  • Albrektsen T., Sorensen B. B., Hjorto G. M., Fleckner J., Rao L. V., Petersen L. C. Transcriptional program induced by factor VIIa-tissue factor, PAR1 and PAR2 in MDA-MB-231 cells. J Thromb Haemost 2007; 5(8)1588–1597
  • Bretschneider E., Braun M., Fischer A., Wittpoth M., Glusa E., Schror K. Factor Xa acts as a PDGF-independent mitogen in human vascular smooth muscle cells. Thromb Haemost 2000; 84(3)499–505
  • Gasic G. P., Arenas C. P., Gasic T. B., Gasic G. J. Coagulation factors X, Xa, and protein S as potent mitogens of cultured aortic smooth muscle cells. Proc Natl Acad Sci USA 1992; 89(6)2317–2320
  • Herbert J., Bono F., Herault J., Avril C., Dol F., Mares A., Schaeffer P. Effector protease receptor 1 mediates the mitogenic activity of factor Xa for vascular smooth muscle cells in vitro and in vivo. J Clin Invest 1998; 101(5)993–1000
  • McLean K., Schirm S., Johns A., Morser J., Light D. R. FXa-induced responses in vascular wall cells are PAR-mediated and inhibited by ZK-807834. Thromb Res 2001; 103(4)281–297
  • Ko F. N., Yang Y. C., Huang S. C., Ou J. T. Coagulation factor Xa stimulates platelet-derived growth factor release and mitogenesis in cultured vascular smooth muscle cells of rat. J Clin Invest 1996; 98(6)1493–1501
  • Altieri D. C. Xa receptor EPR-1. Faseb J 1995; 9(10)860–865
  • Bhattacharjee G., Ahamed J., Pawlinski R., Liu C., Mackman N., Ruf W., Edgington T. S. Factor Xa binding to annexin 2 mediates signal transduction via protease-activated receptor 1. Circ Res 2008; 102(4)457–464
  • Macfarlane S. R., Seatter M. J., Kanke T., Hunter G. D., Plevin R. Proteinase-activated receptors. Pharmacol Rev 2001; 53(2)245–282
  • Patterson C., Stouffer G. A., Madamanchi N., Runge M. S. New tricks for old dogs: nonthrombotic effects of thrombin in vessel wall biology. Circ Res 2001; 88(10)987–997
  • Ishihara H., Connolly A. J., Zeng D., Kahn M. L., Zheng Y. W., Timmons C., Tram T., Coughlin S. R. Protease-activated receptor 3 is a second thrombin receptor in humans. Nature 1997; 386(6624)502–506
  • Nakanishi-Matsui M., Zheng Y. W., Sulciner D. J., Weiss E. J., Ludeman M. J., Coughlin S. R. PAR3 is a cofactor for PAR4 activation by thrombin. Nature 2000; 404(6778)609–613
  • O'Brien P. J., Prevost N., Molino M., Hollinger M. K., Woolkalis M. J., Woulfe D. S., Brass L. F. Thrombin responses in human endothelial cells. Contributions from receptors other than PAR1 include the transactivation of PAR2 by thrombin-cleaved PAR1. J Biol Chem 2000; 275(18)13502–13509
  • Griffin C. T., Srinivasan Y., Zheng Y. W., Huang W., Coughlin S. R. A role for thrombin receptor signaling in endothelial cells during embryonic development. Science (New York, N. Y.) 2001; 293(5535)1666–1670
  • Haralabopoulos G. C., Grant D. S., Kleinman H. K., Maragoudakis M. E. Thrombin promotes endothelial cell alignment in Matrigel in vitro and angiogenesis in vivo. Am J Physiol 1997; 273: C239–C245, (1 Pt 1)
  • Maragoudakis M. E., Kraniti N., Giannopoulou E., Alexopoulos K., Matsoukas J. Modulation of angiogenesis and progelatinase a by thrombin receptor mimetics and antagonists. Endothelium 2001; 8(3)195–205
  • Daniel T. O., Gibbs V. C., Milfay D. F., Garovoy M. R., Williams L. T. Thrombin stimulates c-sis gene expression in microvascular endothelial cells. J Biol Chem 1986; 261(21)9579–9582
  • Papadimitriou E., Manolopoulos V. G., Hayman G. T., Maragoudakis M. E., Unsworth B. R., Fenton J. W., 2nd, Lelkes P. I. Thrombin modulates vectorial secretion of extracellular matrix proteins in cultured endothelial cells. Am J Physiol 1997; 272: C1112–1122, (4 Pt 1)
  • Even-Ram S., Uziely B., Cohen P., Grisaru-Granovsky S., Maoz M., Ginzburg Y., Reich R., Vlodavsky I., Bar-Shavit R. Thrombin receptor overexpression in malignant and physiological invasion processes. Nat Med 1998; 4(8)909–914
  • Tsopanoglou N. E., Maragoudakis M. E. On the mechanism of thrombin-induced angiogenesis. Potentiation of vascular endothelial growth factor activity on endothelial cells by up-regulation of its receptors. J Biol Chem 1999; 274(34)23969–23976
  • Wojtukiewicz M. Z., Tang D. G., Ciarelli J. J., Nelson K. K., Walz D. A., Diglio C. A., Mammen E. F., Honn K. V. Thrombin increases the metastatic potential of tumor cells. Int J Cancer 1993; 54(5)793–806
  • Wojtukiewicz M. Z., Tang D. G., Nelson K. K., Walz D. A., Diglio C. A., Honn K. V. Thrombin enhances tumor cell adhesive and metastatic properties via increased alpha IIb beta 3 expression on the cell surface. Thromb Res 1992; 68(3)233–245
  • Hattori R., Hamilton K. K., Fugate R. D., McEver R. P., Sims P. J. Stimulated secretion of endothelial von Willebrand factor is accompanied by rapid redistribution to the cell surface of the intracellular granule membrane protein GMP-140. J Biol Chem 1989; 264(14)7768–7771
  • Stenberg P. E., McEver R. P., Shuman M. A., Jacques Y. V., Bainton D. F. A platelet alpha-granule membrane protein (GMP-140) is expressed on the plasma membrane after activation. J Cell Biol 1985; 101(3)880–886
  • Henn V., Slupsky J. R., Grafe M., Anagnostopoulos I., Forster R., Muller-Berghaus G., Kroczek R. A. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 1998; 391(6667)591–594
  • Yin Y. J., Salah Z., Grisaru-Granovsky S., Cohen I., Even-Ram S. C., Maoz M., Uziely B., Peretz T., Bar-Shavit R. Human protease-activated receptor 1 expression in malignant epithelia: a role in invasiveness. Arterioscler Thromb Vasc Biol 2003; 23(6)940–944
  • Maloney J. P., Silliman C. C., Ambruso D. R., Wang J., Tuder R. M., Voelkel N. F. In vitro release of vascular endothelial growth factor during platelet aggregation. Am J Physiol 1998; 275: H1054–H1061, (3 Pt 2)
  • Mohle R., Green D., Moore M. A., Nachman R. L., Rafii S. Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci USA 1997; 94(2)663–668
  • Nierodzik M. L., Chen K., Takeshita K., Li J. J., Huang Y. Q., Feng X. S., D'Andrea M. R., Andrade-Gordon P., Karpatkin S. Protease-activated receptor 1 (PAR-1) is required and rate-limiting for thrombin-enhanced experimental pulmonary metastasis. Blood 1998; 92(10)3694–3700
  • Camerer E., Qazi A. A., Duong D. N., Cornelissen I., Advincula R., Coughlin S. R. Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood 2004; 104(2)397–401
  • Nierodzik M. L., Plotkin A., Kajumo F., Karpatkin S. Thrombin stimulates tumor-platelet adhesion in vitro and metastasis in vivo. J Clin Invest 1991; 87(1)229–236
  • Fischer E. G., Riewald M., Huang H. Y., Miyagi Y., Kubota Y., Mueller B. M., Ruf W. Tumor cell adhesion and migration supported by interaction of a receptor-protease complex with its inhibitor. J Clin Invest 1999; 104(9)1213–1221
  • Karpatkin S. Does hypercoagulability awaken dormant tumor cells in the host?. J Thromb Haemost 2004; 2(12)2103–2106
  • Rickles F. R., Patierno S., Fernandez P. M. Tissue factor, thrombin, and cancer. Chest 2003; 124(Suppl. 3)58S–68S
  • Lalla R. V., Goralnick S. J., Tanzer M. L., Kreutzer D. L. Fibrin induces IL-8 expression from human oral squamous cell carcinoma cells. Oral Oncol 2001; 37(3)234–242
  • Medved L., Tsurupa G., Yakovlev S. Conformational changes upon conversion of fibrinogen into fibrin. The mechanisms of exposure of cryptic sites. Ann N Y Acad Sci 2001; 936: 185–204
  • Degen J. L., Drew A. F., Palumbo J. S., Kombrinck K. W., Bezerra J. A., Danton M. J., Holmback K., Suh T. T. Genetic manipulation of fibrinogen and fibrinolysis in mice. Ann N Y Acad Sci 2001; 936: 276–290
  • van Hinsbergh V. W., Collen A., Koolwijk P. Role of fibrin matrix in angiogenesis. Ann N Y Acad Sci 2001; 936: 426–437
  • Palumbo J. S., Kombrinck K. W., Drew A. F., Grimes T. S., Kiser J. H., Degen J. L., Bugge T. H. Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood 2000; 96(10)3302–3309
  • Palumbo J. S., Potter J. M., Kaplan L. S., Talmage K., Jackson D. G., Degen J. L. Spontaneous hematogenous and lymphatic metastasis, but not primary tumor growth or angiogenesis, is diminished in fibrinogen-deficient mice. Cancer Res 2002; 62(23)6966–6972
  • Hu L., Lee M., Campbell W., Perez-Soler R., Karpatkin S. Role of endogenous thrombin in tumor implantation, seeding, and spontaneous metastasis. Blood 2004; 104(9)2746–2751
  • Bardos H., Molnar P., Csecsei G., Adany R. Fibrin deposition in primary and metastatic human brain tumours. Blood Coagul Fibrinolysis 1996; 7(5)536–548
  • Wojtukiewicz M. Z., Zacharski L. R., Memoli V. A., Kisiel W., Kudryk B. J., Moritz T. E., Rousseau S. M., Stump D. C. Fibrin formation on vessel walls in hyperplastic and malignant prostate tissue. Cancer 1991; 67(5)1377–1383
  • Bootle-Wilbraham C. A., Tazzyman S., Marshall J. M., Lewis C. E. Fibrinogen E-fragment inhibits the migration and tubule formation of human dermal microvascular endothelial cells in vitro. Cancer Res 2000; 60(17)4719–4724
  • Thompson W. D., Smith E. B., Stirk C. M., Marshall F. I., Stout A. J., Kocchar A. Angiogenic activity of fibrin degradation products is located in fibrin fragment E. J Pathol 1992; 168(1)47–53
  • Rickles F. R., Falanga A. Molecular basis for the relationship between thrombosis and cancer. Thromb Res 2001; 102(6)V215–V224

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.