Effects of tumor-expressed coagulation factors on cancer progression and venous thrombosis: Is there a key factor?

Thrombosis Research

Volumn 133, Issue SUPPL. 2, 2014, Pages

  Ünlü, Betül ^a   Versteeg, Henri H ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

asTF; Cancer; Ectopic FVII; Thrombosis; Tissue factor

Indexed keywords

ANTINEOPLASTIC AGENT; BETA1 INTEGRIN; BIOLOGICAL MARKER; BLOOD CLOTTING FACTOR; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 7A; D DIMER; PROTEIN Z PROTEASE INHIBITOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE INHIBITOR; RECOMBINANT THROMBOPLASTIN; THROMBIN; THROMBOPLASTIN; TISSUE FACTOR PATHWAY INHIBITOR; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANGIOGENESIS; ARTICLE; BLOOD CLOTTING; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER PATIENT; CANCER PROGNOSIS; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; COLORECTAL CANCER; DISEASE ASSOCIATION; EXTRACELLULAR MATRIX; GLIOBLASTOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HISTOPATHOLOGY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LUNG CANCER; LUNG NON SMALL CELL CANCER; MEMBRANE MICROPARTICLE; METASTASIS; NEOPLASM; NONHUMAN; OVARY CANCER; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; VENOUS THROMBOEMBOLISM; BLOOD; COMPLICATION; DISEASE COURSE; METABOLISM;

BLOOD COAGULATION FACTORS; DISEASE PROGRESSION; HUMANS; NEOPLASMS; VENOUS THROMBOEMBOLISM;

EID: 84901460303     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/S0049-3848(14)50013-8     Document Type: Article

References (123)

1. Y.W. Van den Berg, S. Osanto, P.H. Reitsma, and H.H. Versteeg The relationship between tissue factor and cancer progression: insights from bench and bedside Blood 119 2012 924 932
2. A.A. Khorana, C.W. Francis, E. Culakova, N.M. Kuderer, and G.H. Lyman Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy J Thromb Haemost 5 2007 632 634 (Pubitemid 46680709)
3. M. Mandala, S. Barni, M. Prins, R. Labianca, C. Tondini, and L. Russo et al. Acquired and inherited risk factors for developing venous thromboembolism in cancer patients receiving adjuvant chemotherapy: A prospective trial Ann Oncol 21 2010 871 876
4. C. Ay, D. Dunkler, R. Simanek, J. Thaler, S. Koder, and C. Marosi et al. Prediction of venous thromboembolism in patients with cancer by measuring thrombin generation: results from the Vienna Cancer and Thrombosis Study J Clin Oncol 29 2011 2099 2103
5. J.S. Palumbo, K.E. Talmage, J.V. Massari, C.M. La Jeunesse, M.J. Flick, and K.W. Kombrinck et al. Tumor cell-associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell-dependent and-independent mechanisms Blood 110 2007 133 141 (Pubitemid 47026828)
6. H.T. Sorensen, L. Mellemkjaer, J.H. Olsen, and J.A. Baron Prognosis of cancers associated with venous thromboembolism N Engl J Med 343 2000 1846 1850 (Pubitemid 32104130)
7. N. Levitan, A. Dowlati, S.C. Remick, H.I. Tahsildar, L.D. Sivinski, and R. Beyth et al. Rates of initial and recurrent thromboembolic disease among patients with malignancy versus those without malignancy. Risk analysis using Medicare claims data Medicine (Baltimore) 78 1999 285 291 (Pubitemid 29439263)
8. J.L. Degen, and J.S. Palumbo Hemostatic factors, innate immunity and malignancy Thromb Res 129 Suppl 1 2012 S1 S5
9. S. Sallah, J.Y. Wan, N.P. Nguyen, L.R. Hanrahan, and G. Sigounas Disseminated intravascular coagulation in solid tumors: clinical and pathologic study Thromb Haemost 86 2001 828 833 (Pubitemid 32834193)
10. H.H. Versteeg, M.P. Peppelenbosch, and C.A. Spek The pleiotropic effects of tissue factor: A possible role for factor VIIa-induced intracellular signalling? Thromb Haemost 86 2001 1353 1359 (Pubitemid 34007503)
11. T.C. Carneiro-Lobo, F. Schaffner, J. Disse, H. Ostergaard, I.M. Francischetti, and R.Q. Monteiro et al. The tick-derived inhibitor Ixolaris prevents tissue factor signaling on tumor cells J Thromb Haemost 10 2012 1849 1858
12. D.M. Monroe, and N.S. Key The tissue factor-factor VIIa complex: procoagulant activity, regulation, and multitasking J Thromb Haemost 5 2007 1097 1105 (Pubitemid 46902106)
13. R.W. Colman Are hemostasis and thrombosis two sides of the same coin? J Exp Med 203 2006 493 495
14. B. Kocaturk, and H.H. Versteeg Tissue factor isoforms in cancer and coagulation: may the best isoform win Thromb Res 129 Suppl 1 2012 S69 S75
15. K. Date, J. Hall, J. Greenman, A. Maraveyas, and L.A. Madden Tumour and microparticle tissue factor expression and cancer thrombosis Thromb Res 131 2013 109 115
16. B. Kocaturk, and H.H. Versteeg Tissue factor-integrin interactions in cancer and thrombosis: every Jack has his Jill J Thromb Haemost 11 Suppl 1 2013 285 293
17. D. Garnier, N. Magnus, E. D'Asti, M. Hashemi, B. Meehan, and C. Milsom et al. Genetic pathways linking hemostasis and cancer Thromb Res 129 Suppl 1 2012 S22 S29
18. A.K. Kakkar, N.R. Lemoine, M.F. Scully, S. Tebbutt, and R.C. Williamson Tissue factor expression correlates with histological grade in human pancreatic cancer Br J Surg 82 1995 1101 1104
19. T. Ueno, M. Toi, M. Koike, S. Nakamura, and T. Tominaga Tissue factor expression in breast cancer tissues: its correlation with prognosis and plasma concentration Br J Cancer 83 2000 164 170 (Pubitemid 30411712)
20. A.A. Khorana, S.A. Ahrendt, C.K. Ryan, C.W. Francis, R.H. Hruban, and Y.C. Hu et al. Tissue factor expression, angiogenesis, and thrombosis in pancreatic cancer Clin Cancer Res 13 2007 2870 2875 (Pubitemid 46849560)
21. M. Riewald, and W. Ruf Mechanistic coupling of protease signaling and initiation of coagulation by tissue factor Proc Natl Acad Sci U S A 98 2001 7742 7747 (Pubitemid 32642631)
22. L.G. Lima, and R.Q. Monteiro Activation of blood coagulation in cancer: implications for tumor progression Biosci Rep 33 2013 e00064
23. E. Camerer, W. Huang, and S.R. Coughlin Tissue factor- and factor X-dependent activation of protease-activated receptor 2 by factor VIIa Proc Natl Acad Sci U S A 97 2000 5255 5260 (Pubitemid 30313705)
24. G.M. Hjortoe, L.C. Petersen, T. Albrektsen, B.B. Sorensen, P.L. Norby, and S.K. Mandal et al. 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 103 2004 3029 3037 (Pubitemid 38451676)
25. A. Li, M.L. Varney, J. Valasek, M. Godfrey, B.J. Dave, and R.K. Singh Autocrine role of interleukin-8 in induction of endothelial cell proliferation, survival, migration and MMP-2 production and angiogenesis Angiogenesis 8 2005 63 71 (Pubitemid 41223840)
26. J.Q. Tang, Q. Fan, W.H. Wu, Z.C. Jia, H. Li, and Y.M. Yang et al. Extrahepatic synthesis of coagulation factor VII by colorectal cancer cells promotes tumor invasion and metastasis Chin Med J (Engl) 123 2010 3559 3565
27. W. Ruf, J. Disse, T.C. Carneiro-Lobo, N. Yokota, and F. Schaffner Tissue factor and cell signalling in cancer progression and thrombosis J Thromb Haemost 9 Suppl 1 2011 306 315
28. F. Schaffner, H.H. Versteeg, A. Schillert, N. Yokota, L.C. Petersen, and B.M. Mueller et al. Cooperation of tissue factor cytoplasmic domain and PAR2 signaling in breast cancer development Blood 116 2010 6106 6113
29. M. Belting, M.I. Dorrell, S. Sandgren, E. Aguilar, J. Ahamed, and A. Dorfleutner et al. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling Nat Med 10 2004 502 509 (Pubitemid 38667909)
30. H.H. Versteeg, F. Schaffner, M. Kerver, L.G. Ellies, P. Andrade-Gordon, and B.M. Mueller et al. Protease-activated receptor (PAR) 2, but not PAR1, signaling promotes the development of mammary adenocarcinoma in polyoma middle T mice Cancer Res 68 2008 7219 7227
31. H.H. Versteeg, F. Schaffner, M. Kerver, H.H. Petersen, J. Ahamed, and B. Felding-Habermann et al. Inhibition of tissue factor signaling suppresses tumor growth Blood 111 2008 190 199
32. B.M. Mueller, and W. Ruf Requirement for binding of catalytically active factor VIIa in tissue factor-dependent experimental metastasis J Clin Invest 101 1998 1372 1378 (Pubitemid 28166834)
33. A. Dorfleutner, E. Hintermann, T. Tarui, Y. Takada, and W. Ruf Cross-talk of integrin alpha3beta1 and tissue factor in cell migration Mol Biol Cell 15 2004 4416 4425 (Pubitemid 39299092)
34. J. Thaler, C. Ay, and I. Pabinger Clinical significance of circulating microparticles for venous thromboembolism in cancer patients Hamostaseologie 32 2012 127 131
35. J.L. Yu, and J.W. Rak 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 2 2004 2065 2067 (Pubitemid 40192770)
36. J.I. Zwicker, B.C. Furie, and B. Furie Cancer-associated thrombosis Crit Rev Oncol Hematol 62 2007 126 136 (Pubitemid 46575277)
37. K.E. Eilertsen, and B. Osterud Tissue factor: (patho)physiology and cellular biology Blood Coagul Fibrinolysis 15 2004 521 538 (Pubitemid 39372467)
38. J.I. Zwicker, H.A. Liebman, D. Neuberg, R. Lacroix, K.A. Bauer, and B.C. Furie et al. Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy Clin Cancer Res 15 2009 6830 6840
39. A. Janowska-Wieczorek, M. Wysoczynski, J. Kijowski, L. Marquez-Curtis, B. Machalinski, and J. Ratajczak et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer Int J Cancer 113 2005 752 760 (Pubitemid 40101256)
40. L.G. Lima, R. Chammas, R.Q. Monteiro, M.E. Moreira, and M.A. Barcinski Tumor-derived microvesicles modulate the establishment of metastatic melanoma in a phosphatidylserine-dependent manner Cancer Lett 283 2009 168 175
41. M.E. Tesselaar, F.P. Romijn, I.K. Van Der Linden, F.A. Prins, R.M. Bertina, and S. Osanto Microparticle-associated tissue factor activity: A link between cancer and thrombosis? J Thromb Haemost 5 2007 520 527 (Pubitemid 46680685)
42. M.E. Tesselaar, F.P. Romijn, I.K. Van Der Linden, R.M. Bertina, and S. Osanto Microparticle-associated tissue factor activity in cancer patients with and without thrombosis J Thromb Haemost 7 2009 1421 1423
43. G.M. Thomas, L. Panicot-Dubois, R. Lacroix, F. Dignat-George, D. Lombardo, and C. Dubois Cancer cell-derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo J Exp Med 206 2009 1913 1927
44. M. Shoji, W.W. Hancock, K. Abe, C. Micko, K.A. Casper, and R.M. Baine et al. 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 152 1998 399 411 (Pubitemid 28106386)
45. T.A. Hembrough, G.M. Swartz, A. Papathanassiu, G.P. Vlasuk, W.E. Rote, and S.J. Green et al. Tissue factor/factor VIIa inhibitors block angiogenesis and tumor growth through a nonhemostatic mechanism Cancer Res 63 2003 2997 3000 (Pubitemid 36667175)
46. H.H. Versteeg, C.A. Spek, D.J. Richel, and M.P. Peppelenbosch Coagulation factors VIIa and Xa inhibit apoptosis and anoikis Oncogene 23 2004 410 417 (Pubitemid 38174995)
47. B.B. Sorensen, L.V. Rao, D. Tornehave, S. Gammeltoft, and L.C. Petersen Antiapoptotic effect of coagulation factor VIIa Blood 102 2003 1708 1715 (Pubitemid 37022564)
48. K. Abe, M. Shoji, J. Chen, A. Bierhaus, I. Danave, and C. Micko et al. Regulation of vascular endothelial growth factor production and angiogenesis by the cytoplasmic tail of tissue factor Proc Natl Acad Sci U S A 96 1999 8663 8668 (Pubitemid 29354848)
49. D. Erdmann, and J. Heim Orphan nuclear receptor HNF-4 binds to the human coagulation factor VII promoter J Biol Chem 270 1995 22988 22996
50. D.S. Fair, and R.A. Marlar Biosynthesis and secretion of factor VII, protein C, protein S, and the Protein C inhibitor from a human hepatoma cell line Blood 67 1986 64 70 (Pubitemid 16167012)
51. B.P. Tsao, D.S. Fair, L.K. Curtiss, and T.S. Edgington Monocytes can be induced by lipopolysaccharide-triggered T lymphocytes to express functional factor VII/VIIa protease activity J Exp Med 159 1984 1042 1057 (Pubitemid 14171618)
52. H.A. Chapman Jr., C.L. Allen, O.L. Stone, and D.S. Fair Human alveolar macrophages synthesize factor VII in vitro. Possible role in interstitial lung disease J Clin Invest 75 1985 2030 2037 (Pubitemid 15233594)
53. J.N. Wilcox, S. Noguchi, and J. Casanova Extrahepatic synthesis of factor VII in human atherosclerotic vessels Arterioscler Thromb Vasc Biol 23 2003 136 141 (Pubitemid 36091638)
54. V. Neaud, T. Hisaka, A. Monvoisin, C. Bedin, C. Balabaud, and D.C. Foster et al. Paradoxical pro-invasive effect of the serine proteinase inhibitor tissue factor pathway inhibitor-2 on human hepatocellular carcinoma cells J Biol Chem 275 2000 35565 35569
55. E.G. Fischer, M. Riewald, H.Y. Huang, Y. Miyagi, Y. Kubota, and B.M. Mueller et al. Tumor cell adhesion and migration supported by interaction of a receptor-protease complex with its inhibitor J Clin Invest 104 1999 1213 1221 (Pubitemid 29536292)
56. L.R. Zacharski, V.A. Memoli, D.L. Ornstein, S.M. Rousseau, W. Kisiel, and B.J. Kudryk Tumor cell procoagulant and urokinase expression in carcinoma of the ovary J Natl Cancer Inst 85 1993 1225 1230 (Pubitemid 23223528)
57. M.Z. Wojtukiewicz, L.R. Zacharski, M. Rucinska, L. Zimnoch, J. Jaromin, and M. Rozanska-Kudelska et al. Expression of tissue factor and tissue factor pathway inhibitor in situ in laryngeal carcinoma Thromb Haemost 82 1999 1659 1662
58. I.M. Francischetti, J.G. Valenzuela, J.F. Andersen, T.N. Mather, and J.M. Ribeiro Ixolaris, a novel recombinant tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick, Ixodes scapularis: identification of factor X and factor Xa as scaffolds for the inhibition of factor VIIa/tissue factor complex Blood 99 2002 3602 3612 (Pubitemid 34534529)
59. W. Ruf, E.A. Seftor, R.J. Petrovan, R.M. Weiss, L.M. Gruman, and N.V. Margaryan et al. Differential role of tissue factor pathway inhibitors 1 and 2 in melanoma vasculogenic mimicry Cancer Res 63 2003 5381 5389 (Pubitemid 37139855)
60. S. Koizume, M.S. Jin, E. Miyagi, F. Hirahara, Y. Nakamura, and J.H. Piao et al. Activation of cancer cell migration and invasion by ectopic synthesis of coagulation factor VII Cancer Res 66 2006 9453 9460 (Pubitemid 44623642)
61. E.S. Pollak, H.L. Hung, W. Godin, G.C. Overton, and K.A. High Functional characterization of the human factor VII 5'-flanking region J Biol Chem 271 1996 1738 1747
62. S. Koizume, N. Yokota, E. Miyagi, F. Hirahara, Y. Nakamura, and Y. Sakuma et al. Hepatocyte nuclear factor-4-independent synthesis of coagulation factor VII in breast cancer cells and its inhibition by targeting selective histone acetyltransferases Mol Cancer Res 7 2009 1928 1936
63. M.J. Barrero, and S. Malik Two functional modes of a nuclear receptor-recruited arginine methyltransferase in transcriptional activation Mol Cell 24 2006 233 243 (Pubitemid 44557129)
64. J.J. Hung, Y.T. Wang, and W.C. Chang Sp1 deacetylation induced by phorbol ester recruits p300 to activate 12(S)-lipoxygenase gene transcription Mol Cell Biol 26 2006 1770 1785
65. G. Sa, and T. Das Anti cancer effects of curcumin: cycle of life and death Cell Div 3 2008 14
66. N. Yokota, S. Koizume, E. Miyagi, F. Hirahara, Y. Nakamura, and K. Kikuchi et al. Self-production of tissue factor-coagulation factor VII complex by ovarian cancer cells Br J Cancer 101 2009 2023 2029
67. X. Jiang, M.A. Bailly, T.S. Panetti, M. Cappello, W.H. Konigsberg, and M.E. Bromberg Formation of tissue factor-factor VIIa-factor Xa complex promotes cellular signaling and migration of human breast cancer cells J Thromb Haemost 2 2004 93 101 (Pubitemid 40185625)
68. M.E. Bromberg, M.A. Bailly, and W.H. Konigsberg Role of protease-activated receptor 1 in tumor metastasis promoted by tissue factor Thromb Haemost 86 2001 1210 1214 (Pubitemid 33064570)
69. N. Magnus, D. Garnier, and J. Rak Oncogenic epidermal growth factor receptor up-regulates multiple elements of the tissue factor signaling pathway in human glioma cells Blood 116 2010 815 818
70. N. Magnus, N. Gerges, N. Jabado, and J. Rak Coagulation-related gene expression profile in glioblastoma is defined by molecular disease subtype J Thromb Haemost 11 2013 1197 1200
71. L.C. Petersen Microarray studies of factor VIIa-activated cancer cells Thromb Res 122 Suppl 1 2008 S11 S13
72. K.S. Kim, S. Sengupta, M. Berk, Y.G. Kwak, P.F. Escobar, and J. Belinson et al. Hypoxia enhances lysophosphatidic acid responsiveness in ovarian cancer cells and lysophosphatidic acid induces ovarian tumor metastasis in vivo Cancer Res 66 2006 7983 7990 (Pubitemid 44299162)
73. C. Amin, N. Mackman, and N.S. Key Microparticles and cancer Pathophysiol Haemost Thromb 36 2008 177 183
74. T. Satoh, A. Oki, K. Uno, M. Sakurai, H. Ochi, and S. Okada et al. High incidence of silent venous thromboembolism before treatment in ovarian cancer Br J Cancer 97 2007 1053 1057 (Pubitemid 47587007)
75. S. Tateo, L. Mereu, S. Salamano, C. Klersy, M. Barone, and A.C. Spyropoulos et al. Ovarian cancer and venous thromboembolic risk Gynecol Oncol 99 2005 119 125 (Pubitemid 41354592)
76. T.C. Carneiro-Lobo, S. Konig, D.E. Machado, L.E. Nasciutti, M.F. Forni, and I.M. Francischetti et al. Ixolaris, a tissue factor inhibitor, blocks primary tumor growth and angiogenesis in a glioblastoma model J Thromb Haemost 7 2009 1855 1864
77. V.Y. Bogdanov, V. Balasubramanian, J. Hathcock, O. Vele, M. Lieb, and Y. Nemerson Alternatively spliced human tissue factor: A circulating, soluble, thrombogenic protein Nat Med 9 2003 458 462 (Pubitemid 36460081)
78. B. Kocaturk, Y.W. Van den Berg, C. Tieken, J.S. Mieog, E.M. de Kruijf, and C.C. Engels et al. Alternatively spliced tissue factor promotes breast cancer growth in a beta1 integrin-dependent manner Proc Natl Acad Sci U S A 110 2013 11517 11522
79. J.E. Hobbs, A. Zakarija, D.L. Cundiff, J.A. Doll, E. Hymen, and M. Cornwell et al. Alternatively spliced human tissue factor promotes tumor growth and angiogenesis in a pancreatic cancer tumor model Thromb Res 120 Suppl 2 2007 S13 S21
80. Y.W. Van den Berg, L.G. Van den Hengel, H.R. Myers, O. Ayachi, E. Jordanova, and W. Ruf et al. Alternatively spliced tissue factor induces angiogenesis through integrin ligation Proc Natl Acad Sci U S A 106 2009 19497 19502
81. F.S. Ribeiro, T.A. Simao, N.D. Amoedo, N.A. Andreollo, L.R. Lopes, and R. Acatauassu et al. Evidence for increased expression of tissue factor and protease-activated receptor-1 in human esophageal cancer Oncol Rep 21 2009 1599 1604
82. P. Goldin-Lang, Q.V. Tran, I. Fichtner, A. Eisenreich, S. Antoniak, and K. Schulze et al. Tissue factor expression pattern in human non-small cell lung cancer tissues indicate increased blood thrombogenicity and tumor metastasis Oncol Rep 20 2008 123 128
83. N. Von Offenberg Sweeney, P.M. Cummins, E.J. Cotter, P.A. Fitzpatrick, Y.A. Birney, and E.M. Redmond et al. Cyclic strain-mediated regulation of vascular endothelial cell migration and tube formation Biochem Biophys Res Commun 329 2005 573 582 (Pubitemid 40311782)
84. E.H. Danen, P. Sonneveld, C. Brakebusch, R. Fassler, and A. Sonnenberg The fibronectin-binding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis J Cell Biol 159 2002 1071 1086 (Pubitemid 36055761)
85. P. Censarek, A. Bobbe, M. Grandoch, K. Schror, and A.A. Weber Alternatively spliced human tissue factor (asHTF) is not pro-coagulant Thromb Haemost 97 2007 11 14 (Pubitemid 46242381)
86. A.N. Boing, C.M. Hau, A. Sturk, and R. Nieuwland Human alternatively spliced tissue factor is not secreted and does not trigger coagulation J Thromb Haemost 7 2009 1423 1426
87. B. Szotowski, S. Antoniak, W. Poller, H.P. Schultheiss, and U. Rauch Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines Circ Res 96 2005 1233 1239 (Pubitemid 40962100)
88. D. Unruh, K. Turner, R. Srinivasan, B. Kocaturk, X. Qi, and Z. Chu et al. Alternatively spliced tissue factor contributes to tumor spread and activation of coagulation in pancreatic ductal adenocarcinoma Int J Cancer 134 2014 9 20
89. C. Furlan-Freguia, P. Marchese, A. Gruber, Z.M. Ruggeri, and W. Ruf P2X7 receptor signaling contributes to tissue factor-dependent thrombosis in mice J Clin Invest 121 2011 2932 2944
90. R. Srinivasan, E. Ozhegov, Y.W. Van den Berg, B.J. Aronow, R.S. Franco, and M.B. Palascak et al. Splice variants of tissue factor promote monocyte-endothelial interactions by triggering the expression of cell adhesion molecules via integrin-mediated signaling J Thromb Haemost 9 2011 2087 2096
91. R.E. Tilley, B. Pedersen, R. Pawlinski, Y. Sato, J.H. Erlich, and Y. Shen et al. Atherosclerosis in mice is not affected by a reduction in tissue factor expression Arterioscler Thromb Vasc Biol 26 2006 555 562
92. E. Sierko, M.Z. Wojtukiewicz, L. Zimnoch, P. Tokajuk, K. Ostrowska-Cichocka, and W. Kisiel Co-localization of Protein Z, Protein Z-Dependent protease inhibitor and coagulation factor X in human colon cancer tissue: implications for coagulation regulation on tumor cells Thromb Res 129 2012 e112 e118
93. E. Sierko, M.Z. Wojtukiewicz, L. Zimnoch, P. Tokajuk, K. Ostrowska-Cichocka, and W. Kisiel Protein Z/protein Z-dependent protease inhibitor system in loco in human gastric cancer Ann Hematol 2013
94. E. Sierko, M.Z. Wojtukiewicz, L. Zimnoch, K. Ostrowska-Cichocka, P. Tokajuk, and R. Ramlau et al. Protein Z/protein Z-dependent protease inhibitor system in human non-small-cell lung cancer tissue Thromb Res 129 2012 e92 e96
95. E. Sierko, M.Z. Wojtukiewicz, L. Zimnoch, P. Tokajuk, and W. Kisiel Protein Z is present in human breast cancer tissue Int J Hematol 93 2011 681 683
96. L.R. Zacharski, C. Dunwiddie, E.M. Nutt, J. Hunt, and V.A. Memoli Cellular localization of activated factor X by Xa-specific probes Thromb Haemost 65 1991 545 548
97. D. Darmoul, V. Gratio, H. Devaud, T. Lehy, and M. Laburthe Aberrant expression and activation of the thrombin receptor protease-activated receptor-1 induces cell proliferation and motility in human colon cancer cells Am J Pathol 162 2003 1503 1513 (Pubitemid 36512832)
98. X. Han, R. Fiehler, and G.J. Broze Jr. Isolation of a protein Z-dependent plasma protease inhibitor Proc Natl Acad Sci U S A 95 1998 9250 9255 (Pubitemid 28506217)
99. G.W. Tormoen, A. Khader, A. Gruber, and O.J. McCarty Physiological levels of blood coagulation factors IX and X control coagulation kinetics in an in vitro model of circulating tissue factor Phys Biol 10 2013 036003
100. M. Maden Regeneration: every clot has a thrombin lining Curr Biol 13 2003 R517 R518
101. D. Rittirsch, M.A. Flierl, and P.A. Ward Harmful molecular mechanisms in sepsis Nat Rev Immunol 8 2008 776 787
102. M.L. Nierodzik, and S. Karpatkin Thrombin induces tumor growth, metastasis, and angiogenesis: Evidence for a thrombin-regulated dormant tumor phenotype Cancer Cell 10 2006 355 362 (Pubitemid 44693468)
103. G.H. Lyman, and A.A. Khorana Cancer, clots and consensus: new understanding of an old problem J Clin Oncol 27 2009 4821 4826
104. S. Danckwardt, A.S. Gantzert, S. Macher-Goeppinger, H.C. Probst, M. Gentzel, and M. Wilm et al. p38 MAPK controls prothrombin expression by regulated RNA 3' end processing Mol Cell 41 2011 298 310
105. M.L. Nierodzik, A. Plotkin, F. Kajumo, and S. Karpatkin Thrombin stimulates tumor-platelet adhesion in vitro and metastasis in vivo J Clin Invest 87 1991 229 236
106. J.J. Li, Y.Q. Huang, R. Basch, and S. Karpatkin Thrombin induces the release of angiopoietin-1 from platelets Thromb Haemost 85 2001 204 206 (Pubitemid 32140561)
107. N.E. Tsopanoglou, and M.E. Maragoudakis 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 274 1999 23969 23976
108. G. Finak, N. Bertos, F. Pepin, S. Sadekova, M. Souleimanova, and H. Zhao et al. Stromal gene expression predicts clinical outcome in breast cancer Nat Med 14 2008 518 527 (Pubitemid 351655218)
109. N. Esumi, D. Fan, and I.J. Fidler Inhibition of murine melanoma experimental metastasis by recombinant desulfatohirudin, a highly specific thrombin inhibitor Cancer Res 51 1991 4549 4556
110. M.T. Nieman, G. LaRusch, C. Fang, Y. Zhou, and A.H. Schmaier Oral thrombostatin FM19 inhibits prostate cancer Thromb Haemost 104 2010 1044 1048
111. I. Pabinger, J. Thaler, and C. Ay Biomarkers for prediction of venous thromboembolism in cancer Blood 122 2013 2011 2018
112. J. Thaler, C. Ay, H. Weinstabl, D. Dunkler, R. Simanek, and R. Vormittag et al. Circulating procoagulant microparticles in cancer patients Ann Hematol 90 2011 447 453
113. J. Thaler, C. Ay, N. Mackman, R.M. Bertina, A. Kaider, and C. Marosi et al. Microparticle-associated tissue factor activity, venous thromboembolism and mortality in pancreatic, gastric, colorectal and brain cancer patients J Thromb Haemost 10 2012 1363 1370
114. S. Taucher, A. Salat, M. Gnant, W. Kwasny, B. Mlineritsch, and R.C. Menzel et al. Impact of pretreatment thrombocytosis on survival in primary breast cancer Thromb Haemost 89 2003 1098 1106 (Pubitemid 36798163)
115. C. Ay, D. Dunkler, R. Pirker, J. Thaler, P. Quehenberger, and O. Wagner et al. High d-dimer levels are associated with poor prognosis in cancer patients Haematologica 97 2012 1158 1164
116. G. Arpaia, M. Carpenedo, M. Verga, O. Mastrogiacomo, D. Fagnani, and M. Lanfredini et al. d-dimer before chemotherapy might predict venous thromboembolism Blood Coagul Fibrinolysis 20 2009 170 175
117. P. Ferroni, F. Martini, I. Portarena, G. Massimiani, S. Riondino, and F. La Farina et al. Novel high-sensitive D-dimer determination predicts chemotherapy-associated venous thromboembolism in intermediate risk lung cancer patients Clin Lung Cancer 13 2012 482 487
118. M.T. Stender, J.B. Frokjaer, T.B. Larsen, S. Lundbye-Christensen, and O. Thorlacius-Ussing Preoperative plasma D-dimer is a predictor of postoperative deep venous thrombosis in colorectal cancer patients: A clinical, prospective cohort study with one-year follow-up Dis Colon Rectum 52 2009 446 451
119. C. Ay, R. Vormittag, D. Dunkler, R. Simanek, A.L. Chiriac, and J. Drach et al. d-dimer and prothrombin fragment 1 + 2 predict venous thromboembolism in patients with cancer: results from the Vienna Cancer and Thrombosis Study J Clin Oncol 27 2009 4124 4129
120. B. Dickmann, J. Ahlbrecht, C. Ay, D. Dunkler, J. Thaler, and W. Scheithauer et al. Regional lymph node metastases are a strong risk factor for venous thromboembolism: results from the Vienna Cancer and Thrombosis Study Haematologica 98 2013 1309 1314
121. J.J. Auwerda, Y. Yuana, S. Osanto, M.P. de Maat, P. Sonneveld, and R.M. Bertina et al. Microparticle-associated tissue factor activity and venous thrombosis in multiple myeloma Thromb Haemost 105 2011 14 20
122. F. Van Doormaal, A. Kleinjan, R.J. Berckmans, N. Mackman, D. Manly, and P.W. Kamphuisen et al. Coagulation activation and microparticle-associated coagulant activity in cancer patients. An exploratory prospective study Thromb Haemost 108 2012 160 165
123. I. Pabinger, and C. Ay Biomarkers and venous thromboembolism Arterioscler Thromb Vasc Biol 29 2009 332 336