Genetic basis of thrombosis in cancer

Seminars in Thrombosis and Hemostasis

Volumn 40, Issue 3, 2014, Pages 284-295

  D'Asti, Esterina ^a   Magnus, Nathalie ^a   Meehan, Brian ^a   Garnier, Delphine ^a   Rak, Janusz ^a  

^a MONTREAL CHILDREN S HOSPITAL   (Canada)

Author keywords

cancer; coagulation; microparticles; oncogenes; tissue factor

Indexed keywords

ARTICLE; BLOOD CLOTTING; BLOOD CLOTTING DISORDER; CANCER GENETICS; CANCER SURVIVAL; CANCER THERAPY; DISEASE COURSE; HUMAN; ONCOGENE; PERSONALIZED MEDICINE; PRIORITY JOURNAL; STROMA; TUMOR CELL; TUMOR GROWTH; TUMOR THROMBUS; VASCULAR TUMOR; ANIMAL; BLOOD; COMPLICATION; GENETICS; NEOPLASM; THROMBOSIS;

ANIMALS; HUMANS; NEOPLASMS; THROMBOSIS;

EID: 84897954649     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0034-1370766     Document Type: Article

References (161)

1. Dvorak H. F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med: 1986; 315 26 1650 1659
2. Browder T., Folkman J., Pirie-Shepherd S. The hemostatic system as a regulator of angiogenesis. J Biol Chem: 2000; 275 3 1521 1524
3. Dahlbäck B. Coagulation and inflammation-close allies in health and disease. Semin Immunopathol: 2012; 34 1 1 3
4. van Hinsbergh V. W. Endothelium-role in regulation of coagulation and inflammation. Semin Immunopathol: 2012; 34 1 93 106
5. Ruf W. Tissue factor and cancer. Thromb Res: 2012; 130 01 S84 S87
6. Degen J. L., Palumbo J. S. Hemostatic factors, innate immunity and malignancy. Thromb Res: 2012; 129 01 S1 S5
7. Fang H., Declerck Y. A. Targeting the tumor microenvironment: from understanding pathways to effective clinical trials. Cancer Res: 2013; 73 16 4965 4977
8. Peinado H., Alečković M., Lavotshkin S., et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med: 2012; 18 6 883 891
9. Folkman J. Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov: 2007; 6 4 273 286
10. Mantovani A., Garlanda C. Platelet-macrophage partnership in innate immunity and inflammation. Nat Immunol: 2013; 14 8 768 770
11. Trousseau A. Phlegmasia alba dolens. Clinique Medicale de l'Hotel -Dieu de Paris. Paris, France The Sydenham Society 2nd: 1865; 654 712
12. Falanga A., Marchetti M., Vignoli A. Coagulation and cancer: biological and clinical aspects. J Thromb Haemost: 2013; 11 2 223 233
13. Rickles F. R., Patierno S., Fernandez P. M. Tissue factor, thrombin, and cancer. Chest: 2003; 124 (3, Suppl): 58S 68S
14. Tchou J., Conejo-Garcia J. Targeting the tumor stroma as a novel treatment strategy for breast cancer: shifting from the neoplastic cell-centric to a stroma-centric paradigm. Adv Pharmacol: 2012; 65 45 61
15. Ferrara N. VEGF as a therapeutic target in cancer. Oncology: 2005; 69 03 11 16
16. Kerbel R. S. Tumor angiogenesis. N Engl J Med: 2008; 358 19 2039 2049
17. Carmeliet P., Jain R. K. Molecular mechanisms and clinical applications of angiogenesis. Nature: 2011; 473 7347 298 307
18. Mackman N. Triggers, targets and treatments for thrombosis. Nature: 2008; 451 7181 914 918
19. Abe K., Shoji M., Chen J., 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: 1999; 96 15 8663 8668
20. von Hundelshausen P., Weber C., von HP. Platelets as immune cells: bridging inflammation and cardiovascular disease. Circ Res: 2007; 100 1 27 40
21. Semple J. W., Italiano J. E. Jr, Freedman J. Platelets and the immune continuum. Nat Rev Immunol: 2011; 11 4 264 274
22. Schulz C., Engelmann B., Massberg S. Crossroads of coagulation and innate immunity: the case of deep vein thrombosis. J Thromb Haemost: 2013; 11 01 233 241
23. Semenza G. L. Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci: 2012; 33 4 207 214
24. Finak G., Bertos N., Pepin F., et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med: 2008; 14 5 518 527
25. Rak J. Ras oncogenes and tumor vascular interface. In: Thomas-Tikhonenko A., ed. Cancer Genome and Tumor Microenvironment. New York, NY Springer: 2009; 133 165
26. Magnus N., Garnier D., Rak J. Oncogenic epidermal growth factor receptor up-regulates multiple elements of the tissue factor signaling pathway in human glioma cells. Blood: 2010; 116 5 815 818
27. Magnus N., Gerges N., Jabado N., Rak J. Coagulation-related gene expression profile in glioblastoma is defined by molecular disease subtype. J Thromb Haemost: 2013; 11 6 1197 1200
28. Timp J. F., Braekkan S. K., Versteeg H. H., Cannegieter S. C. Epidemiology of cancer-associated venous thrombosis. Blood: 2013; 122 10 1712 1723
29. Sturm D., Witt H., Hovestadt V., et al. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell: 2012; 22 4 425 437
30. Bishop J. M. Cancer: the rise of the genetic paradigm. Genes Dev: 1995; 9 11 1309 1315
31. Gerlinger M., Rowan A. J., Horswell S., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med: 2012; 366 10 883 892
32. Killela P. J., Reitman Z. J., Jiao Y., et al. TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc Natl Acad Sci U S A: 2013; 110 15 6021 6026
33. Rak J., Mitsuhashi Y., Bayko L., et al. Mutant ras oncogenes upregulate VEGF/VPF expression: implications for induction and inhibition of tumor angiogenesis. Cancer Res: 1995; 55 20 4575 4580
34. Petit A. M., Rak J., Hung M-C., et al. Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor tyrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am J Pathol: 1997; 151 6 1523 1530
35. Rastinejad F., Polverini P. J., Bouck N. P. Regulation of the activity of a new inhibitor of angiogenesis by a cancer suppressor gene. Cell: 1989; 56 3 345 355
36. Volpert O. V., Pili R., Sikder H. A., et al. Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1. Cancer Cell: 2002; 2 6 473 483
37. Takahashi Y., Bucana C. D., Cleary K. R., Ellis L. M. p53, vessel count, and vascular endothelial growth factor expression in human colon cancer. Int J Cancer: 1998; 79 1 34 38
38. Bouck N., Stellmach V., Hsu S. C. How tumors become angiogenic. Adv Cancer Res: 1996; 69 135 174
39. Zabrenetzky V., Harris C. C., Steeg P. S., Roberts D. D. Expression of the extracellular matrix molecule thrombospondin inversely correlates with malignant progression in melanoma, lung and breast carcinoma cell lines. Int J Cancer: 1994; 59 2 191 195
40. Teodoro J. G., Parker A. E., Zhu X., Green M. R. p53-mediated inhibition of angiogenesis through up-regulation of a collagen prolyl hydroxylase. Science: 2006; 313 5789 968 971
41. Assadian S., El-Assaad W., Wang X. Q., et al. p53 inhibits angiogenesis by inducing the production of Arresten. Cancer Res: 2012; 72 5 1270 1279
42. Mazure N. M., Chen E. Y., Yeh P., Laderoute K. R., Giaccia A. J. Oncogenic transformation and hypoxia synergistically act to modulate vascular endothelial growth factor expression. Cancer Res: 1996; 56 15 3436 3440
43. Viloria-Petit A., Miquerol L., Yu J. L., et al. Contrasting effects of VEGF gene disruption in embryonic stem cell-derived versus oncogene-induced tumors. EMBO J: 2003; 22 16 4091 4102
44. Casanovas O., Hicklin D. J., Bergers G., Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell: 2005; 8 4 299 309
45. Phan V. T., Wu X., Cheng J. H., et al. Oncogenic RAS pathway activation promotes resistance to anti-VEGF therapy through G-CSF-induced neutrophil recruitment. Proc Natl Acad Sci U S A: 2013; 110 15 6079 6084
46. Yachida S., Iacobuzio-Donahue C. A. Evolution and dynamics of pancreatic cancer progression. Oncogene: 2013; 32 45 5253 5260
47. Feig C., Gopinathan A., Neesse A., Chan D. S., Cook N., Tuveson D. A. The pancreas cancer microenvironment. Clin Cancer Res: 2012; 18 16 4266 4276
48. Tas F., Karabulut S., Bilgin E., Kılıc L., Ciftci R., Duranyildiz D. Clinical significance of coagulation assays in metastatic pancreatic adenocarcinoma. J Gastrointest Cancer: 2013; 44 4 404 409
49. Wun T., White R. H. Epidemiology of cancer-related venous thromboembolism. Best Pract Res Clin Haematol: 2009; 22 1 9 23
50. Sparmann A., Bar-Sagi D. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell: 2004; 6 5 447 458
51. Ancrile B., Lim K. H., Counter C. M. Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis. Genes Dev: 2007; 21 14 1714 1719
52. Demers M., Krause D. S., Schatzberg D., et al. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci U S A: 2012; 109 32 13076 13081
53. Borrello M. G., Degl'Innocenti D., Pierotti M. A. Inflammation and cancer: the oncogene-driven connection. Cancer Lett: 2008; 267 2 262 270
54. Burrell K., Agnihotri S., Leung M., Dacosta R., Hill R., Zadeh G. A novel high-resolution in vivo imaging technique to study the dynamic response of intracranial structures to tumor growth and therapeutics. J Vis Exp: 2013; 76 e50363
55. Lisanti M. P., Martinez-Outschoorn U. E., Sotgia F. Oncogenes induce the cancer-associated fibroblast phenotype: Metabolic symbiosis and fibroblast addiction are new therapeutic targets for drug discovery. Cell Cycle: 2013; 123 17 2723 2732
56. Tchou J., Kossenkov A. V., Chang L., et al. Human breast cancer associated fibroblasts exhibit subtype specific gene expression profiles. BMC Med Genomics: 2012; 5 39
57. Hill R., Song Y., Cardiff R. D., Van Dyke T. Selective evolution of stromal mesenchyme with p53 loss in response to epithelial tumorigenesis. Cell: 2005; 123 6 1001 1011
58. Ricci-Vitiani L., Pallini R., Biffoni M., et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature: 2010; 468 7325 824 828
59. Soda Y., Marumoto T., Friedmann-Morvinski D., et al. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc Natl Acad Sci U S A: 2011; 108 11 4274 4280
60. Al-Nedawi K., Meehan B., Kerbel R. S., Allison A. C., Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A: 2009; 106 10 3794 3799
61. Skog J., Würdinger T., van Rijn S., et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol: 2008; 10 12 1470 1476
62. Yang F. C., Ingram D. A., Chen S., et al. Nf1-dependent tumors require a microenvironment containing Nf1+/- and c-kit-dependent bone marrow. Cell: 2008; 135 3 437 448
63. Bronisz A., Godlewski J., Wallace J. A., et al. Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320. Nat Cell Biol: 2012; 14 2 159 167
64. Josson S., Matsuoka Y., Chung L. W., Zhau H. E., Wang R. Tumor-stroma co-evolution in prostate cancer progression and metastasis. Semin Cell Dev Biol: 2010; 21 1 26 32
65. Smalheiser N. R. Do Neural Cells Communicate with Endothelial Cells via Secretory Exosomes and Microvesicles? Cardiovasc Psychiatry Neurol: 2009; 2009 383086
66. Rak J. Extracellular vesicles - biomarkers and effectors of the cellular interactome in cancer. Front Pharmacol: 2013; 4 21
67. Luga V., Zhang L., Viloria-Petit A. M., et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell: 2012; 151 7 1542 1556
68. Ratajczak J., Wysoczynski M., Hayek F., Janowska-Wieczorek A., Ratajczak M. Z. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia: 2006; 20 9 1487 1495
69. Grange C., Tapparo M., Collino F., et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res: 2011; 71 15 5346 5356
70. Putz U., Doan A., Tan S-S. The tumor suppressor PTEN is transported in exosomes for extracellular phosphatase activity. J Extracellular Vesicles: 2012; 1 78
71. Al-Nedawi K., Meehan B., Micallef J., et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol: 2008; 10 5 619 624
72. Rak J., Klement G. Impact of oncogenes and tumor suppressor genes on deregulation of hemostasis and angiogenesis in cancer. Cancer Metastasis Rev: 2000; 19 1-2 93 96
73. Jain R. K., di Tomaso E., Duda D. G., Loeffler J. S., Sorensen A. G., Batchelor T. T. Angiogenesis in brain tumours. Nat Rev Neurosci: 2007; 8 8 610 622
74. Dvorak H. F., Quay S. C., Orenstein N. S., et al. Tumor shedding and coagulation. Science: 1981; 212 4497 923 924
75. Tehrani M., Friedman T. M., Olson J. J., Brat D. J. Intravascular thrombosis in central nervous system malignancies: a potential role in astrocytoma progression to glioblastoma. Brain Pathol: 2008; 18 2 164 171
76. Rong Y., Durden D. L., Van Meir E. G., Brat D. J. 'Pseudopalisading' necrosis in glioblastoma: a familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis. J Neuropathol Exp Neurol: 2006; 65 6 529 539
77. Brat D. J., Van Meir E. G. Vaso-occlusive and prothrombotic mechanisms associated with tumor hypoxia, necrosis, and accelerated growth in glioblastoma. Lab Invest: 2004; 84 4 397 405
78. Holash J., Maisonpierre P. C., Compton D., et al. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science: 1999; 284 5422 1994 1998
79. Del Conde I., Shrimpton C. N., Thiagarajan P., López J. A. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood: 2005; 106 5 1604 1611
80. Rak J., Yu J., Milsom C. Oncogene-driven hemostatic changes in cancer. Cancer Invest: 2009; 27 s1 28 35
81. Rak J., Yu J. L., Luyendyk J., Mackman N. Oncogenes, trousseau syndrome, and cancer-related changes in the coagulome of mice and humans. Cancer Res: 2006; 66 22 10643 10646
82. Yu J. L., May L., Lhotak V., et al. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood: 2005; 105 4 1734 1741
83. Regina S., Valentin J. B., Lachot S., Lemarié E., Rollin J., Gruel Y. Increased tissue factor expression is associated with reduced survival in non-small cell lung cancer and with mutations of TP53 and PTEN. Clin Chem: 2009; 55 10 1834 1842
84. Regina S., Rollin J., Bléchet C., Iochmann S., Reverdiau P., Gruel Y. Tissue factor expression in non-small cell lung cancer: relationship with vascular endothelial growth factor expression, microvascular density, and K-ras mutation. J Thorac Oncol: 2008; 3 7 689 697
85. Milsom C. C., Yu J. L., Mackman N., et al. Tissue factor regulation by epidermal growth factor receptor and epithelial-to-mesenchymal transitions: effect on tumor initiation and angiogenesis. Cancer Res: 2008; 68 24 10068 10076
86. 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
87. Rong Y., Hu F., Huang R., et al. Early growth response gene-1 regulates hypoxia-induced expression of tissue factor in glioblastoma multiforme through hypoxia-inducible factor-1-independent mechanisms. Cancer Res: 2006; 66 14 7067 7074
88. Rong Y., Belozerov V. E., Tucker-Burden C., et al. Epidermal growth factor receptor and PTEN modulate tissue factor expression in glioblastoma through JunD/activator protein-1 transcriptional activity. Cancer Res: 2009; 69 6 2540 2549
89. Jähner D., Hunter T. The stimulation of quiescent rat fibroblasts by v-src and v-fps oncogenic protein-tyrosine kinases leads to the induction of a subset of immediate early genes. Oncogene: 1991; 6 7 1259 1268
90. Provençal M., Berger-Thibault N., Labbé D., et al. Tissue factor mediates the HGF/Met-induced anti-apoptotic pathway in DAOY medulloblastoma cells. J Neurooncol: 2010; 97 3 365 372
91. D'Asti E., Huang A., Rak J. Downregulation of tissue factor (TF) in medulloblastoma cells expressing miR-520g. Presented at: Keystone Syposia; March 30, 2012; Snowmass, CO
92. Yu G., Li H., Wang X., et al. MicroRNA-19a targets tissue factor to inhibit colon cancer cells migration and invasion. Mol Cell Biochem: 2013; 380 1-2 239 247
93. Yu Y-H, Wu D-S, Huang F-F., et al. MicroRNA-20b and ERK1/2 pathway independently regulate the expression of tissue factor in hematopoietic and trophoblastic differentiation of human embryonic stem cells. Stem Cell Res Ther: 2013; 4 5s 121
94. Tallman M. S., Lefèbvre P., Baine R. M., et al. Effects of all-trans retinoic acid or chemotherapy on the molecular regulation of systemic blood coagulation and fibrinolysis in patients with acute promyelocytic leukemia. J Thromb Haemost: 2004; 2 8 1341 1350
95. Falanga A., Marchetti M., Vignoli A., et al. V617F JAK-2 mutation in patients with essential thrombocythemia: relation to platelet, granulocyte, and plasma hemostatic and inflammatory molecules. Exp Hematol: 2007; 35 5 702 711
96. 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
97. van den Berg Y. W., van den Hengel L. G., Myers H. R., et al. Alternatively spliced tissue factor induces angiogenesis through integrin ligation. Proc Natl Acad Sci U S A: 2009; 106 46 19497 19502
98. Boccaccio C., Sabatino G., Medico E., et al. The MET oncogene drives a genetic programme linking cancer to haemostasis. Nature: 2005; 434 7031 396 400
99. Koizume S., Jin M. S., Miyagi E., et al. Activation of cancer cell migration and invasion by ectopic synthesis of coagulation factor VII. Cancer Res: 2006; 66 19 9453 9460
100. Schulze E. B., Hedley B. D., Goodale D., et al. The thrombin inhibitor Argatroban reduces breast cancer malignancy and metastasis via osteopontin-dependent and osteopontin-independent mechanisms. Breast Cancer Res Treat: 2008; 112 2 243 254
101. Ohgaki H., Kleihues P. Genetic profile of astrocytic and oligodendroglial gliomas. Brain Tumor Pathol: 2011; 28 3 177 183
102. Verhaak R. G., Hoadley K. A., Purdom E., et al. Cancer Genome Atlas Research Network. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell: 2010; 17 1 98 110
103. Kool M., Korshunov A., Remke M., et al. Molecular subgroups of medulloblastoma: an international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta Neuropathol: 2012; 123 4 473 484
104. Northcott P. A., Korshunov A., Witt H., et al. Medulloblastoma comprises four distinct molecular variants. J Clin Oncol: 2011; 29 11 1408 1414
105. Rickles F. R. Mechanisms of cancer-induced thrombosis in cancer. Pathophysiol Haemost Thromb: 2006; 35 1-2 103 110
106. Kasthuri R. S., Taubman M. B., Mackman N. Role of tissue factor in cancer. J Clin Oncol: 2009; 27 29 4834 4838
107. Nash G. F. Tissue factor (TF) and vascular endothelial growth factor (VEGF) expression in colorectal cancer: relation with cancer recurrence. Colorectal Dis: 2007; 9 9 858 859
108. Young A., Chapman O., Connor C., Poole C., Rose P., Kakkar A. K. Thrombosis and cancer. Nat Rev Clin Oncol: 2012; 9 8 437 449
109. Buller H. R., van Doormaal F. F., van Sluis G. L., Kamphuisen P. W. Cancer and thrombosis: from molecular mechanisms to clinical presentations. J Thromb Haemost: 2007; 5 01 246 254
110. Versteeg H. H., Schaffner F., Kerver M., et al. Inhibition of tissue factor signaling suppresses tumor growth. Blood: 2008; 111 1 190 199
111. Keshava S., Kothari H., Rao L. V., Pendurthi U. R. Influence of endothelial cell protein C receptor on breast cancer development. J Thromb Haemost: 2013; 11 11 2062 2065
112. Amirkhosravi A., Meyer T., Amaya M., et al. The role of tissue factor pathway inhibitor in tumor growth and metastasis. Semin Thromb Hemost: 2007; 33 7 643 652
113. Auer R. A., Scheer A. S., McSparron J. I., et al. Postoperative venous thromboembolism predicts survival in cancer patients. Ann Surg: 2012; 255 5 963 970
114. Gil-Bernabé A. M., Ferjancic S., Tlalka M., et al. Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice. Blood: 2012; 119 13 3164 3175
115. Zacharski L. R. Malignancy as a solid-phase coagulopathy: implications for the etiology, pathogenesis, and treatment of cancer. Semin Thromb Hemost: 2003; 29 3 239 246
116. Palumbo J. S., Talmage K. E., Massari J. V., 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: 2007; 110 1 133 141
117. Ngo C. V., Picha K., McCabe F., et al. 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
118. Liu Y., Jiang P., Capkova K., et al. Tissue factor-activated coagulation cascade in the tumor microenvironment is critical for tumor progression and an effective target for therapy. Cancer Res: 2011; 71 20 6492 6502
119. Zhao J., Aguilar G., Palencia S., Newton E., Abo A. rNAPc2 inhibits colorectal cancer in mice through tissue factor. Clin Cancer Res: 2009; 15 1 208 216
120. Vossen C. Y., Hoffmeister M., Chang-Claude J. C., Rosendaal F. R., Brenner H. Clotting factor gene polymorphisms and colorectal cancer risk. J Clin Oncol: 2011; 29 13 1722 1727
121. Palumbo J. S., Degen J. L. Mechanisms coupling the hemostatic system to colitis-associated cancer. Thromb Res: 2010; 125 02 S39 S43
122. Sorensen H. T., Mellemkjaer L., Olsen J. H., Baron J. A. Prognosis of cancers associated with venous thromboembolism. N Engl J Med: 2000; 343 25 1846 1850
123. Fotopoulou C., duBois A., Karavas A. N., et al. Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group. Incidence of venous thromboembolism in patients with ovarian cancer undergoing platinum/paclitaxel- containing first-line chemotherapy: an exploratory analysis by the Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group. J Clin Oncol: 2008; 26 16 2683 2689
124. Kakkar A. K., Levine M. N., Kadziola Z., et al. Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: the fragmin advanced malignancy outcome study (FAMOUS). J Clin Oncol: 2004; 22 10 1944 1948
125. Lee A. Y., Rickles F. R., Julian J. A., et al. Randomized comparison of low molecular weight heparin and coumarin derivatives on the survival of patients with cancer and venous thromboembolism. J Clin Oncol: 2005; 23 10 2123 2129
126. Altinbas M., Coskun H. S., Er O., et al. A randomized clinical trial of combination chemotherapy with and without low-molecular-weight heparin in small cell lung cancer. J Thromb Haemost: 2004; 2 8 1266 1271
127. Klerk C. P., Smorenburg S. M., Otten H. M., et al. The effect of low molecular weight heparin on survival in patients with advanced malignancy. J Clin Oncol: 2005; 23 10 2130 2135
128. Akl E. A., Gunukula S., Barba M., et al. Parenteral anticoagulation in patients with cancer who have no therapeutic or prophylactic indication for anticoagulation. Cochrane Database Syst Rev: 2011; 4 CD006652
129. Zhang J., Zhang Y. L., Ma K. X., Qu J. M. Efficacy and safety of adjunctive anticoagulation in patients with lung cancer without indication for anticoagulants: a systematic review and meta-analysis. Thorax: 2013; 68 5 442 450
130. Weitz J. I. Potential of new anticoagulants in patients with cancer. Thromb Res: 2010; 125 02 S30 S35
131. Khorana A. A. Venous thromboembolism and prognosis in cancer. Thromb Res: 2010; 125 6 490 493
132. Soff G. A. Pathophysiology and management of thrombosis in cancer: 150 years of progress. J Thromb Thrombolysis: 2013; 35 3 346 351
133. Yu J., May L., Milsom C., et al. Contribution of host-derived tissue factor to tumor neovascularization. Arterioscler Thromb Vasc Biol: 2008; 28 11 1975 1981
134. Vogelstein B., Papadopoulos N., Velculescu V. E., Zhou S., Diaz L. A. Jr, Kinzler K. W. Cancer genome landscapes. Science: 2013; 339 6127 1546 1558
135. Rak J., Milsom C., Yu J. Vascular determinants of cancer stem cell dormancy-do age and coagulation system play a role? APMIS: 2008; 116 7-8 660 676
136. Dick J. E. Looking ahead in cancer stem cell research. Nat Biotechnol: 2009; 27 1 44 46
137. Calabrese C., Poppleton H., Kocak M., et al. A perivascular niche for brain tumor stem cells. Cancer Cell: 2007; 11 1 69 82
138. Ghajar C. M., Peinado H., Mori H., et al. The perivascular niche regulates breast tumour dormancy. Nat Cell Biol: 2013; 15 7 807 817
139. Fidler I. J. Biological heterogeneity of cancer: implication to therapy. Hum Vaccin Immunother: 2012; 8 8 1141 1142
140. Milsom C., Magnus N., Meehan B., Al-Nedawi K., Garnier D., Rak J. Tissue factor and cancer stem cells: is there a linkage? Arterioscler Thromb Vasc Biol: 2009; 29 12 2005 2014
141. Milsom C., Anderson G. M., Weitz J. I., Rak J. Elevated tissue factor procoagulant activity in CD133-positive cancer cells. J Thromb Haemost: 2007; 5 12 2550 2552
142. Garnier D., Magnus N., Lee T. H., et al. Cancer cells induced to express mesenchymal phenotype release exosome-like extracellular vesicles carrying tissue factor. J Biol Chem: 2012; 287 52 43565 43572
143. Aguirre-Ghiso J. A. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer: 2007; 7 11 834 846
144. Black W. C., Welch H. G. Advances in diagnostic imaging and overestimations of disease prevalence and the benefits of therapy. N Engl J Med: 1993; 328 17 1237 1243
145. Nierodzik M. L., Karpatkin S. Thrombin induces tumor growth, metastasis, and angiogenesis: Evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell: 2006; 10 5 355 362
146. Miller J. W., Adamis A. P., Shima D. T., et al. Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model. Am J Pathol: 1994; 145 3 574 584
147. Magnus N., Garnier D., Meehan B., et al. Tissue factor expression provokes escape from tumor dormancy and leads to genomic alterations (e-pub ahead of print). Proc Natl Acad Sci USA: 2013;; doi: 10.1073/pnas.1314118111
148. Rak J. Microparticles in cancer. Semin Thromb Hemost: 2010; 36 8 888 906
149. Dignat-George F., Boulanger C. M. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol: 2011; 31 1 27 33
150. 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
151. Rauch U., Antoniak S., Boots M., et al. 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
152. Giesen P. L., Nemerson Y. Tissue factor on the loose. Semin Thromb Hemost: 2000; 26 4 379 384
153. Geddings J. E., Mackman N. Tumor-derived tissue factor-positive microparticles and venous thrombosis in cancer patients. Blood: 2013; 122 11 1873 1880
154. Rak J., Klement P., Yu J. Genetic determinants of cancer coagulopathy, angiogenesis and disease progression. Vnitr Lek: 2006; 52 01 135 138
155. Izumi H., Takahashi C., Oh J., Noda M. Tissue factor pathway inhibitor-2 suppresses the production of active matrix metalloproteinase-2 and is down-regulated in cells harboring activated ras oncogenes. FEBS Lett: 2000; 481 1 31 36
156. Mazzieri R., Furlan F., D'Alessio S., et al. A direct link between expression of urokinase plasminogen activator receptor, growth rate and oncogenic transformation in mouse embryonic fibroblasts. Oncogene: 2007; 26 5 725 732
157. Zhao Y., Xiao A., Dipierro C. G., et al. H-Ras increases urokinase expression and cell invasion in genetically modified human astrocytes through Ras/Raf/MEK signaling pathway. Glia: 2008; 56 8 917 924
158. Yu J. L., May L., Klement P., Weitz J. I., Rak J. Oncogenes as regulators of tissue factor expression in cancer: implications for tumor angiogenesis and anti-cancer therapy. Semin Thromb Hemost: 2004; 30 1 21 30
159. Yu J. L., Xing R., Milsom C., Rak J. Modulation of the oncogene-dependent tissue factor expression by kinase suppressor of ras 1. Thromb Res: 2010; 126 1 e6 e10
160. Provençal M., Labbé D., Veitch R., et al. c-Met activation in medulloblastoma induces tissue factor expression and activity: effects on cell migration. Carcinogenesis: 2009; 30 7 1089 1096
161. Zhang X., Yu H., Lou J. R., et al. MicroRNA-19 (miR-19) regulates tissue factor expression in breast cancer cells. J Biol Chem: 2011; 286 2 1429 1435