Brain neoplasms and coagulation

Seminars in Thrombosis and Hemostasis

Volumn 39, Issue 8, 2013, Pages 881-895

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

^a MONTREAL CHILDREN S HOSPITAL   (Canada)

Author keywords

brain tumors; coagulation; microparticles; molecular subtypes; oncogenes; tissue factor; tumor dormancy

Indexed keywords

ANTIVITAMIN K; BEVACIZUMAB; BLOOD CLOTTING FACTOR 7A; CANCER PROCOAGULANT; D DIMER; ENDOTHELIAL PROTEIN C RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR; HISTONE H3; INTEGRIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN C; PROTEIN P53; PROTEIN TYROSINE KINASE; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTHROMBIN; RAS PROTEIN; SCATTER FACTOR RECEPTOR; THROMBIN; THROMBOMODULIN; THROMBOPLASTIN; TISSUE FACTOR PATHWAY INHIBITOR; TISSUE PLASMINOGEN ACTIVATOR; VASCULOTROPIN;

ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; ANTICOAGULATION; ARTICLE; ASTROCYTOMA; BLOOD CLOTTING; BLOOD CLOTTING DISORDER; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; BRAIN CANCER; BRAIN HEMORRHAGE; BRAIN HYPOXIA; BRAIN METASTASIS; CANCER CONTROL; CANCER DIAGNOSIS; CANCER REGRESSION; CANCER STEM CELL; CANCER SUSCEPTIBILITY; CELL PROTECTION; DORMANCY; EPENDYMOMA; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; GLIOBLASTOMA; HEMOSTASIS; HETEROZYGOSITY LOSS; HUMAN; IMMUNOSURVEILLANCE; LOSS OF FUNCTION MUTATION; MEDULLOBLASTOMA; MELANOMA; MENINGIOMA; MISSENSE MUTATION; NEUROECTODERM TUMOR; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYSTEMIC CIRCULATION; THROMBOCYTE ACTIVATION; THROMBOEMBOLISM; THROMBOSIS; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR GENE; TUMOR VASCULARIZATION; UPREGULATION; VENOUS THROMBOEMBOLISM;

ADULT; BLOOD COAGULATION; BRAIN NEOPLASMS; CHILD; GLIOBLASTOMA; HUMANS; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION; THROMBOPLASTIN;

EID: 84887045971     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0033-1357483     Document Type: Article

References (188)

1. Bondy M. L., Scheurer M. E., Malmer B., et al. Brain Tumor Epidemiology Consortium. Brain tumor epidemiology: consensus from the Brain Tumor Epidemiology Consortium. Cancer: 2008; 113 (7, Suppl): 1953 1968
2. Wen P. Y., Kesari S. Malignant gliomas in adults. N Engl J Med: 2008; 359 5 492 507
3. 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
4. Phillips H. S., Kharbanda S., Chen R., et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell: 2006; 9 3 157 173
5. 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
6. 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
7. 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
8. 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
9. Perry J. R. Thromboembolic disease in patients with high-grade glioma. Neuro-oncol: 2012; 14 04 iv73 iv80
10. Thaler J., Ay C., Mackman N., et al. Microparticle-associated tissue factor activity, venous thromboembolism and mortality in pancreatic, gastric, colorectal and brain cancer patients. J Thromb Haemost: 2012; 10 7 1363 1370
11. Sartori M. T., Della Puppa A., Ballin A., et al. Prothrombotic state in glioblastoma multiforme: an evaluation of the procoagulant activity of circulating microparticles. J Neurooncol: 2011; 104 1 225 231
12. Jenkins E. O., Schiff D., Mackman N., Key N. S. Venous thromboembolism in malignant gliomas. J Thromb Haemost: 2010; 8 2 221 227
13. 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
14. Zwicker J. I., Trenor C. C. III, Furie B. C., Furie B. Tissue factor-bearing microparticles and thrombus formation. Arterioscler Thromb Vasc Biol: 2011; 31 4 728 733
15. Hossmann K. A. The hypoxic brain. Insights from ischemia research. Adv Exp Med Biol: 1999; 474 155 169
16. Henry-Feugeas M. C., Koskas P. Cerebral vascular aging: extending the concept of pulse wave encephalopathy through capillaries to the cerebral veins. Curr Aging Sci: 2012; 5 2 157 167
17. Kieran M. W., Walker D., Frappaz D., Prados M. Brain tumors: from childhood through adolescence into adulthood. J Clin Oncol: 2010; 28 32 4783 4789
18. Wrensch M., Minn Y., Chew T., Bondy M., Berger M. S. Epidemiology of primary brain tumors: current concepts and review of the literature. Neuro-oncol: 2002; 4 4 278 299
19. Zhu Y., Parada L. F. The molecular and genetic basis of neurological tumours. Nat Rev Cancer: 2002; 2 8 616 626
20. Gilbertson R. J., Ellison D. W. The origins of medulloblastoma subtypes. Annu Rev Pathol: 2008; 3 341 365
21. Pfister S., Witt O. Pediatric gliomas. Recent Results Cancer Res: 2009; 171 67 81
22. Ohgaki H., Kleihues P. Genetic alterations and signaling pathways in the evolution of gliomas. Cancer Sci: 2009; 100 12 2235 2241
23. 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
24. Schwartzentruber J., Korshunov A., Liu X. Y., et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature: 2012; 482 7384 226 231
25. Bredel M., Scholtens D. M., Yadav A. K., et al. NFKBIA deletion in glioblastomas. N Engl J Med: 2011; 364 7 627 637
26. Li J., Sulman E., Aldape K. Molecular biology of brain tumors. Handb Clin Neurol: 2012; 104 23 34
27. Parsons D. W., Jones S., Zhang X., et al. An integrated genomic analysis of human glioblastoma multiforme. Science: 2008; 321 5897 1807 1812
28. Northcott P. A., Korshunov A., Pfister S. M., Taylor M. D. The clinical implications of medulloblastoma subgroups. Nat Rev Neurol: 2012; 8 6 340 351
29. Calabrese C., Poppleton H., Kocak M., et al. A perivascular niche for brain tumor stem cells. Cancer Cell: 2007; 11 1 69 82
30. Gilbertson R. J., Rich J. N. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer: 2007; 7 10 733 736
31. Biernat W., Huang H., Yokoo H., Kleihues P., Ohgaki H. Predominant expression of mutant EGFR (EGFRvIII) is rare in primary glioblastomas. Brain Pathol: 2004; 14 2 131 136
32. Inda M. M., Bonavia R., Mukasa A., et al. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev: 2010; 24 16 1731 1745
33. Snuderl M., Fazlollahi L., Le L. P., et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell: 2011; 20 6 810 817
34. Wu X., Northcott P. A., Dubuc A., et al. Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature: 2012; 482 7386 529 533
35. Dirks P. B. Brain tumor stem cells: bringing order to the chaos of brain cancer. J Clin Oncol: 2008; 26 17 2916 2924
36. 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
37. Rak J. Ras oncogenes and tumour vascular interface. In: Thomas-Tikhonenko A., ed. Cancer Genome and Tumor Microenvironment. New York, NY Springer: 2009; 133 165
38. Steeg P. S., Camphausen K. A., Smith Q. R. Brain metastases as preventive and therapeutic targets. Nat Rev Cancer: 2011; 11 5 352 363
39. Gril B., Evans L., Palmieri D., Steeg P. S. Translational research in brain metastasis is identifying molecular pathways that may lead to the development of new therapeutic strategies. Eur J Cancer: 2010; 46 7 1204 1210
40. Schettino C., Bareschino M. A., Rossi A., et al. Targeting angiogenesis for treatment of NSCLC brain metastases. Curr Cancer Drug Targets: 2012; 12 3 289 299
41. Curtis C., Shah S. P., Chin S. F., et al. METABRIC Group. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature: 2012; 486 7403 346 352
42. Bos P. D., Zhang X. H., Nadal C., et al. Genes that mediate breast cancer metastasis to the brain. Nature: 2009; 459 7249 1005 1009
43. Heyn C., Ronald J. A., Ramadan S. S., et al. In vivo MRI of cancer cell fate at the single-cell level in a mouse model of breast cancer metastasis to the brain. Magn Reson Med: 2006; 56 5 1001 1010
44. Izraely S., Sagi-Assif O., Klein A., et al. The metastatic microenvironment: brain-residing melanoma metastasis and dormant micrometastasis. Int J Cancer: 2012; 131 5 1071 1082
45. Folkman J., Kalluri R. Tumor angiogenesis. In: Kufe D. W., Pollock R. E., Weichselbaum R. R., et al., eds. Cancer Medicine. Hamilton, London BC Decker Inc.: 2003; 161 194
46. Carmeliet P., Jain R. K. Molecular mechanisms and clinical applications of angiogenesis. Nature: 2011; 473 7347 298 307
47. Xi G., Fewel M. E., Hua Y., Thompson B. G. Jr, Hoff J. T., Keep R. F. Intracerebral hemorrhage: pathophysiology and therapy. Neurocrit Care: 2004; 1 1 5 18
48. Hardee M. E., Zagzag D. Mechanisms of glioma-associated neovascularization. Am J Pathol: 2012; 181 4 1126 1141
49. Maegele M. Coagulopathy after traumatic brain injury: incidence, pathogenesis, and treatment options. Transfusion: 2013; 53 01 28S 37S
50. Zadeh G., Koushan K., Baoping Q., Shannon P., Guha A. Role of angiopoietin-2 in regulating growth and vascularity of astrocytomas. J Oncol: 2010; 2010 659231
51. D'Haene N., Catteau X., Maris C., Martin B., Salmon I., Decaestecker C. Endothelial hyperplasia and endothelial galectin-3 expression are prognostic factors in primary central nervous system lymphomas. Br J Haematol: 2008; 140 4 402 410
52. Goldschmidt N., Linetsky E., Shalom E., Varon D., Siegal T. High incidence of thromboembolism in patients with central nervous system lymphoma. Cancer: 2003; 98 6 1239 1242
53. Gijtenbeek J. M., Wesseling P., Maass C., Burgers L., van der Laak J. A. Three-dimensional reconstruction of tumor microvasculature: simultaneous visualization of multiple components in paraffin-embedded tissue. Angiogenesis: 2005; 8 4 297 305
54. Benjamin L. E., Golijanin D., Itin A., Pode D., Keshet E. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J Clin Invest: 1999; 103 2 159 165
55. Döme B., Hendrix M. J., Paku S., Tóvári J., Tímár J. Alternative vascularization mechanisms in cancer: Pathology and therapeutic implications. Am J Pathol: 2007; 170 1 1 15
56. 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
57. Butler J. M., Kobayashi H., Rafii S. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer: 2010; 10 2 138 146
58. Lu J., Ye X., Fan F., et al. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell: 2013; 23 2 171 185
59. Rak J. W., Hegmann E. J., Lu C., Kerbel R. S. Progressive loss of sensitivity to endothelium-derived growth inhibitors expressed by human melanoma cells during disease progression. J Cell Physiol: 1994; 159 2 245 255
60. Hendrix M. J., Seftor E. A., Hess A. R., Seftor R. E. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat Rev Cancer: 2003; 3 6 411 421
61. 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
62. Wang R., Chadalavada K., Wilshire J., et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature: 2010; 468 7325 829 833
63. 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
64. Cheng L., Huang Z., Zhou W., et al. Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell: 2013; 153 1 139 152
65. Rodriguez F. J., Orr B. A., Ligon K. L., Eberhart C. G. Neoplastic cells are a rare component in human glioblastoma microvasculature. Oncotarget: 2012; 3 1 98 106
66. Zhang J., Jiang R., Liu L., Watkins T., Zhang F., Dong J. F. Traumatic brain injury-associated coagulopathy. J Neurotrauma: 2012; 29 17 2597 2605
67. Rogers L. R. Cerebrovascular complications in patients with cancer. Semin Neurol: 2010; 30 3 311 319
68. Prayson N. F., Koch P., Angelov L., Prayson R. A. Microscopic thrombi in anaplastic astrocytoma predict worse survival? Ann Diagn Pathol: 2011; 15 6 389 393
69. 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
70. Wun T., White R. H. Venous thromboembolism (VTE) in patients with cancer: epidemiology and risk factors. Cancer Invest: 2009; 27 01 63 74
71. Alvarado G., Noor R., Bassett R., et al. Risk of intracranial hemorrhage with anticoagulation therapy in melanoma patients with brain metastases. Melanoma Res: 2012; 22 4 310 315
72. Ilhan A., Gartner W., Neziri D., et al. Angiogenic factors in plasma of brain tumour patients. Anticancer Res: 2009; 29 2 731 736
73. Gridley D. S., Loredo L. N., Slater J. D., et al. Pilot evaluation of cytokine levels in patients undergoing radiotherapy for brain tumor. Cancer Detect Prev: 1998; 22 1 20 29
74. 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
75. Wang J. G., Geddings J. E., Aleman M. M., et al. Tumor-derived tissue factor activates coagulation and enhances thrombosis in a mouse xenograft model of human pancreatic cancer. Blood: 2012; 119 23 5543 5552
76. Gerlach R., Scheuer T., Böhm M., et al. Increased levels of plasma tissue factor pathway inhibitor in patients with glioblastoma and intracerebral metastases. Neurol Res: 2003; 25 4 335 338
77. Thaler J., Preusser M., Ay C., et al. Intratumoral tissue factor expression and risk of venous thromboembolism in brain tumor patients. Thromb Res: 2013; 131 2 162 165
78. Ay C., Vormittag R., Dunkler D., 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: 2009; 27 25 4124 4129
79. Hoke M., Dieckmann K., Koppensteiner R., Schillinger M., Marosi C., Mlekusch W. Prognostic value of plasma d-dimer levels in patients with glioblastoma multiforme - Results from a pilot study. Wien Klin Wochenschr: 2011; 123 7-8 199 203
80. Ay C., Dunkler D., Pirker R., et al. High D-dimer levels are associated with poor prognosis in cancer patients. Haematologica: 2012; 97 8 1158 1164
81. Sciacca F. L., Ciusani E., Silvani A., et al. Genetic and plasma markers of venous thromboembolism in patients with high grade glioma. Clin Cancer Res: 2004; 10 4 1312 1317
82. 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
83. Davila M., Amirkhosravi A., Coll E., et al. Tissue factor-bearing microparticles derived from tumor cells: impact on coagulation activation. J Thromb Haemost: 2008; 6 9 1517 1524
84. van der Pol E., Hoekstra A. G., Sturk A., Otto C., van Leeuwen T. G., Nieuwland R. Optical and non-optical methods for detection and characterization of microparticles and exosomes. J Thromb Haemost: 2010; 8 12 2596 2607
85. 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
86. Mackman N. Triggers, targets and treatments for thrombosis. Nature: 2008; 451 7181 914 918
87. Ruf W., Disse J., Carneiro-Lobo T. C., Yokota N., Schaffner F. Tissue factor and cell signalling in cancer progression and thrombosis. J Thromb Haemost: 2011; 9 01 306 315
88. Rickles F. R., Falanga A. Activation of clotting factors in cancer. Cancer Treat Res: 2009; 148 31 41
89. Loynes J. T., Zacharski L. R. The coagulation system as a target for experimental therapy of human gliomas. Expert Opin Ther Targets: 2003; 7 3 399 404
90. Brandsma D., Stalpers L., Taal W., Sminia P., van den Bent M. J. Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol: 2008; 9 5 453 461
91. Feldkamp M. M., Lau N., Rak J., Kerbel R. S., Guha A. Normoxic and hypoxic regulation of vascular endothelial growth factor (VEGF) by astrocytoma cells is mediated by Ras. Int J Cancer: 1999; 81 1 118 124
92. 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
93. Blouw B., Song H., Tihan T., et al. The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell: 2003; 4 2 133 146
94. Dvorak F. H., Rickles F. R. Malignancy and hemostasis. In: Coleman R. B., Marder V. J., Clowes A. W., George J. N., Goldhaber S. Z., eds. Hemostasis and Thrombosis: Basic Principles and Clinical Practice. Philadelphia, PA Lippincott Williams & Wilkins: 2006; 851 873
95. Bárdos H., Molnár P., Csécsei G., Adány R. Fibrin deposition in primary and metastatic human brain tumours. Blood Coagul Fibrinolysis: 1996; 7 5 536 548
96. Shoji M., Hancock W. W., Abe K., 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: 1998; 152 2 399 411
97. 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
98. 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
99. Guan M., Su B., Lu Y. Quantitative reverse transcription-PCR measurement of tissue factor mRNA in glioma. Mol Biotechnol: 2002; 20 2 123 129
100. 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
101. 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. Nat Med: 1996; 2 2 209 215
102. Mechtcheriakova D., Schabbauer G., Lucerna M., Clauss M., Binder B. R., Hofer E.; De Martin R. Specificity, diversity, and convergence in VEGF and TNF-alpha signaling events leading to tissue factor up-regulation via EGR-1 in endothelial cells. FASEB J: 2001; 15 1 230 242
103. Bombeli T., Karsan A., Tait J. F., Harlan J. M. Apoptotic vascular endothelial cells become procoagulant. Blood: 1997; 89 7 2429 2442
104. Milsom C., Yu J., May L., et al. The role of tumor-and host-related tissue factor pools in oncogene-driven tumor progression. Thromb Res: 2007; 120 02 S82 S91
105. 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
106. van den Berg Y. W., Osanto S., Reitsma P. H., Versteeg H. H. The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood: 2012; 119 4 924 932
107. Rak J. Microparticles in cancer. Semin Thromb Hemost: 2010; 36 8 888 906
108. Falanga A., Gordon S. G. Isolation and characterization of cancer procoagulant: a cysteine proteinase from malignant tissue. Biochemistry: 1985; 24 20 5558 5567
109. Bouffet E., Tabori U., Huang A., Bartels U. Possibilities of new therapeutic strategies in brain tumors. Cancer Treat Rev: 2010; 36 4 335 341
110. Salmaggi A., Simonetti G., Trevisan E., et al. Perioperative thromboprophylaxis in patients with craniotomy for brain tumours: a systematic review. J Neurooncol: 2013; 113 2 293 303
111. Reardon D. A., Turner S., Peters K. B., et al. A review of VEGF/VEGFR-targeted therapeutics for recurrent glioblastoma. J Natl Compr Canc Netw: 2011; 9 4 414 427
112. Soffietti R., Trevisan E., Rudà R. Targeted therapy in brain metastasis. Curr Opin Oncol: 2012; 24 6 679 686
113. Vargo J. A., Snelling B. M., Ghareeb E. R., et al. Dural venous sinus thrombosis in anaplastic astrocytoma following concurrent temozolomide and focal brain radiotherapy plus bevacizumab. J Neurooncol: 2011; 104 2 595 598
114. Bergers G. Proinvasive growth of glioma during VEGF inhibition [abstract]. Presented at: The 12th International Symposium on Anti-Angiogenic Agents (Angio 2010); February 4-6, 2010; San Diego, CA
115. Ebos J. M., Lee C. R., Cruz-Munoz W., Bjarnason G. A., Christensen J. G., Kerbel R. S. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell: 2009; 15 3 232 239
116. Pàez-Ribes M., Allen E., Hudock J., et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell: 2009; 15 3 220 231
117. 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
118. Vogelstein B., Kinzler K. W. Cancer genes and the pathways they control. Nat Med: 2004; 10 8 789 799
119. 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
120. Croce C. M. Oncogenes and cancer. N Engl J Med: 2008; 358 5 502 511
121. Spyropoulou A., Piperi C., Adamopoulos C., Papavassiliou A. G. Deregulated chromatin remodeling in the pathobiology of brain tumors. Neuromolecular Med: 2013; 15 1 1 24
122. 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
123. Mazure N. M., Chen E. Y., Laderoute K. R., Giaccia A. J. Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood: 1997; 90 9 3322 3331
124. 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
125. Kohli M., Williams K., Yao J. L., et al. Thrombin expression in prostate: a novel finding. Cancer Invest: 2011; 29 1 62 67
126. 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
127. Meehan B., Dombrovsky A., Lau K., et al. Impact of host ageing on the metastatic phenotype. Mech Ageing Dev: 2013; 134 3-4 118 129
128. 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
129. 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
130. 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
131. 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
132. 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
133. 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
134. 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
135. 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
136. 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
137. D'Asti E., Garnier D., Lee T. H., et al. Oncogenic extracellular vesicles in brain tumor progression. Front Physiol: 2012; 3 294 1 15
138. Walter J., Handel L. L., Brodhun M., et al. Expression of coagulation factors and their receptors in tumor tissue and coagulation factor upregulation in peripheral blood of patients with cerebral carcinoma metastases. J Cancer Res Clin Oncol: 2012; 138 1 141 151
139. Lee A. Y., Levine M. N. Venous thromboembolism and cancer: risks and outcomes. Circulation: 2003; 107 23 01 I17 I21
140. Northcott P. A., Korshunov A., Witt H., et al. Medulloblastoma comprises four distinct molecular variants. J Clin Oncol: 2011; 29 11 1408 1414
141. Loof T. G., Schmidt O., Herwald H., Theopold U. Coagulation systems of invertebrates and vertebrates and their roles in innate immunity: the same side of two coins? J Innate Immun: 2011; 3 1 34 40
142. Ruf W. Redundant signaling of tissue factor and thrombin in cancer progression? J Thromb Haemost: 2007; 5 8 1584 1587
143. 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 U S A: 1995; 92 18 8205 8209
144. 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
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. Camerer E., Gjernes E., Wiiger M., Pringle S., Prydz H. Binding of factor VIIa to tissue factor on keratinocytes induces gene expression. J Biol Chem: 2000; 275 9 6580 6585
147. Sapet C., Simoncini S., Loriod B., et al. Thrombin-induced endothelial microparticle generation: identification of a novel pathway involving ROCK-II activation by caspase-2. Blood: 2006; 108 6 1868 1876
148. Schaffner F., Ruf W. Tissue factor and protease-activated receptor signaling in cancer. Semin Thromb Hemost: 2008; 34 2 147 153
149. Versteeg H. H., Schaffner F., Kerver M., et al. Inhibition of tissue factor signaling suppresses tumor growth. Blood: 2008; 111 1 190 199
150. 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
151. Prydz H., Camerer E., Rottingen J. A., Wiiger M. T., Gjernes E. Cellular consequences of the initiation of blood coagulation. Thromb Haemost: 1999; 82 2 183 192
152. McEachron T. A., Pawlinski R., Richards K. L., Church F. C., Mackman N. Protease-activated receptors mediate crosstalk between coagulation and fibrinolysis. Blood: 2010; 116 23 5037 5044
153. Bezuhly M., Cullen R., Esmon C. T., et al. Role of activated protein C and its receptor in inhibition of tumor metastasis. Blood: 2009; 113 14 3371 3374
154. Burstyn-Cohen T., Lew E. D., Través P. G., Burrola P. G., Hash J. C., Lemke G. Genetic dissection of TAM receptor-ligand interaction in retinal pigment epithelial cell phagocytosis. Neuron: 2012; 76 6 1123 1132
155. Smith H. W., Marshall C. J. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol: 2010; 11 1 23 36
156. Gessler F., Voss V., Dützmann S., Seifert V., Gerlach R., Kögel D. Inhibition of tissue factor/protease-activated receptor-2 signaling limits proliferation, migration and invasion of malignant glioma cells. Neuroscience: 2010; 165 04 1312 1322
157. Palumbo J. S., Degen J. L. Mechanisms linking tumor cell-associated procoagulant function to tumor metastasis. Thromb Res: 2007; 120 02 S22 S28
158. Amirkhosravi A., Meyer T., Chang J. Y., et al. Tissue factor pathway inhibitor reduces experimental lung metastasis of B16 melanoma. Thromb Haemost: 2002; 87 6 930 936
159. 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 U S A: 1992; 89 24 11832 11836
160. Degen J. L., Palumbo J. S. Hemostatic factors, innate immunity and malignancy. Thromb Res: 2012; 129 01 S1 S5
161. 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
162. Labelle M., Begum S., Hynes R. O. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell: 2011; 20 5 576 590
163. Kaplan R. N., Riba R. D., Zacharoulis S., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature: 2005; 438 7069 820 827
164. 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
165. Kirstein J. M., Graham K. C., Mackenzie L. T., et al. Effect of anti-fibrinolytic therapy on experimental melanoma metastasis. Clin Exp Metastasis: 2009; 26 2 121 131
166. 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 U S A: 1997; 94 13 6922 6926
167. 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
168. Hembrough T. A., Swartz G. M., Papathanassiu A., et al. Tissue factor/factor VIIa inhibitors block angiogenesis and tumor growth through a nonhemostatic mechanism. Cancer Res: 2003; 63 11 2997 3000
169. 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
170. 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
171. Carneiro-Lobo T. C., Konig S., Machado D. E., et al. Ixolaris, a tissue factor inhibitor, blocks primary tumor growth and angiogenesis in a glioblastoma model. J Thromb Haemost: 2009; 7 11 1855 1864
172. 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
173. Garnier D., Bentley V., Magnus N., et al. Brain tumor initiating cells express functional coagulation factor receptors and respond to their agonists. Paper presented at: Montreal International Symposium on Angiogenesis and Metastasis; Montreal, QC; June 12, 2013
174. 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
175. 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
176. Goss P. E., Chambers A. F. Does tumour dormancy offer a therapeutic target? Nat Rev Cancer: 2010; 10 12 871 877
177. 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
178. Aguirre-Ghiso J. A. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer: 2007; 7 11 834 846
179. Naumov G. N., Folkman J., Straume O., Akslen L. A. Tumor-vascular interactions and tumor dormancy. APMIS: 2008; 116 7-8 569 585
180. Chittiboina P., Connor D. E. Jr, Caldito G., Quillin J. W., Wilson J. D., Nanda A. Occult tumors presenting with negative imaging: analysis of the literature. J Neurosurg: 2012; 116 6 1195 1203
181. Johnston A. L., Lun X., Rahn J. J., et al. The p75 neurotrophin receptor is a central regulator of glioma invasion. PLoS Biol: 2007; 5 8 e212
182. Karpatkin S. Does hypercoagulability awaken dormant tumor cells in the host? J Thromb Haemost: 2004; 2 12 2103 2106
183. Walter N. D., Rice P. L., Redente E. F., et al. Wound healing after trauma may predispose to lung cancer metastasis: review of potential mechanisms. Am J Respir Cell Mol Biol: 2011; 44 5 591 596
184. Hochberg F., Toniolo P., Cole P. Head trauma and seizures as risk factors of glioblastoma. Neurology: 1984; 34 11 1511 1514
185. Anderson J. A., Weitz J. I. Hypercoagulable states. Crit Care Clin: 2011; 27 4 933 952, vii
186. Kasthuri R. S., Taubman M. B., Mackman N. Role of tissue factor in cancer. J Clin Oncol: 2009; 27 29 4834 4838
187. Falanga A. Thrombophilia in cancer. Semin Thromb Hemost: 2005; 31 1 104 110
188. Mackman N. Tissue-specific hemostasis in mice. Arterioscler Thromb Vasc Biol: 2005; 25 11 2273 2281