Best Practice & Research Clinical Haematology
Volume 22, Issue 1 , Pages 49-60 , March 2009

Procoagulant mechanisms in tumour cells

  • Anna Falanga, MD (Director of Haemostasis and Thrombosis Centre)

      Affiliations

    • Haemostasis and Thrombosis Centre, Department of Haematology-Oncology, Ospedali Riuniti Bergamo, Largo Barozzi n. 1, Bergamo 24128, Italy
    • Corresponding Author InformationCorresponding author. Tel.: +39 035 269 491; Fax: +39 035 266 659.
  • ,
  • Marina Panova-Noeva, MD (Post-Doctoral Fellow)

      Affiliations

    • Haemostasis and Thrombosis Centre, Department of Haematology-Oncology, Ospedali Riuniti Bergamo, Largo Barozzi n. 1, Bergamo 24128, Italy
    • Maastricht University Medical Centre, Department of Internal Medicine and Cardiovascular Research Institute, Maastricht, the Netherlands
  • ,
  • Laura Russo, BSc (Research Fellow)

      Affiliations

    • Haemostasis and Thrombosis Centre, Department of Haematology-Oncology, Ospedali Riuniti Bergamo, Largo Barozzi n. 1, Bergamo 24128, Italy

References 

  1. Rickles FR, Falanga A. Molecular basis for the relationship between thrombosis and cancer. Thromb Res. 2001;102:V215–V224
  2. Lee AY. Cancer and thromboembolic disease: pathogenic mechanisms. Cancer Treat Rev. 2002;28:137–140
  3. Rickles FR, Patierno S, Fernandez PM. Tissue factor, thrombin, and cancer. Chest. 2003;124:58S–68S
  4. Heit JA, Silverstein MD, Mohr DN, et al. Risk factors for deep vein thrombosis and pulmonary embolism: a population-based case–control study. Arch Intern Med. 2000;160:809–815
  5. Khorana AA, Kuderer NM, Culakova E, et al. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood. 2008;111:4902–4907
  6. Ay C, Simanek R, Vormittag R, et al. High plasma levels of soluble P-selectin are predictive of venous thromboembolism in cancer patients – results from the Vienna Cancer and Thrombosis Study (CATS). Blood. 2008;112(7):2703–2708
  7. 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;35:702–711
  8. Falanga A, Rickles FR. Pathogenesis and management of the bleeding diathesis in acute promyelocytic leukaemia. Best Pract Res Clin Haematol. 2003;16:463–482
  9. Furie B, Furie BC. Mechanisms of thrombus formation. N Engl J Med. 2008;359:938–949
  10. Rak J, Milsom C, May L, et al. Tissue factor in cancer and angiogenesis: the molecular link between genetic tumor progression, tumor neovascularization, and cancer coagulopathy. Semin Thromb Hemost. 2006;32:54–70
  11. Falanga A, Gordon SG. Isolation and characterization of cancer procoagulant: a cysteine proteinase from malignant tissue. Biochemistry. 1985;24:5558–5567
  12. Donati MB, Gambacorti-Passerini C, Casali B, et al. Cancer procoagulant in human tumor cells: evidence from melanoma patients. Cancer Res. 1986;46:6471–6474
  13. Mielicki W, Serwa J, Kurzawinski T, et al. Procoagulant activity of human stomach and colon cancers. Oncology. 1990;47:299–302
  14. Falanga A, Consonni R, Marchetti M, et al. Cancer procoagulant and tissue factor are differently modulated by all-trans-retinoic acid in acute promyelocytic leukemia cells. Blood. 1998;92:143–151
  15. Falanga A, Toma S, Marchetti M, et al. Effect of all-trans-retinoic acid on the hypercoagulable state of patients with breast cancer. Am J Hematol. 2002;70:9–15
  16. Dvorak HF, Quay SC, Orenstein NS, et al. Tumor shedding and coagulation. Science. 1981;212:923–924
  17. Tesselaar ME, Romijn FP, Van Der Linden IK, et al. Microparticle-associated tissue factor activity: a link between cancer and thrombosis?. J Thromb Haemost. 2007;5:520–527
  18. Del Conde I, Bharwani LD, Dietzen DJ, et al. Microvesicle-associated tissue factor and Trousseau's syndrome. J Thromb Haemost. 2007;5:70–74
  19. Carr JM, Dvorak AM, Dvorak HF. Circulating membrane vesicles in leukemic blood. Cancer Res. 1985;45:5944–5951
  20. Hugel B, Martinez MC, Kunzelmann C, et al. Membrane microparticles: two sides of the coin. Physiology. 2005;20:22–27
  21. Hron G, Kollars M, Weber H, et al. Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer. Thromb Haemost. 2007;97:119–123
  22. Hajjar KA. Cellular receptors in the regulation of plasmin generation. Thromb Haemost. 1995;74:294–301
  23. Annecke K, Schmitt M, Euler U, et al. uPA and PAI-1 in breast cancer: review of their clinical utility and current validation in the prospective NNBC-3 trial. Adv Clin Chem. 2008;45:31–45
  24. McMahon GA, Petitclerc E, Stefansson S, et al. Plasminogen activator inhibitor-1 regulates tumor growth and angiogenesis. J Biol Chem. 2001;276:33964–33968
  25. van Hinsbergh VW, Bauer KA, Kooistra T, et al. Progress of fibrinolysis during tumor necrosis factor infusions in humans. Concomitant increase in tissue-type plasminogen activator, plasminogen activator inhibitor type-1, and fibrin(ogen) degradation products. Blood. 1990;76:2284–2289
  26. Van de Wouwer M, Collen D, Conway EM. Thrombomodulin-protein C-EPCR system: integrated to regulate coagulation and inflammation. Arterioscler Thromb Vasc Biol. 2004;24:1374–1383
  27. Rice GE, Bevilacqua MP. An inducible endothelial cell surface glycoprotein mediates melanoma adhesion. Science. 1989;246:1303–1306
  28. Giavazzi R, Foppolo M, Dossi R, et al. Rolling and adhesion of human tumor cells on vascular endothelium under physiological flow conditions. J Clin Invest. 1993;92:3038–3044
  29. Chen M, Geng JG. P-selectin mediates adhesion of leukocytes, platelets, and cancer cells in inflammation, thrombosis, and cancer growth and metastasis. Arch Immunol Ther Exp. 2006;54(2):75–84
  30. Karpatkin S, Pearlstein E, Ambrogio C, et al. Role of adhesive proteins in platelet tumor interaction in vitro and metastasis formation in vivo. J Clin Invest. 1988;81:1012–1019
  31. Biggerstaff JP, Seth N, Amirkhosravi A, et al. Soluble fibrin augments platelet/tumor cell adherence in vitro and in vivo, and enhances experimental metastasis. Clin Exp Metastasis. 1999;17:723–730
  32. Nierodzik ML, Karpatkin S. Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell. 2006;10:355–362
  33. Felding-Habermann B, O'Toole TE, Smith JW, et al. Integrin activation controls metastasis in human breast cancer. Proc Natl Acad Sci U S A. 2001;98:1853–1858
  34. Felding-Habermann B. Targeting tumor cell-platelet interaction in breast cancer metastasis. Pathophysiol Haemost Thromb. 2003;33(Suppl. 1):56–58
  35. Borsig L, Wong R, Feramisco J, et al. Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc Natl Acad Sci U S A. 2001;98:3352–3357
  36. Borsig L. Non-anticoagulant effects of heparin in carcinoma metastasis and Trousseau's syndrome. Pathophysiol Haemost Thromb. 2003;33(Suppl. 1):64–66
  37. Merten M, Beythien C, Gutensohn K, et al. Sulfatides activate platelets through P-selectin and enhance platelet and platelet-leukocyte aggregation. Arterioscler Thromb Vasc Biol. 2005;25:258–263
  38. Jain S, Zuka M, Liu J, et al. Platelet glycoprotein Ib alpha supports experimental lung metastasis. Proc Natl Acad Sci U S A. 2007;104:9024–9028
  39. Yano S, Nishioka Y, Goto H, et al. Molecular mechanisms of angiogenesis in non-small cell lung cancer, and therapeutics targeting related molecules. Cancer Sci. 2003;94:479–485
  40. Rickles FR. Mechanisms of cancer-induced thrombosis in cancer. Pathophysiol Haemost Thromb. 2006;35:103–110
  41. Uusitalo-Jarvinen H, Kurokawa T, Mueller BM, et al. Role of protease activated receptor 1 and 2 signaling in hypoxia-induced angiogenesis. Arterioscler Thromb Vasc Biol. 2007;27:1456–1462
  42. Ruf W. Tissue factor and PAR signaling in tumor progression. Thromb Res. 2007;120:S7–S12
  43. Palumbo JS, Kombrinck KW, Drew AF, et al. Fibrinogen is an important determinant of the metastatic potential of circulating tumor cells. Blood. 2000;96:3302–3309
  44. Pinedo HM, Verheul HM, D'Amato RJ, et al. Involvement of platelets in tumour angiogenesis?. Lancet. 1998;352:1775–1777
  45. English D, Garcia JG, Brindley DN. Platelet-released phospholipids link haemostasis and angiogenesis. Cardiovasc Res. 2001;49:588–599
  46. Palumbo JS, Talmage KE, Massari JV, 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;110:133–141
  47. Wojtukiewicz MZ, Tang DG, Ciarelli JJ, et al. Thrombin increases the metastatic potential of tumor cells. Int J Cancer. 1993;54:793–806
  48. Nierodzik ML, Plotkin A, Kajumo F, et al. Thrombin stimulates tumor-platelet adhesion in vitro and metastasis in vivo. J Clin Invest. 1991;87:229–236
  49. Nierodzik ML, Kajumo F, Karpatkin S. Effect of thrombin treatment of tumor cells on adhesion of tumor cells to platelets in vitro and tumor metastasis in vivo. Cancer Res. 1992;52:3267–3272
  50. Shi X, Gangadharan B, Brass LF, et al. Protease-activated receptors (PAR1 and PAR2) contribute to tumor cell motility and metastasis. Mol Cancer Res. 2004;2:395–402
  51. Even-Ram S, Uziely B, Cohen P, et al. Thrombin receptor overexpression in malignant and physiological invasion processes. Nat Med. 1998;4:909–914
  52. Boire A, Covic L, Agarwal A, et al. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell. 2005;120:303–313
  53. Palumbo JS, Talmage KE, Massari JV, et al. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood. 2005;105:178–185
  54. Aeed PA, Nakajima M, Welch DR. The role of polymorphonuclear leukocytes (PMN) on the growth and metastatic potential of 13762NF mammary adenocarcinoma cells. Int J Cancer. 1988;42:748–759
  55. Starkey JR, Liggitt HD, Jones W, et al. Influence of migratory blood cells on the attachment of tumor cells to vascular endothelium. Int J Cancer. 1984;34:535–543
  56. Welch DR, Schissel DJ, Howrey RP, et al. Tumor-elicited polymorphonuclear cells, in contrast to “normal” circulating polymorphonuclear cells, stimulate invasive and metastatic potentials of rat mammary adenocarcinoma cells. Proc Natl Acad Sci U S A. 1989;86:5859–5863
  57. Wu QD, Wang JH, Condron C, et al. Human neutrophils facilitate tumor cell transendothelial migration. Am J Physiol. 2001;280:C814–C822
  58. Borsig L. Selectins facilitate carcinoma metastasis and heparin can prevent them. News Physiol Sci. 2004;19:16–21
  59. Klink M, Jastrzembska K, Nowak M, et al. Ovarian cancer cells modulate human blood neutrophils response to activation in vitro. Scand J Immunol. 2008;68:328–336
  60. Zacharski LR, Henderson WG, Rickles FR, et al. Effect of warfarin anticoagulation on survival in carcinoma of the lung, colon, head and neck, and prostate. Final report of VA Cooperative Study #75. Cancer. 1984;53:2046–2052
  61. Kuderer NM, Khorana AA, Lyman GH, et al. A meta-analysis and systematic review of the efficacy and safety of anticoagulants as cancer treatment: impact on survival and bleeding complications. Cancer. 2007;110:1149–1161
  62. Lazo-Langner A, Goss GD, Spaans JN, et al. The effect of low-molecular-weight heparin on cancer survival. A systematic review and meta-analysis of randomized trials. J Thromb Haemost. 2007;5:729–737
  63. Falanga A, Piccioli A. Effect of anticoagulant drugs in cancer. Curr Opin Pulm Med. 2005;11:403–407
  64. Boccaccio C, Sabatino G, Medico E, et al. The MET oncogene drives a genetic programme linking cancer to haemostasis. Nature. 2005;434:396–400
  65. Rak J, Yu JL, Luyendyk J, et al. Oncogenes, trousseau syndrome, and cancer-related changes in the coagulome of mice and humans. Cancer Res. 2006;66:10643–10646
  66. Rong Y, Post DE, Pieper RO, et al. PTEN and hypoxia regulate tissue factor expression and plasma coagulation by glioblastoma. Cancer Res. 2005;65:1406–1413
  67. Falanga A, Rickles FR. Management of Thrombohemorrhagic Syndromes (THS) in Hematologic Malignancies. Hematology/the Education Program of the American Society of Hematology; 2007;p. 165–171
  68. Falanga A, Barbui T, Rickles F. Hypercoagulability and tissue factor gene upregulation in hematologic malignancies. Semin Thromb Hemost. 2008;34:204–210
  69. Maugeri N, Giordano G, Petrilli MP, et al. Inhibition of tissue factor expression by hydroxyurea in polymorphonuclear leukocytes from patients with myeloproliferative disorders: a new effect for an old drug?. J Thromb Haemost. 2006;4:2593–2598

PII: S1521-6926(08)00113-8

doi: 10.1016/j.beha.2008.12.009

Best Practice & Research Clinical Haematology
Volume 22, Issue 1 , Pages 49-60 , March 2009