Cancer cell-derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo

Journal of Experimental Medicine

Volumn 206, Issue 9, 2009, Pages 1913-1927

  Thomas, Grace M ^a,b   Panicot Dubois, Laurence ^a,b   Lacroix, Romaric ^a   Dignat George, Françoise ^a   Lombardo, Dominique ^a,b   Dubois, Christophe ^a,b  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; P SELECTIN ANTIBODY; P SELECTIN GLYCOPROTEIN LIGAND 1; THROMBOPLASTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOLE; ARTICLE; BLEEDING TIME; BLOOD; BLOOD VESSEL OCCLUSION; CANCER CELL; CONTROLLED STUDY; DRUG TARGETING; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG CANCER; METASTASIS; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; TAIL; THROMBOCYTE; THROMBOCYTE AGGREGATION; THROMBOGENESIS; THROMBOSIS; THROMBOSIS PREVENTION; VENULE;

EID: 69549103137     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20082297     Document Type: Article

References (54)

1. Abid Hussein, M.N., E.W. Meesters, N. Osmanovic, F.P. Romijn, R. Nieuwland, and A. Sturk. 2003. Antigenic characterization of endothelial cell-derived microparticles and their detection ex vivo. J. Thromb. Haemost. 1:2434-2443.
2. Berckmans, R.J., R. Neiuwland, A.N. Böing, F.P. Romijn, C.E. Hack, and A. Sturk. 2001. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb. Haemost. 85:639-646.
3. Bertram, J.S., and P. Janik. 1980. Establishment of a cloned line of Lewis Lung Carcinoma cells adapted to cell culture. Cancer Lett. 11:63-73.
4. Blom, J.W., S. Osanto, and F.R. Rosendaal. 2006a. High risk of venous thrombosis in patients with pancreatic cancer: a cohort study of 202 patients. Eur. J. Cancer. 42:410-414.
5. Blom, J.W., J.P. Vanderschoot, M.J. Oostindiër, S. Osanto, F.J. van der Meer, and F.R. Rosendaal. 2006b. Incidence of venous thrombosis in a large cohort of 66,329 cancer patients: results of a record linkage study. J. Thromb. Haemost. 4:529-535.
6. Chamouard, P., D. Desprez, B. Hugel, C. Kunzelmann, C. Gidon-Jeangirard, M. Lessard, R. Baumann, J.M. Freyssinet, and L. Grunebaum. 2005. Circulating cell-derived microparticles in Crohn's disease. Dig. Dis. Sci. 50:574-580. (Pubitemid 40543751)
7. Combes, V., A.C. Simon, G.E. Grau, D. Arnoux, L. Camoin, F. Sabatier, M. Mutin, M. Sanmarco, J. Sampol, and F. Dignat-George. 1999. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J. Clin. Invest. 104:93-102. (Pubitemid 29534349)
8. Corbett, T.H., B.J. Roberts, W.R. Leopold, J.C. Peckham, L.J. Wilkoff, D.P. Griswold Jr., and F.M. Schabel Jr. 1984. Induction and chemotherapeutic response of two transplantable ductal adenocarcinomas of the pancreas in C57BL/6 mice. Cancer Res. 44:717-726.
9. Davila, M., A. Amirkhosravi, E. Coll, H. Desai, L. Robles, J. Colon, C.H. Baker, and J.L. Francis. 2008. Tissue factor-bearing microparticles derived from tumor cells: impact on coagulation activation. J. Thromb. Haemost. 6:1517-1524.
10. Del Conde, I., L.D. Bharwani, D.J. Dietzen, U. Pendurthi, P. Thiagarajan, and J.A. López. 2007. Microvesicle-associated tissue factor and Trousseau's syndrome. J. Thromb. Haemost. 5:70-74. (Pubitemid 44921069)
11. Dignat-George, F. 2006. Detection of circulating endothelial cells and endothelial progenitor cells by flow cytometry. Cytometry B Clin. Cytom. 70:104-105.
12. Dubois, C., B. Steiner, and S.C. Meyer Reigner. 2004. Contribution of PAR-1, PAR-4 and GPIbalpha in intracellular signaling leading to the cleavage of the beta3 cytoplasmic domain during thrombin-induced platelet aggregation. Thromb. Haemost. 91:733-742. (Pubitemid 38477454)
13. Dubois, C., B. Atkinson, B.C. Furie, and B. Furie. 2006a. Real time in vivo imaging of platelets during thrombus formation. In Platelets. A.D. Michelson, editor. Elsevier/Academic Press, Worcester, MA. 611-628.
14. Dubois, C., L. Panicot-Dubois, G. Merrill-Skoloff, B. Furie, and B.C. Furie. 2006b. Glycoprotein VI-dependent and -independent pathways of thrombus formation in vivo. Blood. 107:3902-3906. (Pubitemid 43726794)
15. Dubois, C., L. Panicot-Dubois, J.F. Gainor, B.C. Furie, and B. Furie. 2007. Thrombin-initiated platelet activation in vivo is vWF independent during thrombus formation in a laser injury model. J. Clin. Invest. 117:953-960. (Pubitemid 46556751)
16. Dvorak, H.F., S.C. Quay, N.S. Orenstein, A.M. Dvorak, P. Hahn, A.M. Bitzer, and A.C. Carvalho. 1981. Tumor shedding and coagulation. Science. 212:923-924.
17. Falati, S., Q. Liu, P. Gross, G. Merrill-Skoloff, J. Chou, E. Vandendries, A. Celi, K. Croce, B.C. Furie, and B. Furie. 2003. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J. Exp. Med. 197:1585-1598. (Pubitemid 36682554)
18. Fujii, Y., M. Sekiguchi, Y. Shiroko, H. Shimizu, I. Sugawara, K. Hasumi, M. Eriguchi, T. Ikeuchi, and H. Uchida. 1990. Establishment and characterization of human pancreatic adenocarcinoma cell line SOJ producing carcinoembryonic antigen and carbohydrate antigen 19-9. Hum. Cell. 3:31-36.
19. Furie, B., and B.C. Furie. 2006. Cancer-associated thrombosis. Blood Cells Mol. Dis. 36:177-181.
20. Gasic, G.J., P.A. Koch, B. Hsu, T.B. Gasic, and S. Niewiarowski. 1976. Thrombogenic activity of mouse and human tumors: effects on platelets, coagulation, and fibrinolysis, and possible significance for metastases. Z. Krebsforsch. Klin. Onkol. Cancer Res. Clin. Oncol. 86:263-277.
21. Ghosh, A., W. Li, M. Febbraio, R.G. Espinola, K.R. McCrae, E. Cockrell, and R.L. Silverstein. 2008. Platelet CD36 mediates interactions with endothelial cell-derived microparticles and contributes to thrombosis in mice. J. Clin. Invest. 118:1934-1943. (Pubitemid 351632395)
22. Haas, S.L., R. Jesnowski, M. Steiner, F. Hummel, J. Ringel, C. Burstein, H. Nizze, S. Liebe, and J.M. Löhr. 2006. Expression of tissue factor in pancreatic adenocarcinoma is associated with activation of coagulation. World J. Gastroenterol. 12:4843-4849. (Pubitemid 44323209)
23. Hron, G., M. Kollars, H. Weber, V. Sagaster, P. Quehenberger, S. Eichinger, P.A. Kyrle, and A. Weltermann. 2007. Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer. Thromb. Haemost. 97:119-123. (Pubitemid 46242392)
24. Kakkar, A.K., and R.C. Williamson. 1999. Prevention of venous thromboembolism in cancer patients. Semin. Thromb. Hemost. 25:239-243. (Pubitemid 29227152)
25. Kaplan, R.N., S. Rafii, and D. Lyden. 2006. Preparing the "soil": the pre-metastatic niche. Cancer Res. 66:11089-11093.
26. Khorana, A.A., S.A. Ahrendt, C.K. Ryan, C.W. Francis, R.H. Hruban, Y.C. Hu, G. Hostetter, J. Harvey, and M.B. Taubman. 2007. Tissue factor expression, angiogenesis, and thrombosis in pancreatic cancer. Clin. Cancer Res. 13:2870-2875. (Pubitemid 46849560)
27. Kim, H.K., K.S. Song, Y.S. Park, Y.H. Kang, Y.J. Lee, K.R. Lee, H.K. Kim, K.W. Ryu, J.M. Bae, and S. Kim. 2003. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur. J. Cancer. 39:184-191.
28. Lacroix, R., F. Sabatier, A. Mialhe, A. Basire, R. Pannell, H. Borghi, S. Robert, E. Lamy, L. Plawinski, L. Camoin-Jau, et al. 2007. Activation of plasminogen into plasmin at the surface of endothelial microparticles: a mechanism that modulates angiogenic properties of endothelial progenitor cells in vitro. Blood. 110:2432-2439. (Pubitemid 47523164)
29. Langer, F., B. Spath, K. Haubold, K. Holstein, G. Marx, J. Wierecky, T.H. Brümmendorf, J. Dierlamm, C. Bokemeyer, and B. Eifrig. 2008. Tissue factor procoagulant activity of plasma microparticles in patients with cancer-associated disseminated intravascular coagulation. Ann. Hematol. 87:451-457.
30. Milsom, C., J. Yu, L. May, B. Meehan, N. Magnus, K. Al-Nedawi, J. Luyendyk, J. Weitz, P. Klement, G. Broze, et al. 2007. The role of tumor-and host-related tissue factor pools in oncogene-driven tumor progression. Thromb. Res. 120(Suppl. 2):S82-S91. (Pubitemid 350101776)
31. Müller, I., A. Klocke, M. Alex, M. Kotzsch, T. Luther, E. Morgenstern, S. Zieseniss, S. Zahler, K. Preissner, and B. Engelmann. 2003. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J. 17:476-478.
32. Myers, D.D., A.E. Hawley, D.M. Farris, S.K. Wrobleski, P. Thanaporn, R.G. Schaub, D.D. Wagner, A. Kumar, and T.W. Wakefield. 2003. P-selectin and leukocyte microparticles are associated with venous thrombogenesis. J. Vasc. Surg. 38:1075-1089.
33. Neoptolemos, J.P., D.D. Stocken, J.A. Dunn, J. Almond, H.G. Beger, P. Pederzoli, C. Bassi, C. Dervenis, L. Fernandez-Cruz, F. Lacaine, et al; European Study Group for Pancreatic Cancer. 2001. Influence of resection margins on survival for patients with pancreatic cancer treated by adjuvant chemoradiation and/or chemotherapy in the ESPAC-1 randomized controlled trial. Ann. Surg. 234:758-768.
34. Ni, H., P.S. Yuen, J.M. Papalia, J.E. Trevithick, T. Sakai, R. Fässler, R.O. Hynes, and D.D. Wagner. 2003. Plasma fibronectin promotes thrombus growth and stability in injured arterioles. Proc. Natl. Acad. Sci. USA. 100:2415-2419.
35. Panicot-Dubois, L., M. Aubert, C. Franceschi, E. Mas, F. Silvy, C. Crotte, J.P. Bernard, D. Lombardo, and M.O. Sadoulet. 2004. Monoclonal antibody 16D10 to the C-terminal domain of the feto-acinar pancreatic protein binds to membrane of human pancreatic tumoral SOJ-6 cells and inhibits the growth of tumor xenografts. Neoplasia. 6:713-724. (Pubitemid 40041489)
36. Panicot-Dubois, L., G.M. Thomas, B.C. Furie, B. Furie, D. Lombardo, and C. Dubois. 2007. Bile salt-dependent lipase interacts with platelet CXCR4 and modulates thrombus formation in mice and humans. J. Clin. Invest. 117:3708-3719. (Pubitemid 350224082)
37. Pawlinski, R., and N. Mackman. 2008. Use of mouse models to study the role of tissue factor in tumor biology. Semin. Thromb. Hemost. 34:182-186.
38. Piccin, A., W.G. Murphy, and O.P. Smith. 2007. Circulating microparticles: pathophysiology and clinical implications. Blood Rev. 21:157-171. (Pubitemid 46529055)
39. Prandoni, P., A.W. Lensing, H.R. Büller, A. Cogo, M.H. Prins, A.M. Cattelan, S. Cuppini, F. Noventa, and J.W. ten Cate. 1992. Deep-vein thrombosis and the incidence of subsequent symptomatic cancer. N. Engl. J. Med. 327:1128-1133.
40. Riewald, M., and W. Ruf. 2001. Mechanistic coupling of protease signaling and initiation of coagulation by tissue factor. Proc. Natl. Acad. Sci. USA. 98:7742-7747. (Pubitemid 32642631)
41. Robert, S., P. Poncelet, R. Lacroix, L. Arnaud, L. Giraudo, A. Hauchard, J. Sampol, and F. Dignat-George. 2009. Standardization of platelet-derived microparticle counting using calibrated beads and a Cytomics FC500 routine flow cytometer: a first step towards multicenter studies? J. Thromb. Haemost. 7:190-197.
42. Sabatier, F., P. Darmon, B. Hugel, V. Combes, M. Sanmarco, J.G. Velut, D. Arnoux, P. Charpiot, J.M. Freyssinet, C. Oliver, et al. 2002. Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes. 51:2840-2845. (Pubitemid 34970939)
43. Sack, G.H., Jr., J. Levin, and W.R. Bell. 1977. Trousseau's syndrome and other manifestations of chronic disseminated coagulopathy in patients with neoplasms: clinical, pathophysiologic, and therapeutic features. Medicine (Baltimore). 56:1-37.
44. Schiavetti, A., M. Foco, A. Ingrosso, E. Bonci, L. Conti, and M. Matrunola. 2008. Venous thrombosis in children with solid tumors. J. Pediatr. Hematol. Oncol. 30:148-152.
45. Sierko, E., and M.Z. Wojtukiewicz. 2007. Inhibition of platelet function: does it offer a chance of better cancer progression control? Semin. Thromb. Hemost. 33:712-721. (Pubitemid 350157017)
46. Stein, P.D., A. Beemath, F.A. Meyers, E. Skaf, J. Sanchez, and R.E. Olson. 2006. Incidence of venous thromboembolism in patients hospitalized with cancer. Am. J. Med. 119:60-68. (Pubitemid 43117468)
47. Tesselaar, M.E., F.P. Romijn, I.K. Van Der Linden, F.A. Prins, R.M. Bertina, and S. Osanto. 2007. Microparticle-associated tissue factor activity: a link between cancer and thrombosis? J. Thromb. Haemost. 5:520-527. (Pubitemid 46680685)
48. Tilley, R.E., T. Holscher, R. Belani, J. Nieva, and N. Mackman. 2008. Tissue factor activity is increased in a combined platelet and microparticle sample from cancer patients. Thromb. Res. 122:604-609.
49. Trousseau, A. 1865. Phlegmasia alba dolens. In Clinique Médicale de l'Hôtel-Dieu. J.-B. Baillière, Paris. 654-712.
50. Vandendries, E.R., J.R. Hamilton, S.R. Coughlin, B. Furie, and B.C. Furie. 2007. Par4 is required for platelet thrombus propagation but not fibrin generation in a mouse model of thrombosis. Proc. Natl. Acad. Sci. USA. 104:288-292.
51. Versteeg, H.H., F. Schaffner, M. Kerver, H.H. Petersen, J. Ahamed, B. Felding-Habermann, Y. Takada, B.M. Mueller, and W. Ruf. 2008. Inhibition of tissue factor signaling suppresses tumor growth. Blood. 111:190-199.
52. Willekens, F.L., J.M. Werre, J.K. Kruijt, B. Roerdinkholder-Stoelwinder, Y.A. Groenen-Döpp, A.G. van den Bos, G.J. Bosman, and T.J. van Berkel. 2005. Liver Kupffer cells rapidly remove red blood cell-derived vesicles from the circulation by scavenger receptors. Blood. 105:2141-2145.
53. Yu, J.L., L. May, V. Lhotak, S. Shahrzad, S. Shirasawa, J.I. Weitz, B.L. Coomber, N. Mackman, and J.W. Rak. 2005. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood. 105:1734-1741.
54. Zwicker, J.I., B.C. Furie, and B. Furie. 2007. Cancer-associated thrombosis. Crit. Rev. Oncol. Hematol. 62:126-136.