Breast-cancer extracellular vesicles induce platelet activation and aggregation by tissue factor-independent and -dependent mechanisms

Thrombosis Research

Volumn 159, Issue , 2017, Pages 24-32

  Gomes, Fausto G ^a   Sandim, Vanessa ^a   Almeida, Vitor H ^a   Rondon, Araci M R ^a   Succar, Barbara B ^a   Hottz, Eugenio D ^b,d   Leal, Ana Carolina ^a   Verçoza, Brunno Renato F ^a,c   Rodrigues, Juliany Cola F ^a,c   Bozza, Patrícia T ^b   Zingali, Russolina B ^a   Monteiro, Robson Q ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c Instituto Nacional de Ciência E Tecnologia de Biologia Estrutural E Bioimagem   (Brazil)

^d FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

Author keywords

Cancer; Exosomes; Extracellular vesicles; Microvesicles; Platelets; Thrombosis

Indexed keywords

PADGEM PROTEIN; PLASMA PROTEIN; THROMBOPLASTIN;

ARTICLE; BLOOD CLOTTING; BLOOD CLOTTING TIME; BREAST CANCER; CELL INTERACTION; CELL ISOLATION; CELLULAR DISTRIBUTION; CONDITIONED MEDIUM; CONTROLLED STUDY; EXOSOME; HUMAN; HUMAN CELL; MCF-7 CELL LINE; MDA-MB-231 CELL LINE; MEMBRANE MICROPARTICLE; PLASMA; PRIORITY JOURNAL; PROTEIN FUNCTION; THROMBIN TIME; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOSIS; TUMOR THROMBUS; WESTERN BLOTTING; BREAST TUMOR; FEMALE; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; EXTRACELLULAR VESICLES; FEMALE; HUMANS; PLATELET ACTIVATION; PLATELET AGGREGATION; THROMBOPLASTIN; THROMBOSIS;

EID: 85029787430     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/j.thromres.2017.09.019     Document Type: Article

References (56)

1. Varki, A., Trousseau's syndrome: multiple definitions and multiple mechanisms. Blood 110 (2007), 1723–1729.
2. Donati, M.B., Thrombosis and cancer: trousseau syndrome revisited. Best Pract. Res. Clin. Haematol. 22 (2009), 3–8.
3. 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. 5 (2007), 246–254.
4. Timp, J.F., Braekkan, S.K., Versteeg, H.H., Cannegieter, S.C., Epidemiology of cancer-associated venous thrombosis. Blood 122 (2013), 1712–1723.
5. Hisada, Y., Geddings, J.E., Ay, C., Mackman, N., Venous thrombosis and cancer: from mouse models to clinical trials. J. Thromb. Haemost. 13 (2015), 1372–1382.
6. Levitan, N., Dowlati, A., Remick, S.C., Tahsildar, H.I., Sivinski, L.D., Beyth, R., Rimm, A.A., 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.
7. Hamada, K., Kuratsu, J., Saitoh, Y., Takeshima, H., Nishi, T., Ushio, Y., Expression of tissue factor correlates with grade of malignancy in human glioma. Cancer 77 (1996), 1877–1883.
8. Kaushal, V., Mukunyadzi, P., Siegel, E.R., Dennis, R.A., Johnson, D.E., Kohli, M., Expression of tissue factor in prostate cancer correlates with malignant phenotype. Appl. Immunohistochem. Mol. Morphol. 16 (2008), 1–6.
9. Rak, J., Milsom, C., Magnus, N., Yu, J., Tissue factor in tumour progression. Best Pract. Res. Clin. Haematol. 22 (2009), 71–83.
10. Kasthuri, R.S., Taubman, M.B., Mackman, N., Role of tissue factor in cancer. J. Clin. Oncol. 27 (2009), 4834–4838.
11. 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. 9 (2011), 306–315.
12. Lima, L.G., Monteiro, R.Q., Activation of blood coagulation in cancer: implications for tumour progression. Biosci. Rep. 33 (2013), 701–710, 10.1042/BSR20130057 (epub).
13. Jurasz, P., Sawicki, G., Duszyk, M., Sawicka, J., Miranda, C., Mayers, I., Radomski, M.W., Matrix metalloproteinase 2 in tumor cell-induced platelet aggregation: regulation by nitric oxide. Cancer Res. 61 (2001), 376–382.
14. Medina, C., Jurasz, P., Santos-Martinez, M.J., Jeong, S.S., Mitsky, T., Chen, R., Radomski, M.W., Platelet aggregation-induced by caco-2 cells: regulation by matrix metalloproteinase-2 and adenosine diphosphate. J. Pharmacol. Exp. Ther. 317 (2006), 739–745.
15. Mitrugno, A., Williams, D., Kerrigan, S.K., Moran, N., A novel and essential role for FcgRIIa in cancer cell–induced platelet activation. Blood 123 (2014), 249–260.
16. Vader, P., Breakefield, X.O., Wood, M.J., Extracellular vesicles: emerging targets for cancer therapy. Trends Mol. Med. 20 (2014), 385–393.
17. Muralidharan-Chari, V., Clancy, J.W., Sedgwick, A., D'Souza-Schorey, C., Microvesicles: mediators of extracellular communication during cancer progression. J. Cell Sci. 123 (2010), 1603–1611.
18. Minciacchi, V.R., Freemana, M.R., Vizio, D.D., Extracellular vesicles in cancer: exosomes. Microvesicles and the emerging role of large oncosomes. Semin. Cell Dev. Biol. 40 (2015), 41–51.
19. Urbanelli, L., Magini, A., Buratta, S., Brozzi, A., Sagini, K., Polchi, A., Tancini, B., Emiliani, C., Signaling pathways in exosomes biogenesis, secretion and fate. Genes (Basel) 28 (2013), 152–170.
20. Raposo, G., Stoorvogel, W., Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200 (2013), 373–383.
21. Aharon, A., Brenner, B., Microparticles, thrombosis and cancer. Best Pract. Res. Clin. Haematol. 22 (2009), 61–69.
22. Rautou, P., Mackman, N., Microvesicles as risk markers for venous thrombosis. Expert. Rev. Hematol. 6 (2013), 91–101.
23. Thomas, G.M., Panicot-Dubois, L., Lacroix, R., Dignat-George, F., Lombardo, D., Dubois, C., Cancer cell–derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo. J. Exp. Med. 206 (2009), 1913–1927.
24. Lima, L.G., Oliveira, A.S., Campos, L.C., Bonamino, M., Chammas, R., Werneck, C., Vicente, C.P., Barcinski, M.A., Petersen, L.C., Monteiro, R.Q., Malignant transformation in melanocytes is associated with increased production of procoagulant microvesicles. Thromb. Haemost. 106 (2011), 712–723.
25. Geddings, J.E., Hisada, Y., Boulaftali, Y., Getz, T.M., Whelihan, M., Fuentes, R., Dee, R., Cooley, B.C., Key, N.S., Wolberg, A.S., Bergmeier, W., Mackman, N., Tissue factor-positive tumor microvesicles activate platelets and enhance thrombosis in mice. J. Thromb. Haemost. 14 (2016), 153–166.
26. Tesselaar, M.E., Romijn, F.P., Van Der Linden, I.K., Prins, F.A., Bertina, R.M., Osanto, S., Microparticle-associated tissue factor activity: a link between cancer and thrombosis?. J. Thromb. Haemost. 5 (2007), 520–527.
27. Hron, G., Kollars, M., Weber, H., Sagaster, V., Quehenberger, P., Eichinger, S., Kyrle, P.A., Weltermann, A., Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer. Thromb. Haemost. 97 (2007), 119–123.
28. Zwicker, J.I., Liebman, H.A., Neuberg, D., Lacroix, R., Bauer, K.A., Furie, B.C., Furie, B., Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy. Clin. Cancer Res. 15 (2009), 6830–6840.
29. Thaler, J., Ay, C., Mackman, N., Bertina, R.M., Kaider, A., Marosi, C., Key, N.S., Barcel, D.A., Scheithauer, W., Kornek, G., Zielinski, C., Pabinger, I., Microparticle-associated tissue factor activity, venous thromboembolism and mortality in pancreatic, gastric, colorectal and brain cancer patients. J. Thromb. Haemost. 10 (2012), 1363–1370.
30. Toth, B., Liebhardt, S., Steinig, K., Ditsch, N., Rank, A., Bauerfeind, I., Spannagl, M., Friese, K., Reininger, A.J., Platelet-derived microparticles and coagulation activation in breast cancer patients. Thromb. Haemost. 100 (2008), 663–669.
31. Bang, O.Y., Chung, J., Lee, M.J., Kim, S.J., Cho, Y.H., Kim, G., Chung, C., Lee, K., Ahn, M., Moon, G.J., Cancer cell-derived extracellular vesicles are associated with coagulopathy causing ischemic stroke via tissue factor- independent way: the OASIS-CANCER study. PLoS One, 11, 2016, 10.1371/journal.pone.0159170 (epub).
32. Yang, C., Robbins, P.D., The roles of tumor-derived exosomes in cancer pathogenesis. Clin. Dev. Immunol., 2011, 2011, 10.1155/2011/842849 (epub).
33. Metcalf, R.L., Fry, D.J., Swindell, R., McGurk, A., Clamp, A.R., Jayson, G.C., Hasan, J., Thrombosis in ovarian cancer: a case control study. Br. J. Cancer 110 (2014), 1118–1124.
34. Taylor, D.D., Gercel-Taylor, C., MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110 (2008), 13–21.
35. Svensson, K.J., Kucharzewska, P., Christianson, H.C., Sköld, S., Löfstedt, T., Johansson, M.C., Mörgelin, M., Bengzon, J., Ruf, W., Belting, M., Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparin-binding EGF signaling in endothelial cells. Proc Nati Acad. 108 (2011), 13147–13152.
36. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951), 265–275.
37. Mehdiani, A., Maier, A., Pinto, A., Barth, M., Akhyari, P., Lichtenberg, A., An innovative method for exosome quantification and size measurement. J. Vis. Exp., 95, 2015, 10.3791/50974.
38. Helwa, I., Cai, J., Drewry, M.D., Zimmerman, A., Dinkins, M.B., Khaled, M.L., Seremwe, M., Dismuke, W.M., Bieberich, E., Stamer, W.D., Hamrick, M.W., Liu, Y., A comparative study of serum exosome isolation using differential ultracentrifugation and three commercial reagents. PLoS One, 12, 2017, 10.1371/journal.pone.0170628 (epub).
39. Walkowiak, B., Kȩsy, A., Michalec, L., Microplate reader—a convenient tool in studies of blood coagulation. Thromb. Res. 87 (1997), 95–103.
40. Krause, S., Scholz, T., Temmler, U., Losche, W., Monitoring the effects of platelet glycoprotein IIb/IIIa antagonists with a microtiter plate method for detection of platelet aggregation. Platelets 12 (2001), 423–430.
41. Lu, Q., Malinauskas, R.A., Comparison of two platelet activation markers using flow cytometry after in vitro shear stress exposure of whole human blood. Artif. Organs 35 (2011), 137–144.
42. Langer, F., Spath, B., Haubold, K., Holstein, K., Marx, G., Wierecky, J., Brümmendorf, T.H., Dierlamm, J., Bokemeyer, C., Eifrig, B., Tissue factor procoagulant activity of plasma microparticles in patients with cancer-associated disseminated intravascular coagulation. Ann. Hematol. 87 (2008), 451–457.
43. Muhsin-Sharafaldine, M.R., Saunderson, S.C., Dunn, A.C., Faed, J.M., Kleffmann, T., McLellan, A.D., Procoagulant and immunogenic properties of melanoma exosomes, microvesicles and apoptotic vesicles. Oncotarget 7 (2016), 56279–56294.
44. Laresche, C., Pelletier, F., Garnache-Ottou, F., Lihoreau, T., Biichlé, S., Mourey, G., Saas, P., Humbert, P., Seilles, E., Aubin, F., Increased levels of circulating microparticles are associated with increased procoagulant activity in patients with cutaneous malignant melanoma. J Invest. Dermatol. 134 (2014), 176–182.
45. Khorana, A.A., Francis, C.W., Menzies, K.E., Wang, J.G., Hyrien, O., Hathcock, J., Mackman, N., Taubman, M.B., Plasma tissue factor may be predictive of venous thromboembolism in pancreatic cancer. J. Thromb. Haemost. 6 (2008), 1983–1985.
46. Nilsson, R.J., Balaj, L., Hulleman, E., van Rijn, S., Pegtel, D.M., Walraven, M., Widmark, A., Gerritsen, W.R., Verheul, H.M., Vandertop, W.P., Noske, D.P., Skog, J., Würdinger, T., Blood platelets contain tumor-derived RNA biomarkers. Blood 118 (2011), 3680–3683.
47. Nilsson, R.J., Karachaliou, N., Berenguer, J., Gimenez-Capitan, A., Schellen, P., Teixido, C., Tannous, K., Kuiper, J.L., Drees, E., Grabowska, M., van Keulen, M., Heideman, D.A., Thunnissen, E., Dingemans, A.M., Viteri, S., Tannous, B.A., Drozdowskyj, A., Rosell, R., Smit, E.F., Wurdinger, T., Rearranged EML4-ALK fusion transcripts sequester in circulating blood platelets and enable blood-based crizotinib response monitoring in non-small-cell lung cancer. Oncotarget 7 (2016), 1066–1075.
48. Sawicki, G., Sanders, E.J., Salas, E., Wozniak, M., Rodrigo, J., Radomski, M.W., Localization and translocation of MMP-2 during aggregation of human platelets. Thromb. Haemost. 80 (1998), 836–839.
49. Woulfe, D., Yang, J., Brass, L., ADP and platelets: the end of the beginning. J. Clin. Invest. 107 (2001), 1503–1505.
50. Leal, A.C., Mizurini, D.M., Gomes, T., Rochael, N.C., Saraiva, E.M., Dias, M.S., Werneck, C.C., Sielski, M.S., Vicente, C.P., Monteiro, R.Q., Tumor-derived exosomes induce the formation of neutrophil extracellular traps: implications for the establishment of cancer-associated thrombosis. Sci Rep, 7, 2017, 10.1038/s41598-017-06893-7 (epub).
51. Davila, M., Amirkhosravi, A., Coll, E., Desai, H., Robles, L., Colon, J., Baker, C.H., Francis, J.L., Tissue factor-bearing microparticles derived from tumor cells: impact on coagulation activation. J. Thromb. Haemost. 6 (2008), 1517–1524.
52. Lima, L.G., Leal, A.C., Vargas, G., Porto-Carreiro, I., Monteiro, R.Q., Intercellular transfer of tissue factor via the uptake of tumor-derived microvesicles. Thromb. Res. 132 (2013), 450–456.
53. Garnier, D., Magnus, N., Lee, T.H., Bentley, V., Meehan, B., Milsom, C., Montermini, L., Kislinger, T., Rak, J., Cancer cells induced to express mesenchymal phenotype release exosome-like extracellular vesicles carrying tissue factor. JBC 52 (2012), 43565–43572.
54. Ettelaie, C., Collier, M.E., Maraveyas, A., Ettelaie, R., Characterization of physical properties of tissue factor-containing microvesicles and a comparison of ultracentrifuge-based recovery procedures. J Extracell Vesicles, 3, 2014, 10.3402/jev.v3.23592 (epub).
55. Gheldof, D., Hardij, J., Cecchet, F., Chatelain, B., Dogné, J.M., Mullier, F., Thrombin generation assay and transmission electron microscopy: a useful combination to study tissue factor-bearing microvesicles. J Extracell Vesicles, 2, 2013, 10.3402/jev.v2i0.19728 (epub).
56. Ahlbrecht, J., Dickmann, B., Ay, C., Dunkler, D., Thaler, J., Schmidinger, M., Quehenberger, P., Haitel, A., Zielinski, C., Pabinger, I., Tumor grade is associated with venous thromboembolism in patients with cancer: results from the Vienna Cancer and Thrombosis Study. J. Clin. Oncol. 30 (2012), 3870–3875.