Download PDF
Semin Thromb Hemost 2019; 45(06): 593-603
DOI: 10.1055/s-0039-1693476
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Microvesicles and Cancer Associated Thrombosis

Romaric Lacroix
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
2   Department of Hematology and Vascular Biology, CHU La Conception, APHM, Marseille, France
,
Loris Vallier
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
,
Amandine Bonifay
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
,
Stephanie Simoncini
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
,
Diane Mege
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
,
Mathilde Aubert
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
,
Laurence Panicot-Dubois
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
,
Christophe Dubois
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
,
Françoise Dignat-George
1   Aix-Marseille University, INSERM, INRA, C2VN UMR_S1263, UFR de Pharmacie, Marseille, France
2   Department of Hematology and Vascular Biology, CHU La Conception, APHM, Marseille, France
› Author Affiliations
Further Information

Publication History

Publication Date:
20 August 2019 (online)

    Permissions and Reprints

Abstract

Microvesicles (MVs) are small membrane enclosed structures released into the extracellular space by virtually all cell types. Their composition varies according to the cell origin and the stimulus which caused their formation. They harbor functional molecules and participate in intercellular communication. Endothelium, inflammatory cells, and cancer cells produce procoagulant MVs which contribute to cancer-associated thrombosis (CAT) in animal models. The tissue factor (TF) conveyed by these MVs was shown to play a key role in different animal models of experimental CAT. Alternatively, other molecular mechanisms involving polyphosphates or phosphatidylethanolamine could also be involved. In clinical practice, an association between an increase in the number of TF-positive or the procoagulant activity of these MVs and the occurrence of CAT has indeed been demonstrated in pancreatic-biliary cancers, suggesting that they could behave as a biomarker predictive for CAT. However, to date, this association was not confirmed in other types of cancer. Potential causes explaining this limited associated between MVs and CAT are (1) the diversity of mechanisms associating MVs and different types of cancer; (2) a more complex role of MVs in hemostasis integrating their anticoagulant and fibrinolytic activity; and (3) the lack of sensitivity, reproducibility, and standardization of current methodologies permitting measurement of MVs. Each of these hypotheses constitutes an interesting exploration path for a future reassessment of the clinical interest of the MVs in CAT.

Keywords

extracellular vesicles - microvesicles - cancer-associated thrombosis
 

  • References

  • 1 van der Pol E, Böing AN, Harrison P, Sturk A, Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev 2012; 64 (03) 676-705
    CrossrefPubMedGoogle Scholar
  • 2 Boulanger CM, Loyer X, Rautou P-E, Amabile N. Extracellular vesicles in coronary artery disease. Nat Rev Cardiol 2017; 14 (05) 259-272
    CrossrefPubMedGoogle Scholar
  • 3 György B, Szabó TG, Pásztói M. , et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 2011; 68 (16) 2667-2688
    CrossrefPubMedGoogle Scholar
  • 4 Ciardiello C, Cavallini L, Spinelli C. , et al. Focus on extracellular vesicles: new frontiers of cell-to-cell communication in cancer. Int J Mol Sci 2016; 17 (02) 175
    CrossrefPubMedGoogle Scholar
  • 5 Dignat-George F, Boulanger CM. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 2011; 31 (01) 27-33
    CrossrefPubMedGoogle Scholar
  • 6 Ridger VC, Boulanger CM, Angelillo-Scherrer A. , et al. Microvesicles in vascular homeostasis and diseases. Position paper of the European Society of Cardiology (ESC) working group on atherosclerosis and vascular biology. Thromb Haemost 2017; 117: 1296-1316
    Article in Thieme ConnectPubMedGoogle Scholar
  • 7 Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013; 13 (01) 34-45
    CrossrefPubMedGoogle Scholar
  • 8 Suzuki J, Umeda M, Sims PJ, Nagata S. Calcium-dependent phospholipid scrambling by TMEM16F. Nature 2010; 468 (7325): 834-838
    CrossrefPubMedGoogle Scholar
  • 9 Lhermusier T, Chap H, Payrastre B. Platelet membrane phospholipid asymmetry: from the characterization of a scramblase activity to the identification of an essential protein mutated in Scott syndrome. J Thromb Haemost 2011; 9 (10) 1883-1891
    CrossrefPubMedGoogle Scholar
  • 10 Dvorak HF, Quay SC, Orenstein NS. , et al. Tumor shedding and coagulation. Science 1981; 212 (4497): 923-924
    CrossrefPubMedGoogle Scholar
  • 11 Dvorak HF, Van DeWater L, Bitzer AM. , et al. Procoagulant activity associated with plasma membrane vesicles shed by cultured tumor cells. Cancer Res 1983; 43 (09) 4434-4442
    PubMedGoogle Scholar
  • 12 Collier MEW, Ettelaie C. Regulation of the incorporation of tissue factor into microparticles by serine phosphorylation of the cytoplasmic domain of tissue factor. J Biol Chem 2011; 286 (14) 11977-11984
    CrossrefPubMedGoogle Scholar
  • 13 Collier MEW, Maraveyas A, Ettelaie C. Filamin-A is required for the incorporation of tissue factor into cell-derived microvesicles. Thromb Haemost 2014; 111 (04) 647-655
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Rothmeier AS, Marchese P, Petrich BG. , et al. Caspase-1-mediated pathway promotes generation of thromboinflammatory microparticles. J Clin Invest 2015; 125 (04) 1471-1484
    CrossrefPubMedGoogle Scholar
  • 15 Ettelaie C, Collier MEW, Featherby S, Greenman J, Maraveyas A. Oligoubiquitination of tissue factor on Lys255 promotes Ser253-dephosphorylation and terminates TF release. Biochim Biophys Acta 2016; 1863 (11) 2846-2857
    PubMedGoogle Scholar
  • 16 Rothmeier AS, Marchese P, Langer F. , et al. Tissue factor prothrombotic activity is regulated by integrin-arf6 trafficking. Arterioscler Thromb Vasc Biol 2017; 37 (07) 1323-1331
    CrossrefPubMedGoogle Scholar
  • 17 Sabatier F, Roux V, Anfosso F, Camoin L, Sampol J, Dignat-George F. Interaction of endothelial microparticles with monocytic cells in vitro induces tissue factor-dependent procoagulant activity. Blood 2002; 99 (11) 3962-3970
    CrossrefPubMedGoogle Scholar
  • 18 Meziani F, Delabranche X, Asfar P, Toti F. Bench-to-bedside review: circulating microparticles--a new player in sepsis?. Crit Care 2010; 14 (05) 236
    CrossrefPubMedGoogle Scholar
  • 19 Del Conde I, Shrimpton CN, Thiagarajan P, López JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005; 106 (05) 1604-1611
    CrossrefPubMedGoogle Scholar
  • 20 Collier MEW, Mah P-M, Xiao Y, Maraveyas A, Ettelaie C. Microparticle-associated tissue factor is recycled by endothelial cells resulting in enhanced surface tissue factor activity. Thromb Haemost 2013; 110 (05) 966-976
    Article in Thieme ConnectPubMedGoogle Scholar
  • 21 Cointe S, Lacroix R, Dignat-George F. Platelet-derived microparticles. In: Gresele P, Kleiman NS, Lopez JA, Page CP. Platelets in Thrombotic and Non-Thrombotic Disorder. Cham, Switzerland: Springer; 2017: 379-392
    Google Scholar
  • 22 Mazurov A, Antonova O, Golubeva N. Procoagulant properties of microparticles produced by monocytes, granulocytes, platelets and endothelial cells. Res Pr Thromb Haemost Berlin 2017; 1: 443-444
    PubMedGoogle Scholar
  • 23 Tripisciano C, Weiss R, Eichhorn T. , et al. Different potential of extracellular vesicles to support thrombin generation: contributions of phosphatidylserine, tissue factor, and cellular origin. Sci Rep 2017; 7 (01) 6522
    CrossrefPubMedGoogle Scholar
  • 24 Van Der Meijden PEJ, Van Schilfgaarde M, Van Oerle R, Renné T, ten Cate H, Spronk HM. Platelet- and erythrocyte-derived microparticles trigger thrombin generation via factor XIIa. J Thromb Haemost 2012; 10 (07) 1355-1362
    CrossrefPubMedGoogle Scholar
  • 25 Rubin O, Delobel J, Prudent M. , et al. Red blood cell-derived microparticles isolated from blood units initiate and propagate thrombin generation. Transfusion 2013; 53 (08) 1744-1754
    CrossrefPubMedGoogle Scholar
  • 26 Angelillo-Scherrer A. Leukocyte-derived microparticles in vascular homeostasis. Circ Res 2012; 110 (02) 356-369
    CrossrefPubMedGoogle Scholar
  • 27 Halim ATA, Ariffin NAFM, Azlan M. Review: the multiple roles of monocytic microparticles. Inflammation 2016; 39 (04) 1277-1284
    CrossrefPubMedGoogle Scholar
  • 28 Stojkovic S, Thulin Å, Hell L. , et al. IL-33 stimulates the release of procoagulant microvesicles from human monocytes and differentially increases tissue factor in human monocyte subsets. Thromb Haemost 2017; 117 (07) 1379-1390
    Article in Thieme ConnectPubMedGoogle Scholar
  • 29 Kambas K, Chrysanthopoulou A, Vassilopoulos D. , et al. Tissue factor expression in neutrophil extracellular traps and neutrophil derived microparticles in antineutrophil cytoplasmic antibody associated vasculitis may promote thromboinflammation and the thrombophilic state associated with the disease. Ann Rheum Dis 2014; 73 (10) 1854-1863
    CrossrefPubMedGoogle Scholar
  • 30 Egorina EM, Sovershaev MA, Olsen JO, Østerud B. Granulocytes do not express but acquire monocyte-derived tissue factor in whole blood: evidence for a direct transfer. Blood 2008; 111 (03) 1208-1216
    CrossrefPubMedGoogle Scholar
  • 31 Geddings JE, Mackman N. Tumor-derived tissue factor-positive microparticles and venous thrombosis in cancer patients. Blood 2013; 122 (11) 1873-1880
    PubMedGoogle Scholar
  • 32 Ettelaie C, Collier ME, Featherby S, Benelhaj NE, Greenman J, Maraveyas A. Analysis of the potential of cancer cell lines to release tissue factor-containing microvesicles: correlation with tissue factor and PAR2 expression. Thromb J 2016; 14: 2
    CrossrefPubMedGoogle Scholar
  • 33 Gomes FG, Sandim V, Almeida VH. , et al. Breast-cancer extracellular vesicles induce platelet activation and aggregation by tissue factor-independent and -dependent mechanisms. Thromb Res 2017; 159: 24-32
    CrossrefPubMedGoogle Scholar
  • 34 Falati S, Liu Q, Gross P. , et al. 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 2003; 197 (11) 1585-1598
    CrossrefPubMedGoogle Scholar
  • 35 Chou J, Mackman N, Merrill-Skoloff G, Pedersen B, Furie BC, Furie B. Hematopoietic cell-derived microparticle tissue factor contributes to fibrin formation during thrombus propagation. Blood 2004; 104 (10) 3190-3197
    PubMedGoogle Scholar
  • 36 Owens III AP, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res 2011; 108 (10) 1284-1297
    CrossrefPubMedGoogle Scholar
  • 37 Zwicker JI, Trenor III CC, Furie BC, Furie B. Tissue factor-bearing microparticles and thrombus formation. Arterioscler Thromb Vasc Biol 2011; 31 (04) 728-733
    CrossrefPubMedGoogle Scholar
  • 38 Reitsma PH, Versteeg HH, Middeldorp S. Mechanistic view of risk factors for venous thromboembolism. Arterioscler Thromb Vasc Biol 2012; 32 (03) 563-568
    CrossrefPubMedGoogle Scholar
  • 39 Mege D, Crescence L, Ouaissi M. , et al. Fibrin-bearing microparticles: marker of thrombo-embolic events in pancreatic and colorectal cancers. Oncotarget 2017; 8 (57) 97394-97406
    CrossrefPubMedGoogle Scholar
  • 40 Hisada Y, Mackman N. Mouse models of cancer-associated thrombosis. Thromb Res 2018; 164 (Suppl. 01) S48-S53
    CrossrefPubMedGoogle Scholar
  • 41 Sørensen HT, Mellemkjaer L, Olsen JH, Baron JA. Prognosis of cancers associated with venous thromboembolism. N Engl J Med 2000; 343 (25) 1846-1850
    CrossrefPubMedGoogle Scholar
  • 42 Tesselaar MET, Romijn FPHTM, Van Der Linden IK, Prins FA, Bertina RM, Osanto S. Microparticle-associated tissue factor activity: a link between cancer and thrombosis?. J Thromb Haemost 2007; 5 (03) 520-527
    CrossrefPubMedGoogle Scholar
  • 43 Zwicker JI, Liebman HA, Neuberg D. , et al. Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res 2009; 15 (22) 6830-6840
    CrossrefPubMedGoogle Scholar
  • 44 Manly DA, Wang J, Glover SL. , et al. Increased microparticle tissue factor activity in cancer patients with venous thromboembolism. Thromb Res 2010; 125 (06) 511-512
    CrossrefPubMedGoogle Scholar
  • 45 Campello E, Spiezia L, Radu CM. , et al. Endothelial, platelet, and tissue factor-bearing microparticles in cancer patients with and without venous thromboembolism. Thromb Res 2011; 127 (05) 473-477
    CrossrefPubMedGoogle Scholar
  • 46 Khorana AA, Francis CW, Menzies KE. , et al. Plasma tissue factor may be predictive of venous thromboembolism in pancreatic cancer. J Thromb Haemost 2008; 6 (11) 1983-1985
    CrossrefPubMedGoogle Scholar
  • 47 van Doormaal F, Kleinjan A, Berckmans RJ. , et al. Coagulation activation and microparticle-associated coagulant activity in cancer patients. An exploratory prospective study. Thromb Haemost 2012; 108 (01) 160-165
    Article in Thieme ConnectPubMedGoogle Scholar
  • 48 Sartori MT, Della Puppa A, Ballin A. , et al. Circulating microparticles of glial origin and tissue factor bearing in high-grade glioma: a potential prothrombotic role. Thromb Haemost 2013; 110 (02) 378-385
    Article in Thieme ConnectPubMedGoogle Scholar
  • 49 Bharthuar A, Khorana AA, Hutson A. , et al. Circulating microparticle tissue factor, thromboembolism and survival in pancreaticobiliary cancers. Thromb Res 2013; 132 (02) 180-184
    CrossrefPubMedGoogle Scholar
  • 50 Woei-A-Jin FJSH, Tesselaar MET, Garcia Rodriguez P, Romijn FP, Bertina RM, Osanto S. Tissue factor-bearing microparticles and CA19.9: two players in pancreatic cancer-associated thrombosis?. Br J Cancer 2016; 115 (03) 332-338
    CrossrefPubMedGoogle Scholar
  • 51 van Es N, Hisada Y, Di Nisio M. , et al. Extracellular vesicles exposing tissue factor for the prediction of venous thromboembolism in patients with cancer: A prospective cohort study. Thromb Res 2018; 166: 54-59
    CrossrefPubMedGoogle Scholar
  • 52 Faille D, Bourrienne M-C, de Raucourt E. , et al. Biomarkers for the risk of thrombosis in pancreatic adenocarcinoma are related to cancer process. Oncotarget 2018; 9 (41) 26453-26465
    CrossrefPubMedGoogle Scholar
  • 53 Thaler J, Ay C, Weinstabl H. , et al. Circulating procoagulant microparticles in cancer patients. Ann Hematol 2011; 90 (04) 447-453
    CrossrefPubMedGoogle Scholar
  • 54 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 (07) 1363-1370
    CrossrefPubMedGoogle Scholar
  • 55 Hernández C, Orbe J, Roncal C. , et al. Tissue factor expressed by microparticles is associated with mortality but not with thrombosis in cancer patients. Thromb Haemost 2013; 110 (03) 598-608
    Article in Thieme ConnectPubMedGoogle Scholar
  • 56 Cui C-J, Wang G-J, Yang S, Huang SK, Qiao R, Cui W. Tissue factor-bearing MPs and the risk of venous thrombosis in cancer patients: a meta-analysis. Sci Rep 2018; 8 (01) 1675
    CrossrefPubMedGoogle Scholar
  • 57 Hisada Y, Mackman N. Cancer-associated pathways and biomarkers of venous thrombosis. Blood 2017; 130 (13) 1499-1506
    CrossrefPubMedGoogle Scholar
  • 58 Mege D, Mezouar S, Dignat-George F, Panicot-Dubois L, Dubois C. Microparticles and cancer thrombosis in animal models. Thromb Res 2016; 140 (Suppl. 01) S21-S26
    CrossrefPubMedGoogle Scholar
  • 59 Thomas GM, 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 2009; 206 (09) 1913-1927
    CrossrefPubMedGoogle Scholar
  • 60 Mezouar S, Darbousset R, Dignat-George F, Panicot-Dubois L, Dubois C. Inhibition of platelet activation prevents the P-selectin and integrin-dependent accumulation of cancer cell microparticles and reduces tumor growth and metastasis in vivo. Int J Cancer 2015; 136 (02) 462-475
    CrossrefPubMedGoogle Scholar
  • 61 Thomas GM, Brill A, Mezouar S. , et al. Tissue factor expressed by circulating cancer cell-derived microparticles drastically increases the incidence of deep vein thrombosis in mice. J Thromb Haemost 2015; 13 (07) 1310-1319
    CrossrefPubMedGoogle Scholar
  • 62 Geddings JE, Hisada Y, Boulaftali Y. , et al. Tissue factor-positive tumor microvesicles activate platelets and enhance thrombosis in mice. J Thromb Haemost 2016; 14 (01) 153-166
    CrossrefPubMedGoogle Scholar
  • 63 Hisada Y, Ay C, Auriemma AC, Cooley BC, Mackman N. Human pancreatic tumors grown in mice release tissue factor-positive microvesicles that increase venous clot size. J Thromb Haemost 2017; 15 (11) 2208-2217
    CrossrefPubMedGoogle Scholar
  • 64 Date K, Ettelaie C, Maraveyas A. Tissue factor-bearing microparticles and inflammation: a potential mechanism for the development of venous thromboembolism in cancer. J Thromb Haemost 2017; 15 (12) 2289-2299
    CrossrefPubMedGoogle Scholar
  • 65 Stark K, Schubert I, Joshi U. , et al. Distinct pathogenesis of pancreatic cancer microvesicle-associated venous thrombosis identifies new antithrombotic targets in vivo. Arterioscler Thromb Vasc Biol 2018; 38 (04) 772-786
    CrossrefPubMedGoogle Scholar
  • 66 Lee AYY, Levine MN, Baker RI. , et al; Randomized Comparison of Low-Molecular-Weight Heparin versus Oral Anticoagulant Therapy for the Prevention of Recurrent Venous Thromboembolism in Patients with Cancer (CLOT) Investigators. Low-molecular-weight heparin versus a coumarin for the prevention of recurrent venous thromboembolism in patients with cancer. N Engl J Med 2003; 349 (02) 146-153
    CrossrefPubMedGoogle Scholar
  • 67 Lee AYY, Kamphuisen PW, Meyer G. , et al; CATCH Investigators. Tinzaparin vs warfarin for treatment of acute venous thromboembolism in patients with active cancer: a randomized clinical trial. JAMA 2015; 314 (07) 677-686
    CrossrefPubMedGoogle Scholar
  • 68 Streiff MB, Milentijevic D, McCrae K. , et al. Effectiveness and safety of anticoagulants for the treatment of venous thromboembolism in patients with cancer. Am J Hematol 2018; 93 (05) 664-671
    CrossrefPubMedGoogle Scholar
  • 69 Nickel KF, Ronquist G, Langer F. , et al. The polyphosphate-factor XII pathway drives coagulation in prostate cancer-associated thrombosis. Blood 2015; 126 (11) 1379-1389
    PubMedGoogle Scholar
  • 70 Nickel KF, Labberton L, Long AT. , et al. The polyphosphate/factor XII pathway in cancer-associated thrombosis: novel perspectives for safe anticoagulation in patients with malignancies. Thromb Res 2016; 141 (Suppl. 02) S4-S7
    CrossrefPubMedGoogle Scholar
  • 71 Suzuki-Inoue K, Kato Y, Inoue O. , et al. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem 2007; 282 (36) 25993-26001
    CrossrefPubMedGoogle Scholar
  • 72 Thaler J, Koder S, Kornek G, Pabinger I, Ay C. Microparticle-associated tissue factor activity in patients with metastatic pancreatic cancer and its effect on fibrin clot formation. Transl Res 2014; 163 (02) 145-150
    CrossrefPubMedGoogle Scholar
  • 73 Riedl J, Preusser M, Nazari PMS. , et al. Podoplanin expression in primary brain tumors induces platelet aggregation and increases risk of venous thromboembolism. Blood 2017; 129 (13) 1831-1839
    CrossrefPubMedGoogle Scholar
  • 74 Leal AC, Mizurini DM, Gomes T. , et al. Tumor-derived exosomes induce the formation of neutrophil extracellular traps: implications for the establishment of cancer-associated thrombosis. Sci Rep 2017; 7 (01) 6438
    CrossrefPubMedGoogle Scholar
  • 75 Tans G, Rosing J, Thomassen MC, Heeb MJ, Zwaal RF, Griffin JH. Comparison of anticoagulant and procoagulant activities of stimulated platelets and platelet-derived microparticles. Blood 1991; 77 (12) 2641-2648
    CrossrefPubMedGoogle Scholar
  • 76 Dahlbäck B, Wiedmer T, Sims PJ. Binding of anticoagulant vitamin K-dependent protein S to platelet-derived microparticles. Biochemistry 1992; 31 (51) 12769-12777
    CrossrefPubMedGoogle Scholar
  • 77 Stavenuiter F, Davis NF, Duan E, Gale AJ, Heeb MJ. Platelet protein S directly inhibits procoagulant activity on platelets and microparticles. Thromb Haemost 2013; 109 (02) 229-237
    Article in Thieme ConnectPubMedGoogle Scholar
  • 78 Pérez-Casal M, Downey C, Fukudome K, Marx G, Toh CH. Activated protein C induces the release of microparticle-associated endothelial protein C receptor. Blood 2005; 105 (04) 1515-1522
    CrossrefPubMedGoogle Scholar
  • 79 Satta N, Freyssinet JM, Toti F. The significance of human monocyte thrombomodulin during membrane vesiculation and after stimulation by lipopolysaccharide. Br J Haematol 1997; 96 (03) 534-542
    CrossrefPubMedGoogle Scholar
  • 80 Steppich B, Mattisek C, Sobczyk D, Kastrati A, Schömig A, Ott I. Tissue factor pathway inhibitor on circulating microparticles in acute myocardial infarction. Thromb Haemost 2005; 93 (01) 35-39
    Article in Thieme ConnectPubMedGoogle Scholar
  • 81 Tsimerman G, Roguin A, Bachar A, Melamed E, Brenner B, Aharon A. Involvement of microparticles in diabetic vascular complications. Thromb Haemost 2011; 106 (02) 310-321
    Article in Thieme ConnectPubMedGoogle Scholar
  • 82 Aharon A, Tamari T, Brenner B. Monocyte-derived microparticles and exosomes induce procoagulant and apoptotic effects on endothelial cells. Thromb Haemost 2008; 100 (05) 878-885
    Article in Thieme ConnectPubMedGoogle Scholar
  • 83 Aharon A, Katzenell S, Tamari T, Brenner B. Microparticles bearing tissue factor and tissue factor pathway inhibitor in gestational vascular complications. J Thromb Haemost 2009; 7 (06) 1047-1050
    CrossrefPubMedGoogle Scholar
  • 84 Aharon A, Sabbah A, Ben-Shaul S. , et al. Chemotherapy administration to breast cancer patients affects extracellular vesicles thrombogenicity and function. Oncotarget 2017; 8 (38) 63265-63280
    CrossrefPubMedGoogle Scholar
  • 85 Gheldof D, Mullier F, Chatelain B, Dogné JM, Chatelain C. Inhibition of tissue factor pathway inhibitor increases the sensitivity of thrombin generation assay to procoagulant microvesicles. Blood Coagul Fibrinolysis 2013; 24 (05) 567-572
    CrossrefPubMedGoogle Scholar
  • 86 Hellum M, Franco-Lie I, Øvstebø R, Hauge T, Henriksson CE. The effect of corn trypsin inhibitor, anti-tissue factor pathway inhibitor antibodies and phospholipids on microvesicle-associated thrombin generation in patients with pancreatic cancer and healthy controls. PLoS One 2017; 12 (09) e0184579
    CrossrefPubMedGoogle Scholar
  • 87 Dolo V, Ginestra A, Ghersi G, Nagase H, Vittorelli ML. Human breast carcinoma cells cultured in the presence of serum shed membrane vesicles rich in gelatinolytic activities. J Submicrosc Cytol Pathol 1994; 26 (02) 173-180
    PubMedGoogle Scholar
  • 88 Ginestra A, Monea S, Seghezzi G. , et al. Urokinase plasminogen activator and gelatinases are associated with membrane vesicles shed by human HT1080 fibrosarcoma cells. J Biol Chem 1997; 272 (27) 17216-17222
    CrossrefPubMedGoogle Scholar
  • 89 Dolo V, Ginestra A, Cassarà D. , et al. Selective localization of matrix metalloproteinase 9, beta1 integrins, and human lymphocyte antigen class I molecules on membrane vesicles shed by 8701-BC breast carcinoma cells. Cancer Res 1998; 58 (19) 4468-4474
    PubMedGoogle Scholar
  • 90 Dolo V, D'Ascenzo S, Violini S. , et al. Matrix-degrading proteinases are shed in membrane vesicles by ovarian cancer cells in vivo and in vitro. Clin Exp Metastasis 1999; 17 (02) 131-140
    CrossrefPubMedGoogle Scholar
  • 91 Ginestra A, Miceli D, Dolo V, Romano FM, Vittorelli ML. Membrane vesicles in ovarian cancer fluids: a new potential marker. Anticancer Res 1999; 19 (4C): 3439-3445
    PubMedGoogle Scholar
  • 92 Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, Fishman DA. Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res 2004; 64 (19) 7045-7049
    CrossrefPubMedGoogle Scholar
  • 93 Millimaggi D, Festuccia C, Angelucci A. , et al. Osteoblast-conditioned media stimulate membrane vesicle shedding in prostate cancer cells. Int J Oncol 2006; 28 (04) 909-914
    PubMedGoogle Scholar
  • 94 Ginestra A, La Placa MD, Saladino F, Cassarà D, Nagase H, Vittorelli ML. The amount and proteolytic content of vesicles shed by human cancer cell lines correlates with their in vitro invasiveness. Anticancer Res 1998; 18 (5A): 3433-3437
    PubMedGoogle Scholar
  • 95 Angelucci A, D'Ascenzo S, Festuccia C. , et al. Vesicle-associated urokinase plasminogen activator promotes invasion in prostate cancer cell lines. Clin Exp Metastasis 2000; 18 (02) 163-170
    CrossrefPubMedGoogle Scholar
  • 96 Jung T, Castellana D, Klingbeil P. , et al. CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 2009; 11 (10) 1093-1105
    CrossrefPubMedGoogle Scholar
  • 97 McCready J, Sims JD, Chan D, Jay DG. Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: a role for plasminogen activation. BMC Cancer 2010; 10: 294
    CrossrefPubMedGoogle Scholar
  • 98 Lacroix R, Sabatier F, Mialhe A. , et al. Activation of plasminogen into plasmin at the surface of endothelial microparticles: a mechanism that modulates angiogenic properties of endothelial progenitor cells in vitro. Blood 2007; 110 (07) 2432-2439
    CrossrefPubMedGoogle Scholar
  • 99 Dejouvencel T, Doeuvre L, Lacroix R. , et al. Fibrinolytic cross-talk: a new mechanism for plasmin formation. Blood 2010; 115 (10) 2048-2056
    CrossrefPubMedGoogle Scholar
  • 100 Lacroix R, Plawinski L, Robert S. , et al. Leukocyte- and endothelial-derived microparticles: a circulating source for fibrinolysis. Haematologica 2012; 97 (12) 1864-1872
    CrossrefPubMedGoogle Scholar
  • 101 Lacroix R, Dignat-George F. Microparticles: new protagonists in pericellular and intravascular proteolysis. Semin Thromb Hemost 2013; 39 (01) 33-39
    Article in Thieme ConnectPubMedGoogle Scholar
  • 102 Kwaan HC, Rego EM. Role of microparticles in the hemostatic dysfunction in acute promyelocytic leukemia. Semin Thromb Hemost 2010; 36 (08) 917-924
    Article in Thieme ConnectPubMedGoogle Scholar
  • 103 Durrieu L, Bharadwaj A, Waisman DM. Analysis of the thrombotic and fibrinolytic activities of tumor cell-derived extracellular vesicles. Blood Adv 2018; 2 (10) 1054-1065
    CrossrefPubMedGoogle Scholar
  • 104 Al-Nedawi K, Szemraj J, Cierniewski CS. Mast cell-derived exosomes activate endothelial cells to secrete plasminogen activator inhibitor type 1. Arterioscler Thromb Vasc Biol 2005; 25 (08) 1744-1749
    CrossrefPubMedGoogle Scholar
  • 105 Al Saleh HA, Haas-Neill S, Al-Hashimi A. , et al. Thrombotic characteristics of extracellular vesicles derived from prostate cancer cells. Prostate 2018; 78 (13) 953-961
    CrossrefPubMedGoogle Scholar
  • 106 Lacroix R, Dubois C, Leroyer AS, Sabatier F, Dignat-George F. Revisited role of microparticles in arterial and venous thrombosis. J Thromb Haemost 2013; 11 (Suppl. 01) 24-35
    CrossrefPubMedGoogle Scholar
  • 107 Vallier L, Cointe S, Lacroix R. , et al. Microparticles and Fibrinolysis. Semin Thromb Hemost 2017; 43 (02) 129-134
    Article in Thieme ConnectPubMedGoogle Scholar
  • 108 Cointe S, Harti Souab K, Bouriche T. , et al. A new assay to evaluate microvesicle plasmin generation capacity: validation in disease with fibrinolysis imbalance. J Extracell Vesicles 2018; 7 (01) 1494482
    CrossrefPubMedGoogle Scholar
  • 109 Lacroix R, Judicone C, Poncelet P. , et al. Impact of pre-analytical parameters on the measurement of circulating microparticles: towards standardization of protocol. J Thromb Haemost 2012; 10 (03) 437-446
    CrossrefPubMedGoogle Scholar
  • 110 Coumans FAW, Brisson AR, Buzas EI. , et al. Methodological guidelines to study extracellular vesicles. Circ Res 2017; 120 (10) 1632-1648
    CrossrefPubMedGoogle Scholar
  • 111 Shpacovitch V, Hergenröder R. Optical and surface plasmonic approaches to characterize extracellular vesicles. A review. Anal Chim Acta 2018; 1005: 1-15
    CrossrefPubMedGoogle Scholar
  • 112 Laroche M, Dunois C, Vissac AM, Amiral J. Update on functional and genetic laboratory assays for the detection of platelet microvesicles. Platelets 2017; 28 (03) 235-241
    CrossrefPubMedGoogle Scholar
  • 113 Poncelet P, Robert S, Bailly N. , et al. Tips and tricks for flow cytometry-based analysis and counting of microparticles. Transfus Apheresis Sci 2015; 53 (02) 110-126
    CrossrefPubMedGoogle Scholar
  • 114 Nolan JP, Jones JC. Detection of platelet vesicles by flow cytometry. Platelets 2017; 28 (03) 256-262
    CrossrefPubMedGoogle Scholar
  • 115 Hisada Y, Auriemma AC, Alexander W, Ay C, Mackman N. Detection of tissue factor-positive extracellular vesicles by laser scanning confocal microscopy. Thromb Res 2017; 150: 65-72
    CrossrefPubMedGoogle Scholar
  • 116 Exner T, Joseph J, Low J, Connor D, Ma D. A new activated factor X-based clotting method with improved specificity for procoagulant phospholipid. Blood Coagul Fibrinolysis 2003; 14 (08) 773-779
    CrossrefPubMedGoogle Scholar
  • 117 Jy W, Horstman LL, Jimenez JJ. , et al. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2 (10) 1842-1851
    CrossrefPubMedGoogle Scholar
  • 118 Hemker HC, Giesen P, AlDieri R. , et al. The calibrated automated thrombogram (CAT): a universal routine test for hyper- and hypocoagulability. Pathophysiol Haemost Thromb 2002; 32 (5-6): 249-253
    CrossrefPubMedGoogle Scholar
  • 119 Hellum M, Øvstebø R, Trøseid A-MS, Berg JP, Brandtzaeg P, Henriksson CE. Microparticle-associated tissue factor activity measured with the Zymuphen MP-TF kit and the calibrated automated thrombogram assay. Blood Coagul Fibrinolysis 2012; 23 (06) 520-526
    CrossrefPubMedGoogle Scholar
  • 120 Hisada Y, Alexander W, Kasthuri R. , et al. Measurement of microparticle tissue factor activity in clinical samples: A summary of two tissue factor-dependent FXa generation assays. Thromb Res 2016; 139: 90-97
    CrossrefPubMedGoogle Scholar
  • 121 Tatsumi K, Antoniak S, Monroe III DM, Khorana AA, Mackman N. ; Subcommittee on Hemostasis and Malignancy of the Scientific and Standardization Committee of the International Society on Thrombosis and Hemostasis. Evaluation of a new commercial assay to measure microparticle tissue factor activity in plasma: communication from the SSC of the ISTH. J Thromb Haemost 2014; 12 (11) 1932-1934
    CrossrefPubMedGoogle Scholar
  • 122 Vallier L, Bouriche T, Bonifay A. , et al. New specific and highly sensitive procoagulant test to measure tissue factor activity on microparticles. Res Pract Thromb Haemost Berlin 2017; 1: 1087
    PubMedGoogle Scholar
  • 123 Hisada Y, Mackman N. Measurement of tissue factor activity in extracellular vesicles from human plasma samples. Res Pr Thromb Haemost 2018; 3: 44-48
    PubMedGoogle Scholar
  • 124 Biró E, Sturk-Maquelin KN, Vogel GMT. , et al. Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost 2003; 1 (12) 2561-2568
    CrossrefPubMedGoogle Scholar
  • 125 Berckmans RJ, Sturk A, van Tienen LM, Schaap MC, Nieuwland R. Cell-derived vesicles exposing coagulant tissue factor in saliva. Blood 2011; 117 (11) 3172-3180
    CrossrefPubMedGoogle Scholar