Microparticles: Bridging the Gap between Autoimmunity and Thrombosis

 

 Buy Article Permissions and Reprints

Abstract

Microparticles (MPs) are irregularly shaped small vesicles of heterogeneous size released from the plasma membrane in a tightly controlled process, after different stimuli. MPs have been associated with proinflammatory effects and also with autoimmune processes, being a source of autoantigenic nuclear material, which can form immune complexes. In addition, recent reports have linked a large number of autoimmune disorders to an increased risk of thrombosis, and MPs seem to promote the potential for thrombotic events. A growing mass of evidence supports the idea that MPs could contribute to the generation of an inflammation-induced hypercoagulability state, having a relevant role in the pathogenesis of the thrombotic phenomena associated to autoimmune disease, such as systemic lupus erythematosus, antiphospholipid antibody syndrome, and systemic vasculitis. In this review, we focus on the procoagulant properties of circulating MPs and analyze their contribution to the pathogenesis of autoimmune diseases.

• References

• 1 Peck B, Hoffman GS, Franck WA. Thrombophlebitis in systemic lupus erythematosus. JAMA 1978; 240 (16) 1728-1730
  CrossrefPubMedGoogle Scholar
• 2 Palatinus A, Adams M. Thrombosis in systemic lupus erythematosus. Semin Thromb Hemost 2009; 35 (7) 621-629
  Article in Thieme ConnectPubMedGoogle Scholar
• 3 Di Fabio F, Lykoudis P, Gordon PH. Thromboembolism in inflammatory bowel disease: an insidious association requiring a high degree of vigilance. Semin Thromb Hemost 2011; 37 (3) 220-225
  Article in Thieme ConnectPubMedGoogle Scholar
• 4 Yazici H, Fresko I, Yurdakul S. Behçet's syndrome: disease manifestations, management, and advances in treatment. Nat Clin Pract Rheumatol 2007; 3 (3) 148-155
  CrossrefPubMedGoogle Scholar
• 5 Rahman P, Inman RD, El-Gabalawy H, Krause DO. Pathophysiology and pathogenesis of immune-mediated inflammatory diseases: commonalities and differences. J Rheumatol Suppl 2010; 85: 11-26
  CrossrefPubMedGoogle Scholar
• 6 Cunningham M, Marks N, Barnado A, Wirth JR, Gilkeson G, Markiewicz M. Are microparticles the missing link between thrombosis and autoimmune diseases? Involvement in selected rheumatologic diseases. Semin Thromb Hemost 2014; 40 (6) 675-681
  Article in Thieme ConnectPubMedGoogle Scholar
• 7 Mesri M, Altieri DC. Leukocyte microparticles stimulate endothelial cell cytokine release and tissue factor induction in a JNK1 signaling pathway. J Biol Chem 1999; 274 (33) 23111-23118
  CrossrefPubMedGoogle Scholar
• 8 Mesri M, Altieri DC. Endothelial cell activation by leukocyte microparticles. J Immunol 1998; 161 (8) 4382-4387
  PubMedGoogle Scholar
• 9 Sinauridze EI, Kireev DA, Popenko NY , et al. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost 2007; 97 (3) 425-434
  Article in Thieme ConnectPubMedGoogle Scholar
• 10 Ullal AJ, Reich III CF, Clowse M , et al. Microparticles as antigenic targets of antibodies to DNA and nucleosomes in systemic lupus erythematosus. J Autoimmun 2011; 36 (3–4) 173-180
  CrossrefPubMedGoogle Scholar
• 11 Morel O, Jesel L, Freyssinet JM, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol 2011; 31 (1) 15-26
  CrossrefPubMedGoogle Scholar
• 12 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
• 13 Lacroix R, Dignat-George F. Microparticles: new protagonists in pericellular and intravascular proteolysis. Semin Thromb Hemost 2013; 39 (1) 33-39
  Article in Thieme ConnectPubMedGoogle Scholar
• 14 Prakash PS, Caldwell CC, Lentsch AB, Pritts TA, Robinson BR. Human microparticles generated during sepsis in patients with critical illness are neutrophil-derived and modulate the immune response. J Trauma Acute Care Surg 2012; 73 (2) 401-406 , discussion 406–407
  CrossrefPubMedGoogle Scholar
• 15 Burnier L, Fontana P, Kwak BR, Angelillo-Scherrer A. Cell-derived microparticles in haemostasis and vascular medicine. Thromb Haemost 2009; 101 (3) 439-451
  PubMedGoogle Scholar
• 16 Smeets EF, Comfurius P, Bevers EM, Zwaal RF. Calcium-induced transbilayer scrambling of fluorescent phospholipid analogs in platelets and erythrocytes. Biochim Biophys Acta 1994; 1195 (2) 281-286
  CrossrefPubMedGoogle Scholar
• 17 Williamson P, Bevers EM, Smeets EF, Comfurius P, Schlegel RA, Zwaal RF. Continuous analysis of the mechanism of activated transbilayer lipid movement in platelets. Biochemistry 1995; 34 (33) 10448-10455
  CrossrefPubMedGoogle Scholar
• 18 Comfurius P, Williamson P, Smeets EF, Schlegel RA, Bevers EM, Zwaal RF. Reconstitution of phospholipid scramblase activity from human blood platelets. Biochemistry 1996; 35 (24) 7631-7634
  CrossrefPubMedGoogle Scholar
• 19 Diamant M, Tushuizen ME, Sturk A, Nieuwland R. Cellular microparticles: new players in the field of vascular disease?. Eur J Clin Invest 2004; 34 (6) 392-401
  CrossrefPubMedGoogle Scholar
• 20 Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006; 20 (9) 1487-1495
  CrossrefPubMedGoogle Scholar
• 21 Simak J, Gelderman MP. Cell membrane microparticles in blood and blood products: potentially pathogenic agents and diagnostic markers. Transfus Med Rev 2006; 20 (1) 1-26
  CrossrefPubMedGoogle Scholar
• 22 Herring JM, McMichael MA, Smith SA. Microparticles in health and disease. J Vet Intern Med 2013; 27 (5) 1020-1033
  CrossrefPubMedGoogle Scholar
• 23 Morel O, Toti F, Hugel B , et al. Procoagulant microparticles: disrupting the vascular homeostasis equation?. Arterioscler Thromb Vasc Biol 2006; 26 (12) 2594-2604
  CrossrefPubMedGoogle Scholar
• 24 Brill A, Dashevsky O, Rivo J, Gozal Y, Varon D. Platelet-derived microparticles induce angiogenesis and stimulate post-ischemic revascularization. Cardiovasc Res 2005; 67 (1) 30-38
  CrossrefPubMedGoogle Scholar
• 25 Mause SF, Weber C. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res 2010; 107 (9) 1047-1057
  CrossrefPubMedGoogle Scholar
• 26 Ratajczak J, Miekus K, Kucia M , et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006; 20 (5) 847-856
  CrossrefPubMedGoogle Scholar
• 27 Berckmans RJ, Nieuwland R, Böing AN, Romijn FP, Hack CE, Sturk A. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost 2001; 85 (4) 639-646
  PubMedGoogle Scholar
• 28 Greenwalt TJ. The how and why of exocytic vesicles. Transfusion 2006; 46 (1) 143-152
  CrossrefPubMedGoogle Scholar
• 29 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 (5) 1604-1611
  CrossrefPubMedGoogle Scholar
• 30 Puddu P, Puddu GM, Cravero E, Muscari S, Muscari A. The involvement of circulating microparticles in inflammation, coagulation and cardiovascular diseases. Can J Cardiol 2010; 26 (4) 140-145
  CrossrefPubMedGoogle Scholar
• 31 Boulanger CM, Scoazec A, Ebrahimian T , et al. Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation 2001; 104 (22) 2649-2652
  CrossrefPubMedGoogle Scholar
• 32 Amabile N, Guérin AP, Leroyer A , et al. Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J Am Soc Nephrol 2005; 16 (11) 3381-3388
  CrossrefPubMedGoogle Scholar
• 33 Feng B, Chen Y, Luo Y, Chen M, Li X, Ni Y. Circulating level of microparticles and their correlation with arterial elasticity and endothelium-dependent dilation in patients with type 2 diabetes mellitus. Atherosclerosis 2010; 208 (1) 264-269
  CrossrefPubMedGoogle Scholar
• 34 VanWijk MJ, Nieuwland R, Boer K, van der Post JA, VanBavel E, Sturk A. Microparticle subpopulations are increased in preeclampsia: possible involvement in vascular dysfunction?. Am J Obstet Gynecol 2002; 187 (2) 450-456
  CrossrefPubMedGoogle Scholar
• 35 Goubran HA, Stakiw J, Radosevic M, Burnouf T. Platelet-cancer interactions. Semin Thromb Hemost 2014; 40 (3) 296-305
  Article in Thieme ConnectPubMedGoogle Scholar
• 36 Chironi G, Simon A, Hugel B , et al. Circulating leukocyte-derived microparticles predict subclinical atherosclerosis burden in asymptomatic subjects. Arterioscler Thromb Vasc Biol 2006; 26 (12) 2775-2780
  CrossrefPubMedGoogle Scholar
• 37 Willekens FL, Werre JM, Kruijt JK , et al. Liver Kupffer cells rapidly remove red blood cell-derived vesicles from the circulation by scavenger receptors. Blood 2005; 105 (5) 2141-2145
  CrossrefPubMedGoogle Scholar
• 38 Rubin O, Crettaz D, Tissot JD, Lion N. Microparticles in stored red blood cells: submicron clotting bombs?. Blood Transfus 2010; 8 (Suppl. 03) s31-s38
  PubMedGoogle Scholar
• 39 Nantakomol D, Dondorp AM, Krudsood S , et al. Circulating red cell-derived microparticles in human malaria. J Infect Dis 2011; 203 (5) 700-706
  CrossrefPubMedGoogle Scholar
• 40 Donadee C, Raat NJ, Kanias T , et al. Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion. Circulation 2011; 124 (4) 465-476
  CrossrefPubMedGoogle Scholar
• 41 Kozuma Y, Sawahata Y, Takei Y, Chiba S, Ninomiya H. Procoagulant properties of microparticles released from red blood cells in paroxysmal nocturnal haemoglobinuria. Br J Haematol 2011; 152 (5) 631-639
  CrossrefPubMedGoogle Scholar
• 42 Wagner GM, Chiu DT, Yee MC, Lubin BH. Red cell vesiculation—a common membrane physiologic event. J Lab Clin Med 1986; 108 (4) 315-324
  PubMedGoogle Scholar
• 43 Greenwalt TJ, Bryan DJ, Dumaswala UJ. Erythrocyte membrane vesiculation and changes in membrane composition during storage in citrate-phosphate-dextrose-adenine-1. Vox Sang 1984; 47 (4) 261-270
  CrossrefPubMedGoogle Scholar
• 44 Pakala R. Serotonin and thromboxane A2 stimulate platelet-derived microparticle-induced smooth muscle cell proliferation. Cardiovasc Radiat Med 2004; 5 (1) 20-26
  CrossrefPubMedGoogle Scholar
• 45 Holme PA, Orvim U, Hamers MJ , et al. Shear-induced platelet activation and platelet microparticle formation at blood flow conditions as in arteries with a severe stenosis. Arterioscler Thromb Vasc Biol 1997; 17 (4) 646-653
  CrossrefPubMedGoogle Scholar
• 46 Miyazaki Y, Nomura S, Miyake T , et al. High shear stress can initiate both platelet aggregation and shedding of procoagulant containing microparticles. Blood 1996; 88 (9) 3456-3464
  PubMedGoogle Scholar
• 47 Nomura S, Nakamura T, Cone J, Tandon NN, Kambayashi J. Cytometric analysis of high shear-induced platelet microparticles and effect of cytokines on microparticle generation. Cytometry 2000; 40 (3) 173-181
  CrossrefPubMedGoogle Scholar
• 48 Barry OP, Pratico D, Lawson JA, FitzGerald GA. Transcellular activation of platelets and endothelial cells by bioactive lipids in platelet microparticles. J Clin Invest 1997; 99 (9) 2118-2127
  CrossrefPubMedGoogle Scholar
• 49 Miyamoto S, Marcinkiewicz C, Edmunds Jr LH, Niewiarowski S. Measurement of platelet microparticles during cardiopulmonary bypass by means of captured ELISA for GPIIb/IIIa. Thromb Haemost 1998; 80 (2) 225-230
  PubMedGoogle Scholar
• 50 Barry OP, FitzGerald GA. Mechanisms of cellular activation by platelet microparticles. Thromb Haemost 1999; 82 (2) 794-800
  PubMedGoogle Scholar
• 51 Barry OP, Praticò D, Savani RC, FitzGerald GA. Modulation of monocyte-endothelial cell interactions by platelet microparticles. J Clin Invest 1998; 102 (1) 136-144
  CrossrefPubMedGoogle Scholar
• 52 Forlow SB, McEver RP, Nollert MU. Leukocyte-leukocyte interactions mediated by platelet microparticles under flow. Blood 2000; 95 (4) 1317-1323
  PubMedGoogle Scholar
• 53 Brunetti M, Martelli N, Manarini S , et al. Polymorphonuclear leukocyte apoptosis is inhibited by platelet-released mediators, role of TGFbeta-1. Thromb Haemost 2000; 84 (3) 478-483
  PubMedGoogle Scholar
• 54 Barry OP, Kazanietz MG, Praticò D, FitzGerald GA. Arachidonic acid in platelet microparticles up-regulates cyclooxygenase-2-dependent prostaglandin formation via a protein kinase C/mitogen-activated protein kinase-dependent pathway. J Biol Chem 1999; 274 (11) 7545-7556
  CrossrefPubMedGoogle Scholar
• 55 Weber A, Köppen HO, Schrör K. Platelet-derived microparticles stimulate coronary artery smooth muscle cell mitogenesis by a PDGF-independent mechanism. Thromb Res 2000; 98 (5) 461-466
  CrossrefPubMedGoogle Scholar
• 56 Miyazono K, Okabe T, Urabe A, Yamanaka M, Takaku F. A platelet factor that stimulates the proliferation of vascular endothelial cells. Biochem Biophys Res Commun 1985; 126 (1) 83-88
  CrossrefPubMedGoogle Scholar
• 57 Baj-Krzyworzeka M, Majka M, Pratico D , et al. Platelet-derived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells. Exp Hematol 2002; 30 (5) 450-459
  CrossrefPubMedGoogle Scholar
• 58 Gruber R, Varga F, Fischer MB, Watzek G. Platelets stimulate proliferation of bone cells: involvement of platelet-derived growth factor, microparticles and membranes. Clin Oral Implants Res 2002; 13 (5) 529-535
  CrossrefPubMedGoogle Scholar
• 59 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
  PubMedGoogle Scholar
• 60 Siljander P, Carpen O, Lassila R. Platelet-derived microparticles associate with fibrin during thrombosis. Blood 1996; 87 (11) 4651-4663
  CrossrefPubMedGoogle Scholar
• 61 Nomura S, Tandon NN, Nakamura T, Cone J, Fukuhara S, Kambayashi J. High-shear-stress-induced activation of platelets and microparticles enhances expression of cell adhesion molecules in THP-1 and endothelial cells. Atherosclerosis 2001; 158 (2) 277-287
  CrossrefPubMedGoogle Scholar
• 62 Diehl P, Aleker M, Helbing T , et al. Increased platelet, leukocyte and endothelial microparticles predict enhanced coagulation and vascular inflammation in pulmonary hypertension. J Thromb Thrombolysis 2011; 31 (2) 173-179
  CrossrefPubMedGoogle Scholar
• 63 Lee YJ, Jy W, Horstman LL , et al. Elevated platelet microparticles in transient ischemic attacks, lacunar infarcts, and multiinfarct dementias. Thromb Res 1993; 72 (4) 295-304
  CrossrefPubMedGoogle Scholar
• 64 Chirinos JA, Heresi GA, Velasquez H , et al. Elevation of endothelial microparticles, platelets, and leukocyte activation in patients with venous thromboembolism. J Am Coll Cardiol 2005; 45 (9) 1467-1471
  CrossrefPubMedGoogle Scholar
• 65 Nieuwland R, Berckmans RJ, McGregor S , et al. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood 2000; 95 (3) 930-935
  PubMedGoogle Scholar
• 66 Jimenez JJ, Jy W, Mauro LM, Horstman LL, Ahn YS. Elevated endothelial microparticles in thrombotic thrombocytopenic purpura: findings from brain and renal microvascular cell culture and patients with active disease. Br J Haematol 2001; 112 (1) 81-90
  CrossrefPubMedGoogle Scholar
• 67 Geiser T, Sturzenegger M, Genewein U, Haeberli A, Beer JH. Mechanisms of cerebrovascular events as assessed by procoagulant activity, cerebral microemboli, and platelet microparticles in patients with prosthetic heart valves. Stroke 1998; 29 (9) 1770-1777
  CrossrefPubMedGoogle Scholar
• 68 Singh N, Gemmell CH, Daly PA, Yeo EL. Elevated platelet-derived microparticle levels during unstable angina. Can J Cardiol 1995; 11 (11) 1015-1021
  PubMedGoogle Scholar
• 69 Gawaz M, Neumann FJ, Ott I, Schiessler A, Schömig A. Platelet function in acute myocardial infarction treated with direct angioplasty. Circulation 1996; 93 (2) 229-237
  CrossrefPubMedGoogle Scholar
• 70 Nieuwland R, Berckmans RJ, Rotteveel-Eijkman RC , et al. Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation 1997; 96 (10) 3534-3541
  CrossrefPubMedGoogle Scholar
• 71 Gasser O, Schifferli JA. Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood 2004; 104 (8) 2543-2548
  CrossrefPubMedGoogle Scholar
• 72 Brodsky SV, Zhang F, Nasjletti A, Goligorsky MS. Endothelium-derived microparticles impair endothelial function in vitro. Am J Physiol Heart Circ Physiol 2004; 286 (5) H1910-H1915
  CrossrefPubMedGoogle Scholar
• 73 Dalli J, Norling LV, Renshaw D, Cooper D, Leung KY, Perretti M. Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood 2008; 112 (6) 2512-2519
  CrossrefPubMedGoogle Scholar
• 74 Pluskota E, Woody NM, Szpak D , et al. Expression, activation, and function of integrin alphaMbeta2 (Mac-1) on neutrophil-derived microparticles. Blood 2008; 112 (6) 2327-2335
  CrossrefPubMedGoogle Scholar
• 75 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 (3) 534-542
  CrossrefPubMedGoogle Scholar
• 76 Meziani F, Delabranche X, Asfar P, Toti F. Bench-to-bedside review: circulating microparticles—a new player in sepsis?. Crit Care 2010; 14 (5) 236
  CrossrefPubMedGoogle Scholar
• 77 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 (4) 1515-1522
  CrossrefPubMedGoogle Scholar
• 78 Aharon A, Tamari T, Brenner B. Monocyte-derived microparticles and exosomes induce procoagulant and apoptotic effects on endothelial cells. Thromb Haemost 2008; 100 (5) 878-885
  Article in Thieme ConnectPubMedGoogle Scholar
• 79 Poitevin S, Cochery-Nouvellon E, Dupont A, Nguyen P. Monocyte IL-10 produced in response to lipopolysaccharide modulates thrombin generation by inhibiting tissue factor expression and release of active tissue factor-bound microparticles. Thromb Haemost 2007; 97 (4) 598-607
  PubMedGoogle Scholar
• 80 Rauch U, Bonderman D, Bohrmann B , et al. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood 2000; 96 (1) 170-175
  PubMedGoogle Scholar
• 81 Wang JG, Williams JC, Davis BK , et al. Monocytic microparticles activate endothelial cells in an IL-1β-dependent manner. Blood 2011; 118 (8) 2366-2374
  CrossrefPubMedGoogle Scholar
• 82 Joop K, Berckmans RJ, Nieuwland R , et al. Microparticles from patients with multiple organ dysfunction syndrome and sepsis support coagulation through multiple mechanisms. Thromb Haemost 2001; 85 (5) 810-820
  PubMedGoogle Scholar
• 83 Matsumoto N, Nomura S, Kamihata H, Kimura Y, Iwasaka T. Increased level of oxidized LDL-dependent monocyte-derived microparticles in acute coronary syndrome. Thromb Haemost 2004; 91 (1) 146-154
  PubMedGoogle Scholar
• 84 Leroyer AS, Isobe H, Lesèche G , et al. Cellular origins and thrombogenic activity of microparticles isolated from human atherosclerotic plaques. J Am Coll Cardiol 2007; 49 (7) 772-777
  CrossrefPubMedGoogle Scholar
• 85 Fadok VA, Bratton DL, Frasch SC, Warner ML, Henson PM. The role of phosphatidylserine in recognition of apoptotic cells by phagocytes. Cell Death Differ 1998; 5 (7) 551-562
  CrossrefPubMedGoogle Scholar
• 86 Mallat Z, Hugel B, Ohan J, Lesèche G, Freyssinet JM, Tedgui A. Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity. Circulation 1999; 99 (3) 348-353
  CrossrefPubMedGoogle Scholar
• 87 Baka Z, Senolt L, Vencovsky J , et al. Increased serum concentration of immune cell derived microparticles in polymyositis/dermatomyositis. Immunol Lett 2010; 128 (2) 124-130
  CrossrefPubMedGoogle Scholar
• 88 Brogan PA, Shah V, Brachet C , et al. Endothelial and platelet microparticles in vasculitis of the young. Arthritis Rheum 2004; 50 (3) 927-936
  CrossrefPubMedGoogle Scholar
• 89 Ardoin SP, Shanahan JC, Pisetsky DS. The role of microparticles in inflammation and thrombosis. Scand J Immunol 2007; 66 (2-3) 159-165
  CrossrefPubMedGoogle Scholar
• 90 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
• 91 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 (7) 2432-2439
  CrossrefPubMedGoogle Scholar
• 92 Werner N, Wassmann S, Ahlers P, Kosiol S, Nickenig G. Circulating CD31+/annexin V+ apoptotic microparticles correlate with coronary endothelial function in patients with coronary artery disease. Arterioscler Thromb Vasc Biol 2006; 26 (1) 112-116
  CrossrefPubMedGoogle Scholar
• 93 Nozaki T, Sugiyama S, Koga H , et al. Significance of a multiple biomarkers strategy including endothelial dysfunction to improve risk stratification for cardiovascular events in patients at high risk for coronary heart disease. J Am Coll Cardiol 2009; 54 (7) 601-608
  CrossrefPubMedGoogle Scholar
• 94 Sinning JM, Losch J, Walenta K, Böhm M, Nickenig G, Werner N. Circulating CD31+/Annexin V+ microparticles correlate with cardiovascular outcomes. Eur Heart J 2011; 32 (16) 2034-2041
  CrossrefPubMedGoogle Scholar
• 95 Amabile N, Boulanger CM. Circulating microparticle levels in patients with coronary artery disease: a new indicator of vulnerability?. Eur Heart J 2011; 32 (16) 1958-1960
  CrossrefPubMedGoogle Scholar
• 96 Cherian P, Hankey GJ, Eikelboom JW , et al. Endothelial and platelet activation in acute ischemic stroke and its etiological subtypes. Stroke 2003; 34 (9) 2132-2137
  CrossrefPubMedGoogle Scholar
• 97 Williams JB, Jauch EC, Lindsell CJ, Campos B. Endothelial microparticle levels are similar in acute ischemic stroke and stroke mimics due to activation and not apoptosis/necrosis. Acad Emerg Med 2007; 14 (8) 685-690
  CrossrefPubMedGoogle Scholar
• 98 Simak J, Gelderman MP, Yu H, Wright V, Baird AE. Circulating endothelial microparticles in acute ischemic stroke: a link to severity, lesion volume and outcome. J Thromb Haemost 2006; 4 (6) 1296-1302
  CrossrefPubMedGoogle Scholar
• 99 Preston RA, Jy W, Jimenez JJ , et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 2003; 41 (2) 211-217
  CrossrefPubMedGoogle Scholar
• 100 Jimenez JJ, Jy W, Mauro LM, Horstman LL, Bidot CJ, Ahn YS. Endothelial microparticles (EMP) as vascular disease markers. Adv Clin Chem 2005; 39: 131-157
  PubMedGoogle Scholar
• 101 Agouni A, Lagrue-Lak-Hal AH, Ducluzeau PH , et al. Endothelial dysfunction caused by circulating microparticles from patients with metabolic syndrome. Am J Pathol 2008; 173 (4) 1210-1219
  CrossrefPubMedGoogle Scholar
• 102 Martin S, Tesse A, Hugel B , et al. Shed membrane particles from T lymphocytes impair endothelial function and regulate endothelial protein expression. Circulation 2004; 109 (13) 1653-1659
  CrossrefPubMedGoogle Scholar
• 103 Helal O, Defoort C, Robert S , et al. Increased levels of microparticles originating from endothelial cells, platelets and erythrocytes in subjects with metabolic syndrome: relationship with oxidative stress. Nutr Metab Cardiovasc Dis 2011; 21 (9) 665-671
  CrossrefPubMedGoogle Scholar
• 104 Sabatier F, Camoin-Jau L, Anfosso F, Sampol J, Dignat-George F. Circulating endothelial cells, microparticles and progenitors: key players towards the definition of vascular competence. J Cell Mol Med 2009; 13 (3) 454-471
  CrossrefPubMedGoogle Scholar
• 105 Morel O, Toti F, Morel N, Freyssinet JM. Microparticles in endothelial cell and vascular homeostasis: are they really noxious?. Haematologica 2009; 94 (3) 313-317
  CrossrefPubMedGoogle Scholar
• 106 Combes V, Taylor TE, Juhan-Vague I , et al. Circulating endothelial microparticles in malawian children with severe falciparum malaria complicated with coma. JAMA 2004; 291 (21) 2542-2544
  PubMedGoogle Scholar
• 107 Meziani F, Tesse A, David E , et al. Shed membrane particles from preeclamptic women generate vascular wall inflammation and blunt vascular contractility. Am J Pathol 2006; 169 (4) 1473-1483
  CrossrefPubMedGoogle Scholar
• 108 Takahashi T, Kubo H, Fujino N , et al. Surgical stress increases circulating endothelial microparticles in the elderly. Anaesth Intensive Care 2012; 40 (5) 899-902
  PubMedGoogle Scholar
• 109 Gordon C, Gudi K, Krause A , et al. Circulating endothelial microparticles as a measure of early lung destruction in cigarette smokers. Am J Respir Crit Care Med 2011; 184 (2) 224-232
  CrossrefPubMedGoogle Scholar
• 110 Densmore JC, Signorino PR, Ou J , et al. Endothelium-derived microparticles induce endothelial dysfunction and acute lung injury. Shock 2006; 26 (5) 464-471
  CrossrefPubMedGoogle Scholar
• 111 Ramagopalan SV, Wotton CJ, Handel AE, Yeates D, Goldacre MJ. Risk of venous thromboembolism in people admitted to hospital with selected immune-mediated diseases: record-linkage study. BMC Med 2011; 9: 1
  CrossrefPubMedGoogle Scholar
• 112 Zöller B, Li X, Sundquist J, Sundquist K. Risk of pulmonary embolism in patients with autoimmune disorders: a nationwide follow-up study from Sweden. Lancet 2012; 379 (9812) 244-249
  CrossrefPubMedGoogle Scholar
• 113 Pisetsky DS, Lipsky PE. Microparticles as autoadjuvants in the pathogenesis of SLE. Nat Rev Rheumatol 2010; 6 (6) 368-372
  CrossrefPubMedGoogle Scholar
• 114 Combes V, Simon AC, Grau GE , et al. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J Clin Invest 1999; 104 (1) 93-102
  CrossrefPubMedGoogle Scholar
• 115 Owens III AP, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res 2011; 108 (10) 1284-1297
  CrossrefPubMedGoogle Scholar
• 116 van Beers EJ, Schaap MC, Berckmans RJ , et al; CURAMA study group. Circulating erythrocyte-derived microparticles are associated with coagulation activation in sickle cell disease. Haematologica 2009; 94 (11) 1513-1519
  CrossrefPubMedGoogle Scholar
• 117 Van Der Meijden PE, 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 (7) 1355-1362
  CrossrefPubMedGoogle Scholar
• 118 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 (8) 1744-1754
  CrossrefPubMedGoogle Scholar
• 119 Osterud B, Olsen JO, Bjørklid E. What is blood borne tissue factor?. Thromb Res 2009; 124 (5) 640-641
  CrossrefPubMedGoogle Scholar
• 120 Butenas S, Orfeo T, Mann KG. Tissue factor in coagulation: Which? Where? When?. Arterioscler Thromb Vasc Biol 2009; 29 (12) 1989-1996
  CrossrefPubMedGoogle Scholar
• 121 Bach RR. Tissue factor encryption. Arterioscler Thromb Vasc Biol 2006; 26 (3) 456-461
  CrossrefPubMedGoogle Scholar
• 122 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
  CrossrefPubMedGoogle Scholar
• 123 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
• 124 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 (3) 1208-1216
  CrossrefPubMedGoogle Scholar
• 125 Patel KD, Zimmerman GA, Prescott SM, McIntyre TM. Novel leukocyte agonists are released by endothelial cells exposed to peroxide. J Biol Chem 1992; 267 (21) 15168-15175
  CrossrefPubMedGoogle Scholar
• 126 MacKenzie A, Wilson HL, Kiss-Toth E, Dower SK, North RA, Surprenant A. Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 2001; 15 (5) 825-835
  CrossrefPubMedGoogle Scholar
• 127 Berda-Haddad Y, Robert S, Salers P , et al. Sterile inflammation of endothelial cell-derived apoptotic bodies is mediated by interleukin-1α. Proc Natl Acad Sci U S A 2011; 108 (51) 20684-20689
  CrossrefPubMedGoogle Scholar
• 128 Aksu K, Donmez A, Keser G. Inflammation-induced thrombosis: mechanisms, disease associations and management. Curr Pharm Des 2012; 18 (11) 1478-1493
  CrossrefPubMedGoogle Scholar
• 129 Distler JH, Jüngel A, Huber LC , et al. The induction of matrix metalloproteinase and cytokine expression in synovial fibroblasts stimulated with immune cell microparticles. Proc Natl Acad Sci U S A 2005; 102 (8) 2892-2897
  CrossrefPubMedGoogle Scholar
• 130 Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med 2008; 358 (9) 929-939
  CrossrefPubMedGoogle Scholar
• 131 Tsokos GC. Systemic lupus erythematosus. N Engl J Med 2011; 365 (22) 2110-2121
  CrossrefPubMedGoogle Scholar
• 132 Nielsen CT, Østergaard O, Johnsen C, Jacobsen S, Heegaard NH. Distinct features of circulating microparticles and their relationship to clinical manifestations in systemic lupus erythematosus. Arthritis Rheum 2011; 63 (10) 3067-3077
  CrossrefPubMedGoogle Scholar
• 133 Nielsen CT, Østergaard O, Stener L , et al. Increased IgG on cell-derived plasma microparticles in systemic lupus erythematosus is associated with autoantibodies and complement activation. Arthritis Rheum 2012; 64 (4) 1227-1236
  CrossrefPubMedGoogle Scholar
• 134 Ruiz-Irastorza G, Khamashta MA, Castellino G, Hughes GR. Systemic lupus erythematosus. Lancet 2001; 357 (9261) 1027-1032
  CrossrefPubMedGoogle Scholar
• 135 Esdaile JM, Abrahamowicz M, Grodzicky T , et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2001; 44 (10) 2331-2337
  CrossrefPubMedGoogle Scholar
• 136 Pereira J, Alfaro G, Goycoolea M , et al. Circulating platelet-derived microparticles in systemic lupus erythematosus. Association with increased thrombin generation and procoagulant state. Thromb Haemost 2006; 95 (1) 94-99
  PubMedGoogle Scholar
• 137 Parker B, Al-Husain A, Pemberton P , et al. Suppression of inflammation reduces endothelial microparticles in active systemic lupus erythematosus. Ann Rheum Dis 2014; 73 (6) 1144-1150
  PubMedGoogle Scholar
• 138 Miyakis S, Lockshin MD, Atsumi T , et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 2006; 4 (2) 295-306
  CrossrefPubMedGoogle Scholar
• 139 McNeil HP, Simpson RJ, Chesterman CN, Krilis SA. Anti-phospholipid antibodies are directed against a complex antigen that includes a lipid-binding inhibitor of coagulation: beta 2-glycoprotein I (apolipoprotein H). Proc Natl Acad Sci U S A 1990; 87 (11) 4120-4124
  CrossrefPubMedGoogle Scholar
• 140 de Groot PG, Urbanus RT. The significance of autoantibodies against β2-glycoprotein I. Blood 2012; 120 (2) 266-274
  CrossrefPubMedGoogle Scholar
• 141 Del Papa N, Sheng YH, Raschi E , et al. Human beta 2-glycoprotein I binds to endothelial cells through a cluster of lysine residues that are critical for anionic phospholipid binding and offers epitopes for anti-beta 2-glycoprotein I antibodies. J Immunol 1998; 160 (11) 5572-5578
  PubMedGoogle Scholar
• 142 Giannakopoulos B, Passam F, Rahgozar S, Krilis SA. Current concepts on the pathogenesis of the antiphospholipid syndrome. Blood 2007; 109 (2) 422-430
  CrossrefPubMedGoogle Scholar
• 143 Pierangeli SS, Chen PP, Raschi E , et al. Antiphospholipid antibodies and the antiphospholipid syndrome: pathogenic mechanisms. Semin Thromb Hemost 2008; 34 (3) 236-250
  Article in Thieme ConnectPubMedGoogle Scholar
• 144 Simantov R, LaSala JM, Lo SK , et al. Activation of cultured vascular endothelial cells by antiphospholipid antibodies. J Clin Invest 1995; 96 (5) 2211-2219
  CrossrefPubMedGoogle Scholar
• 145 Pierangeli SS, Espinola RG, Liu X, Harris EN. Thrombogenic effects of antiphospholipid antibodies are mediated by intercellular cell adhesion molecule-1, vascular cell adhesion molecule-1, and P-selectin. Circ Res 2001; 88 (2) 245-250
  CrossrefPubMedGoogle Scholar
• 146 Simantov R, Lo SK, Gharavi A, Sammaritano LR, Salmon JE, Silverstein RL. Antiphospholipid antibodies activate vascular endothelial cells. Lupus 1996; 5 (5) 440-441
  PubMedGoogle Scholar
• 147 Branch DW, Rodgers GM. Induction of endothelial cell tissue factor activity by sera from patients with antiphospholipid syndrome: a possible mechanism of thrombosis. Am J Obstet Gynecol 1993; 168 (1 Pt 1) 206-210
  CrossrefPubMedGoogle Scholar
• 148 Dignat-George F, Camoin-Jau L, Sabatier F , et al. Endothelial microparticles: a potential contribution to the thrombotic complications of the antiphospholipid syndrome. Thromb Haemost 2004; 91 (4) 667-673
  Article in Thieme ConnectPubMedGoogle Scholar
• 149 Jy W, Tiede M, Bidot CJ , et al. Platelet activation rather than endothelial injury identifies risk of thrombosis in subjects positive for antiphospholipid antibodies. Thromb Res 2007; 121 (3) 319-325
  CrossrefPubMedGoogle Scholar
• 150 Brogan PA, Dillon MJ. Vasculitis from the pediatric perspective. Curr Rheumatol Rep 2000; 2 (5) 411-416
  CrossrefPubMedGoogle Scholar
• 151 Sundy JS, Haynes BF. Cytokines and adhesion molecules in the pathogenesis of vasculitis. Curr Rheumatol Rep 2000; 2 (5) 402-410
  CrossrefPubMedGoogle Scholar
• 152 Erdbruegger U, Grossheim M, Hertel B , et al. Diagnostic role of endothelial microparticles in vasculitis. Rheumatology (Oxford) 2008; 47 (12) 1820-1825
  CrossrefPubMedGoogle Scholar
• 153 Daniel L, Fakhouri F, Joly D , et al. Increase of circulating neutrophil and platelet microparticles during acute vasculitis and hemodialysis. Kidney Int 2006; 69 (8) 1416-1423
  CrossrefPubMedGoogle Scholar
• 154 Leroyer AS, Anfosso F, Lacroix R , et al. Endothelial-derived microparticles: biological conveyors at the crossroad of inflammation, thrombosis and angiogenesis. Thromb Haemost 2010; 104 (3) 456-463
  Article in Thieme ConnectPubMedGoogle Scholar
• 155 Hong Y, Eleftheriou D, Hussain AA , et al. Anti-neutrophil cytoplasmic antibodies stimulate release of neutrophil microparticles. J Am Soc Nephrol 2012; 23 (1) 49-62
  CrossrefPubMedGoogle Scholar
• 156 Uriarte SM, Rane MJ, Merchant ML , et al. Inhibition of neutrophil exocytosis ameliorates acute lung injury in rats. Shock 2013; 39 (3) 286-292
  CrossrefPubMedGoogle Scholar
• 157 Nicholls SJ, Hazen SL. Myeloperoxidase, modified lipoproteins, and atherogenesis. J Lipid Res 2009; 50 (Suppl): S346-S351
  PubMedGoogle Scholar
• 158 Pitanga TN, de Aragão França L, Rocha VC , et al. Neutrophil-derived microparticles induce myeloperoxidase-mediated damage of vascular endothelial cells. BMC Cell Biol 2014; 15: 21
  CrossrefPubMedGoogle Scholar
• 159 Stassen PM, Derks RP, Kallenberg CG, Stegeman CA. Venous thromboembolism in ANCA-associated vasculitis—incidence and risk factors. Rheumatology (Oxford) 2008; 47 (4) 530-534
  CrossrefPubMedGoogle Scholar
• 160 Tomasson G, Monach PA, Merkel PA. Thromboembolic disease in vasculitis. Curr Opin Rheumatol 2009; 21 (1) 41-46
  CrossrefPubMedGoogle Scholar
• 161 Clarke LA, Hong Y, Eleftheriou D , et al. Endothelial injury and repair in systemic vasculitis of the young. Arthritis Rheum 2010; 62 (6) 1770-1780
  CrossrefPubMedGoogle Scholar
• 162 Woywodt A, Streiber F, de Groot K, Regelsberger H, Haller H, Haubitz M. Circulating endothelial cells as markers for ANCA-associated small-vessel vasculitis. Lancet 2003; 361 (9353) 206-210
  CrossrefPubMedGoogle Scholar
• 163 Berden AE, Nolan SL, Morris HL , et al. Anti-plasminogen antibodies compromise fibrinolysis and associate with renal histology in ANCA-associated vasculitis. J Am Soc Nephrol 2010; 21 (12) 2169-2179
  CrossrefPubMedGoogle Scholar
• 164 Marshall SE. Behçet's disease. Best Pract Res Clin Rheumatol 2004; 18 (3) 291-311
  CrossrefPubMedGoogle Scholar
• 165 Ames PR, Steuer A, Pap A, Denman AM. Thrombosis in Behçet's disease: a retrospective survey from a single UK centre. Rheumatology (Oxford) 2001; 40 (6) 652-655
  CrossrefPubMedGoogle Scholar
• 166 Macey M, Hagi-Pavli E, Stewart J , et al. Age, gender and disease-related platelet and neutrophil activation ex vivo in whole blood samples from patients with Behçet's disease. Rheumatology (Oxford) 2011; 50 (10) 1849-1859
  CrossrefPubMedGoogle Scholar