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DOI: 10.1055/s-0041-1727111
Microparticles: An Alternative Explanation to the Behavior of Vascular Antiphospholipid Syndrome
Funding This study was supported by Minciencias, Colombia (Grant no. 111580762949).![](https://www.thieme-connect.de/media/sth/202107/lookinside/thumbnails/10-1055-s-0041-1727111_02852-1.jpg)
Abstract
Antiphospholipid syndrome is an autoimmune disease characterized by the persistent presence of antiphospholipid antibodies, along with occurrence of vascular thrombosis and pregnancy morbidity. The variety of antiphospholipid antibodies and their related mechanisms, as well as the behavior of disease in wide groups of patients, have led some authors to propose a differentiation of this syndrome into two independent entities: vascular and obstetric antiphospholipid syndrome. Thus, previous studies have discussed whether specific autoantibodies may be responsible for this differentiation or, in contrast, how the same antibodies are able to generate two different clinical presentations. This discussion is yet to be settled. The capability of serum IgG from patients with vascular thrombosis to trigger the biogenesis of endothelial cell-derived microparticles in vitro is one of the previously discussed differences between the clinical entities of antiphospholipid syndrome. These vesicles constitute a prothrombotic mechanism as they can directly lead to clot activation in murine models and recalcified human plasma. Nevertheless, other indirect mechanisms by which microparticles can spread a procoagulant phenotype could be critical to understanding their role in antiphospholipid syndrome. For this reason, questions regarding the cargo of microparticles, and the signaling pathways involved in their biogenesis, are of interest in attempting to explain the behavior of this autoimmune disease.
Keywords
antiphospholipid syndrome - antiphospholipid antibodies - cell-derived microparticles - thrombosis - blood coagulation disordersAuthors' Contributions
Á.P.C.J. and D.Á. proposed the main topic of this review; D.Á. prepared the draft copy of the manuscript; and C.R. and Á.P.C.J. critically assessed and evaluated the writing process.
Publication History
Article published online:
30 April 2021
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References
- 1 Chargaff E, West R. The biological significance of the thromboplastic protein of blood. J Biol Chem 1946; 166 (01) 189-197
- 2 Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967; 13 (03) 269-288
- 3 Dvorak HF, Quay SC, Orenstein NS. et al. Tumor shedding and coagulation. Science 1981; 212 (4497): 923-924
- 4 Pardo F, Villalobos-Labra R, Sobrevia B, Toledo F, Sobrevia L. Extracellular vesicles in obesity and diabetes mellitus. Mol Aspects Med 2018; 60: 81-91
- 5 Burbano C, Rojas M, Muñoz-Vahos C. et al. Extracellular vesicles are associated with the systemic inflammation of patients with seropositive rheumatoid arthritis. Sci Rep 2018; 8 (01) 17917
- 6 Atehortúa L, Rojas M, Vásquez G. et al. Endothelial activation and injury by microparticles in patients with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Res Ther 2019; 21 (01) 34
- 7 Cicarini WB, Ferreira KS, Loures CMG. et al. Systemic lupus erythematosus: disease activity may influence the release of endothelial microparticles?. Blood Coagul Fibrinolysis 2018; 29 (02) 189-195
- 8 Chaturvedi S, Alluri R, McCrae KR. Extracellular vesicles in the antiphospholipid syndrome. Semin Thromb Hemost 2018; 44 (05) 493-504
- 9 Pericleous C, Clarke LA, Brogan PA. et al. Endothelial microparticle release is stimulated in vitro by purified IgG from patients with the antiphospholipid syndrome. Thromb Haemost 2013; 109 (01) 72-78
- 10 Alijotas-Reig J, Esteve-Valverde E, Ferrer-Oliveras R. et al; EUROAPS Study Group. The European Registry on Obstetric Antiphospholipid Syndrome (EUROAPS): a survey of 1000 consecutive cases. Autoimmun Rev 2019; 18 (04) 406-414
- 11 Meroni PL, Borghi MO, Grossi C, Chighizola CB, Durigutto P, Tedesco F. Obstetric and vascular antiphospholipid syndrome: same antibodies but different diseases?. Nat Rev Rheumatol 2018; 14 (07) 433-440
- 12 Poulton K, Ripoll VM, Pericleous C. et al. Purified IgG from patients with obstetric but not IgG from non-obstetric antiphospholipid syndrome inhibit trophoblast invasion. Am J Reprod Immunol 2015; 73 (05) 390-401
- 13 Lambrianides A, Carroll CJ, Pierangeli SS. et al. Effects of polyclonal IgG derived from patients with different clinical types of the antiphospholipid syndrome on monocyte signaling pathways. J Immunol 2010; 184 (12) 6622-6628
- 14 Fischetti F, Durigutto P, Pellis V. et al. Thrombus formation induced by antibodies to β2-glycoprotein I is complement dependent and requires a priming factor. Blood 2005; 106 (07) 2340-2346
- 15 Ye R, Ye C, Huang Y, Liu L, Wang S. Circulating tissue factor positive microparticles in patients with acute recurrent deep venous thrombosis. Thromb Res 2012; 130 (02) 253-258
- 16 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
- 17 Bucciarelli P, Martinelli I, Artoni A. et al. Circulating microparticles and risk of venous thromboembolism. Thromb Res 2012; 129 (05) 591-597
- 18 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
- 19 Breen KA, Sanchez K, Kirkman N. et al. Endothelial and platelet microparticles in patients with antiphospholipid antibodies. Thromb Res 2015; 135 (02) 368-374
- 20 Willemze R, Bradford RL, Mooberry MJ, Roubey RAS, Key NS. Plasma microparticle tissue factor activity in patients with antiphospholipid antibodies with and without clinical complications. Thromb Res 2014; 133 (02) 187-189
- 21 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 (04) 667-673
- 22 Vikerfors A, Mobarrez F, Bremme K. et al. Studies of microparticles in patients with the antiphospholipid syndrome (APS). Lupus 2012; 21 (07) 802-805
- 23 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 (02) 295-306
- 24 Tektonidou MG, Andreoli L, Limper M. et al. EULAR recommendations for the management of antiphospholipid syndrome in adults. Ann Rheum Dis 2019; 78 (10) 1296-1304
- 25 von Landenberg C, Lackner KJ, von Landenberg P, Lang B, Schmitz G. Isolation and characterization of two human monoclonal anti-phospholipid IgG from patients with autoimmune disease. J Autoimmun 1999; 13 (02) 215-223
- 26 Durigutto P, Grossi C, Borghi MO. et al. New insight into antiphospholipid syndrome: antibodies to β2 glycoprotein I-domain 5 fail to induce thrombi in rats. Haematologica 2019; 104 (04) 819-826
- 27 Litvinova E, Darnige L, Kirilovsky A, Burnel Y, de Luna G, Dragon-Durey M-A. Prevalence and significance of non-conventional antiphospholipid antibodies in patients with clinical APS criteria. Front Immunol 2018; 9: 2971
- 28 Alessandri C, Agmon-Levin N, Conti F. et al. Anti-mutated citrullinated vimentin antibodies in antiphospholipid syndrome: diagnostic value and relationship with clinical features. Immunol Res 2017; 65 (02) 524-531
- 29 Rodríguez-García V, Ioannou Y, Fernández-Nebro A, Isenberg DA, Giles IP. Examining the prevalence of non-criteria anti-phospholipid antibodies in patients with anti-phospholipid syndrome: a systematic review. Rheumatology (Oxford) 2015; 54 (11) 2042-2050
- 30 Žigon P, Podovšovnik A, Ambrožič A. et al. Added value of non-criteria antiphospholipid antibodies for antiphospholipid syndrome: lessons learned from year-long routine measurements. Clin Rheumatol 2019; 38 (02) 371-378
- 31 Zohoury N, Bertolaccini ML, Rodriguez-Garcia JL. et al. Closing the serological gap in the antiphospholipid syndrome: the value of “non-criteria” antiphospholipid antibodies. J Rheumatol 2017; 44 (11) 1597-1602
- 32 de Groot PG, Urbanus RT. Antiphospholipid syndrome--not a noninflammatory disease. Semin Thromb Hemost 2015; 41 (06) 607-614
- 33 Hollerbach A, Müller-Calleja N, Ritter S. et al. Platelet activation by antiphospholipid antibodies depends on epitope specificity and is prevented by mTOR inhibitors. Thromb Haemost 2019; 119 (07) 1147-1153
- 34 Müller-Calleja N, Hollerbach A, Häuser F, Canisius A, Orning C, Lackner KJ. Antiphospholipid antibody-induced cellular responses depend on epitope specificity: implications for treatment of antiphospholipid syndrome. J Thromb Haemost 2017; 15 (12) 2367-2376
- 35 Drozidinsky G, Hadar E, Shmueli A, Gabbay-Benziv R, Shiber S. Obstetric antiphospholipid syndrome and long term arterial thrombosis risk. J Thromb Thrombolysis 2017; 44 (03) 371-375
- 36 Out HJ, Kooijman CD, Bruinse HW, Derksen RHWM. Histopathological findings in placentae from patients with intra-uterine fetal death and anti-phospholipid antibodies. Eur J Obstet Gynecol Reprod Biol 1991; 41 (03) 179-186
- 37 Girardi G, Berman J, Redecha P. et al. Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J Clin Invest 2003; 112 (11) 1644-1654
- 38 Girardi G, Redecha P, Salmon JE. Heparin prevents antiphospholipid antibody-induced fetal loss by inhibiting complement activation. Nat Med 2004; 10 (11) 1222-1226
- 39 Agostinis C, Durigutto P, Sblattero D. et al. A non-complement-fixing antibody to β2 glycoprotein I as a novel therapy for antiphospholipid syndrome. Blood 2014; 123 (22) 3478-3487
- 40 Agostinis C, Biffi S, Garrovo C. et al. In vivo distribution of β2 glycoprotein I under various pathophysiologic conditions. Blood 2011; 118 (15) 4231-4238
- 41 Chighizola CB, Raimondo MG, Comerio C. et al. The risk of obstetric complications and the effects of treatment in women with low titer and medium-high titer anti-phospholipid antibodies. 2017 . Accessed May 8, 2020 at: https://acrabstracts.org/abstract/the-risk-of-obstetric-complications-and-the-effects-of-treatment-in-women-with-low-titer-and-medium-high-titer-anti-phospholipid-antibodies/
- 42 Lippi G, Adcock D, Favaloro EJ. Understanding the “philosophy” of laboratory hemostasis. Diagnosis (Berl) 2019; 6 (03) 223-226
- 43 Bu C, Gao L, Xie W. et al. β2-glycoprotein i is a cofactor for tissue plasminogen activator-mediated plasminogen activation. Arthritis Rheum 2009; 60 (02) 559-568
- 44 Kremers RMW, Zuily S, Kelchtermans H. et al. Prothrombin conversion is accelerated in the antiphospholipid syndrome and insensitive to thrombomodulin. Blood Adv 2018; 2 (11) 1315-1324
- 45 Ramesh S, Morrell CN, Tarango C. et al. Antiphospholipid antibodies promote leukocyte-endothelial cell adhesion and thrombosis in mice by antagonizing eNOS via β2GPI and apoER2. J Clin Invest 2011; 121 (01) 120-131
- 46 Rand JH, Wu XX, Quinn AS. et al. Human monoclonal antiphospholipid antibodies disrupt the annexin A5 anticoagulant crystal shield on phospholipid bilayers: evidence from atomic force microscopy and functional assay. Am J Pathol 2003; 163 (03) 1193-1200
- 47 Shibata S, Harpel PC, Gharavi A, Rand J, Fillit H. Autoantibodies to heparin from patients with antiphospholipid antibody syndrome inhibit formation of antithrombin III-thrombin complexes. Blood 1994; 83 (09) 2532-2540
- 48 de Laat B, Eckmann CM, van Schagen M, Meijer AB, Mertens K, van Mourik JA. Correlation between the potency of a beta2-glycoprotein I-dependent lupus anticoagulant and the level of resistance to activated protein C. Blood Coagul Fibrinolysis 2008; 19 (08) 757-764
- 49 Prinz N, Clemens N, Canisius A, Lackner KJ. Endosomal NADPH-oxidase is critical for induction of the tissue factor gene in monocytes and endothelial cells. Lessons from the antiphospholipid syndrome. Thromb Haemost 2013; 109 (03) 525-531
- 50 Prinz N, Clemens N, Strand D. et al. Antiphospholipid antibodies induce translocation of TLR7 and TLR8 to the endosome in human monocytes and plasmacytoid dendritic cells. Blood 2011; 118 (08) 2322-2332
- 51 Pennings MTT, van Lummel M, Derksen RHWM. et al. Interaction of β2-glycoprotein I with members of the low density lipoprotein receptor family. J Thromb Haemost 2006; 4 (08) 1680-1690
- 52 Raschi E, Chighizola CB, Grossi C. et al. β2-Glycoprotein I, lipopolysaccharide and endothelial TLR4: three players in the two hit theory for anti-phospholipid-mediated thrombosis. J Autoimmun 2014; 55 (01) 42-50
- 53 Colasanti T, Alessandri C, Capozzi A. et al. Autoantibodies specific to a peptide of β2-glycoprotein I cross-react with TLR4, inducing a proinflammatory phenotype in endothelial cells and monocytes. Blood 2012; 120 (16) 3360-3370
- 54 Sorice M, Longo A, Capozzi A. et al. Anti-β2-glycoprotein I antibodies induce monocyte release of tumor necrosis factor α and tissue factor by signal transduction pathways involving lipid rafts. Arthritis Rheum 2007; 56 (08) 2687-2697
- 55 Xia L, Zhou H, Wang T. et al. Activation of mTOR is involved in anti-β2GPI/β2GPI-induced expression of tissue factor and IL-8 in monocytes. Thromb Res 2017; 157: 103-110
- 56 López-Pedrera C, Buendía P, Cuadrado MJ. et al. Antiphospholipid antibodies from patients with the antiphospholipid syndrome induce monocyte tissue factor expression through the simultaneous activation of NF-kappaB/Rel proteins via the p38 mitogen-activated protein kinase pathway, and of the MEK-1/ERK pathway. Arthritis Rheum 2006; 54 (01) 301-311
- 57 Pennings MTT, Derksen RHWM, van Lummel M. et al. Platelet adhesion to dimeric β-glycoprotein I under conditions of flow is mediated by at least two receptors: glycoprotein Ibalpha and apolipoprotein E receptor 2′. J Thromb Haemost 2007; 5 (02) 369-377
- 58 Zhang W, Gao F, Lu D. et al. Anti-β2 glycoprotein I antibodies in complex with β2 glycoprotein I induce platelet activation via two receptors: apolipoprotein E receptor 2′ and glycoprotein I bα. Front Med 2016; 10 (01) 76-84
- 59 Vega-Ostertag M, Harris EN, Pierangeli SS. Intracellular events in platelet activation induced by antiphospholipid antibodies in the presence of low doses of thrombin. Arthritis Rheum 2004; 50 (09) 2911-2919
- 60 Allen KL, Fonseca FV, Betapudi V, Willard B, Zhang J, McCrae KR. A novel pathway for human endothelial cell activation by antiphospholipid/anti-β2 glycoprotein I antibodies. Blood 2012; 119 (03) 884-893
- 61 Wang M, Kong X, Xie Y, He C, Wang T, Zhou H. Role of TLR-4 in anti-β2-glycoprotein I-induced activation of peritoneal macrophages and vascular endothelial cells in mice. Mol Med Rep 2019; 19 (05) 4353-4363
- 62 Vega-Ostertag ME, Ferrara DE, Romay-Penabad Z. et al. Role of p38 mitogen-activated protein kinase in antiphospholipid antibody-mediated thrombosis and endothelial cell activation. J Thromb Haemost 2007; 5 (09) 1828-1834
- 63 Simantov R, LaSala JM, Lo SK. et al. Activation of cultured vascular endothelial cells by antiphospholipid antibodies. J Clin Invest 1995; 96 (05) 2211-2219
- 64 Miranda S, Billoir P, Damian L. et al. Hydroxychloroquine reverses the prothrombotic state in a mouse model of antiphospholipid syndrome: role of reduced inflammation and endothelial dysfunction. PLoS One 2019; 14 (03) e0212614
- 65 Canaud G, Legendre C, Terzi F. AKT/mTORC pathway in antiphospholipid-related vasculopathy: a new player in the game. Lupus 2015; 24 (03) 227-230
- 66 Hsieh WT, Hsu CJ, Capraro BR. et al. Curvature sorting of peripheral proteins on solid-supported wavy membranes. Langmuir 2012; 28 (35) 12838-12843
- 67 Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9 (06) 654-659
- 68 Arienti G, Carlini E, Polci A, Cosmi EV, Palmerini CA. Fatty acid pattern of human prostasome lipid. Arch Biochem Biophys 1998; 358 (02) 391-395
- 69 Tauro BJ, Greening DW, Mathias RA, Mathivanan S, Ji H, Simpson RJ. Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol Cell Proteomics 2013; 12 (03) 587-598
- 70 Denzer K, van Eijk M, Kleijmeer MJ, Jakobson E, de Groot C, Geuze HJ. Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J Immunol 2000; 165 (03) 1259-1265
- 71 Ettelaie C, Elkeeb AM, Maraveyas A, Collier MEW. p38α phosphorylates serine 258 within the cytoplasmic domain of tissue factor and prevents its incorporation into cell-derived microparticles. Biochim Biophys Acta 2013; 1833 (03) 613-621
- 72 Stegmayr B, Ronquist G. Promotive effect on human sperm progressive motility by prostasomes. Urol Res 1982; 10 (05) 253-257
- 73 Morelli AE, Larregina AT, Shufesky WJ. et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004; 104 (10) 3257-3266
- 74 MacKenzie A, Wilson HL, Kiss-Toth E, Dower SK, North RA, Surprenant A. Rapid secretion of interleukin-1β by microvesicle shedding. Immunity 2001; 15 (05) 825-835
- 75 Calzolari A, Raggi C, Deaglio S. et al. TfR2 localizes in lipid raft domains and is released in exosomes to activate signal transduction along the MAPK pathway. J Cell Sci 2006; 119 (Pt 21): 4486-4498
- 76 Pan BT, Teng K, Wu C, Adam M, Johnstone RM. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 1985; 101 (03) 942-948
- 77 Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013; 200 (04) 373-383
- 78 Parolini I, Federici C, Raggi C. et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 2009; 284 (49) 34211-34222
- 79 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
- 80 Mack M, Kleinschmidt A, Brühl H. et al. Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med 2000; 6 (07) 769-775
- 81 Owens III AP, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res 2011; 108 (10) 1284-1297
- 82 Su Y, Deng X, Ma R, Dong Z, Wang F, Shi J. The exposure of phosphatidylserine influences procoagulant activity in retinal vein occlusion by microparticles, blood cells, and endothelium. Oxid Med Cell Longev 2018; 2018: 3658476
- 83 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 (01) 93-102
- 84 Pasquet JM, Dachary-Prigent J, Nurden AT. Calcium influx is a determining factor of calpain activation and microparticle formation in platelets. Eur J Biochem 1996; 239 (03) 647-654
- 85 Hankins HM, Baldridge RD, Xu P, Graham TR. Role of flippases, scramblases and transfer proteins in phosphatidylserine subcellular distribution. Traffic 2015; 16 (01) 35-47
- 86 Butenas S. Tissue factor structure and function. Scientifica (Cairo) 2012; 2012: 964862
- 87 Mackman N, Tilley RE, Key NS. Role of the extrinsic pathway of blood coagulation in hemostasis and thrombosis. Arterioscler Thromb Vasc Biol 2007; 27 (08) 1687-1693
- 88 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
- 89 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 (09) 1467-1471
- 90 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
- 91 Jy W, Jimenez JJ, Mauro LM. et al. Endothelial microparticles induce formation of platelet aggregates via a von Willebrand factor/ristocetin dependent pathway, rendering them resistant to dissociation. J Thromb Haemost 2005; 3 (06) 1301-1308
- 92 Sing CE, Alexander-Katz A. Elongational flow induces the unfolding of von Willebrand factor at physiological flow rates. Biophys J 2010; 98 (09) L35-L37
- 93 Wu M, Barnard J, Kundu S, McCrae KR. A novel pathway of cellular activation mediated by antiphospholipid antibody-induced extracellular vesicles. J Thromb Haemost 2015; 13 (10) 1928-1940
- 94 Thyagarajan A, Kadam SM, Liu L. et al. Gemcitabine induces microvesicle particle release in a platelet-activating factor-receptor-dependent manner via modulation of the MAPK pathway in pancreatic cancer cells. Int J Mol Sci 2018; 20 (01) E32
- 95 Velásquez M, Rojas M, Abrahams VM, Escudero C, Cadavid ÁP. Mechanisms of endothelial dysfunction in antiphospholipid syndrome: association with clinical manifestations. Front Physiol 2018; 9: 1840
- 96 Chaturvedi S, McCrae KR. Clinical risk assessment in the antiphospholipid syndrome: current landscape and emerging biomarkers. Curr Rheumatol Rep 2017; 19 (07) 43
- 97 Campello E, Radu CM, Tonello M. et al. Circulating microparticles in pregnant patients with primary anti-phospholipid syndrome: an exploratory study. Scand J Rheumatol 2018; 47 (06) 501-504
- 98 Chaturvedi S, Cockrell E, Espinola R. et al. Circulating microparticles in patients with antiphospholipid antibodies: characterization and associations. Thromb Res 2015; 135 (01) 102-108
- 99 Mobarrez F, Gunnarsson I, Svenungsson E. Altered β2-glycoprotein I expression on microparticles in the presence of antiphospholipid antibodies. J Thromb Haemost 2017; 15 (09) 1799-1806
- 100 Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014; 30 (01) 255-289
- 101 Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009; 458 (7237): 445-452
- 102 Hicke L, Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 2003; 19 (01) 141-172
- 103 Savina A, Vidal M, Colombo MI. The exosome pathway in K562 cells is regulated by Rab11. J Cell Sci 2002; 115 (Pt 12): 2505-2515
- 104 Sidhu SS, Mengistab AT, Tauscher AN, LaVail J, Basbaum C. The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 2004; 23 (04) 956-963
- 105 Bianco F, Perrotta C, Novellino L. et al. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 2009; 28 (08) 1043-1054
- 106 Curtis AM, Wilkinson PF, Gui M, Gales TL, Hu E, Edelberg JM. p38 mitogen-activated protein kinase targets the production of proinflammatory endothelial microparticles. J Thromb Haemost 2009; 7 (04) 701-709
- 107 Yang S, Zhong Q, Qiu Z. et al. Angiotensin II receptor type 1 autoantibodies promote endothelial microparticles formation through activating p38 MAPK pathway. J Hypertens 2014; 32 (04) 762-770
- 108 Li M, Yu D, Williams KJ, Liu ML. Tobacco smoke induces the generation of procoagulant microvesicles from human monocytes/macrophages. Arterioscler Thromb Vasc Biol 2010; 30 (09) 1818-1824
- 109 Betapudi V, Lominadze G, Hsi L, Willard B, Wu M, McCrae KR. Anti-β2GPI antibodies stimulate endothelial cell microparticle release via a nonmuscle myosin II motor protein-dependent pathway. Blood 2013; 122 (23) 3808-3817
- 110 Zhu HQ, Cheng XW, Xiao LL. et al. Melatonin prevents oxidized low-density lipoprotein-induced increase of myosin light chain kinase activation and expression in HUVEC through ERK/MAPK signal transduction. J Pineal Res 2008; 45 (03) 328-334