Semin Thromb Hemost 2012; 38(01): 102-113
DOI: 10.1055/s-0031-1300956
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Platelet-Derived Microvesicles: Multitalented Participants in Intercellular Communication

Maria Aatonen
1   Division of Biochemistry and Biotechnology, Department of Biosciences, University of Helsinki, Finland
,
Mikaela Grönholm
1   Division of Biochemistry and Biotechnology, Department of Biosciences, University of Helsinki, Finland
,
Pia R.-M. Siljander
1   Division of Biochemistry and Biotechnology, Department of Biosciences, University of Helsinki, Finland
› Author Affiliations
Further Information

Publication History

Publication Date:
07 February 2012 (online)

Abstract

Platelets can release a heterogeneous pool of vesicles which include plasma membrane-derived microparticles (PMPs) and multivesicular body-derived exosomes. As both vesicle types are generated upon activation and their distinction is complicated due to an overlap in their molecular properties and sizes, they are best discussed as an entity, the platelet-derived microvesicles (PMVs). PMPs can be formed through several induction pathways, which determine their different molecular profiles and facilitate tailor-made participation in intercellular communication. This dynamic variability may lie behind the multifaceted and sometimes very different observations of the PMPs in physiological and pathological settings. Currently, little is known of platelet-derived exosomes. In all, PMVs not only participate in several homeostatic multicellular processes, such as hemostasis, maintenance of vascular health, and immunity, but they also play a role in thrombotic and inflammatory diseases and cancer progression. In the past few years, the number of original articles and reviews on microvesicles has dramatically increased, but the data simultaneously raise further questions, the answers to which depend on forthcoming analytical improvements. In this article, the differential activation pathways and the molecular and functional properties of PMVs are reviewed in context with their sometimes paradoxical role in health and in disease. Also, the methodological issues of PMV detection and analysis are discussed in the light of recent advances within the field.

 
  • References

  • 1 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
  • 2 Favaloro EJ. Foreword. Semin Thromb Hemost 2010; 36 (8) 803-804
  • 3 Chargaff E, West R. The biological significance of the thromboplastic protein of blood. J Biol Chem 1946; 166 (1) 189-197
  • 4 Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967; 13 (3) 269-288
  • 5 Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999; 94 (11) 3791-3799
  • 6 Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9 (8) 581-593
  • 7 van Nispen tot Pannerden H, de Haas F, Geerts W, Posthuma G, van Dijk S, Heijnen HF. The platelet interior revisited: electron tomography reveals tubular alpha-granule subtypes. Blood 2010; 116 (7) 1147-1156
  • 8 van der Zee PM, Biró E, Ko Y , et al. P-selectin- and CD63-exposing platelet microparticles reflect platelet activation in peripheral arterial disease and myocardial infarction. Clin Chem 2006; 52 (4) 657-664
  • 9 Biró E, Akkerman JW, Hoek FJ , et al. The phospholipid composition and cholesterol content of platelet-derived microparticles: a comparison with platelet membrane fractions. J Thromb Haemost 2005; 3 (12) 2754-2763
  • 10 Dragovic RA, Gardiner C, Brooks AS , et al. Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis. Nanomedicine 2011; 7 (6) 780-788
  • 11 Yuana Y, Oosterkamp TH, Bahatyrova S , et al. Atomic force microscopy: a novel approach to the detection of nanosized blood microparticles. J Thromb Haemost 2010; 8 (2) 315-323
  • 12 Jy W, Horstman LL, Wang F, Duncan RC, Ahn YS. Platelet factor 3 in plasma fractions: its relation to microparticle size and thromboses. Thromb Res 1995; 80 (6) 471-482
  • 13 Garcia BA, Smalley DM, Cho H, Shabanowitz J, Ley K, Hunt DF. The platelet microparticle proteome. J Proteome Res 2005; 4 (5) 1516-1521
  • 14 Piersma SR, Broxterman HJ, Kapci M , et al. Proteomics of the TRAP-induced platelet releasate. J Proteomics 2009; 72 (1) 91-109
  • 15 Smalley DM, Root KE, Cho H, Ross MM, Ley K. Proteomic discovery of 21 proteins expressed in human plasma-derived but not platelet-derived microparticles. Thromb Haemost 2007; 97 (1) 67-80
  • 16 Dean WL, Lee MJ, Cummins TD, Schultz DJ, Powell DW. Proteomic and functional characterisation of platelet microparticle size classes. Thromb Haemost 2009; 102 (4) 711-718
  • 17 Reininger AJ, Heijnen HF, Schumann H, Specht HM, Schramm W, Ruggeri ZM. Mechanism of platelet adhesion to von Willebrand factor and microparticle formation under high shear stress. Blood 2006; 107 (9) 3537-3545
  • 18 Schoenwaelder SM, Yuan Y, Josefsson EC , et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 2009; 114 (3) 663-666
  • 19 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
  • 20 Forestier M, Reséndiz JC, Pontiggia L, Lassila R, Beer JH. Platelet microparticle suppressing antibody against GP Ibalpha acts independently of the filamin cleavage and increases protein tyrosine phosphorylation. Blood Coagul Fibrinolysis 2008; 19 (8) 801-806
  • 21 Cranmer SL, Ashworth KJ, Yao Y , et al. High shear-dependent loss of membrane integrity and defective platelet adhesion following disruption of the GPIbα-filamin interaction. Blood 2011; 117 (9) 2718-2727
  • 22 Rand ML, Wang H, Bang KW , et al. Phosphatidylserine exposure and other apoptotic-like events in Bernard-Soulier syndrome platelets. Am J Hematol 2010; 85 (8) 584-592
  • 23 Gemmell CH, Sefton MV, Yeo EL. Platelet-derived microparticle formation involves glycoprotein IIb-IIIa. Inhibition by RGDS and a Glanzmann’s thrombasthenia defect. J Biol Chem 1993; 268 (20) 14586-14589
  • 24 Dale GL, Remenyi G, Friese P. Tetraspanin CD9 is required for microparticle release from coated-platelets. Platelets 2009; 20 (6) 361-366
  • 25 Heemskerk JW, Siljander P, Vuist WM , et al. Function of glycoprotein VI and integrin alpha2beta1 in the procoagulant response of single, collagen-adherent platelets. Thromb Haemost 1999; 81 (5) 782-792
  • 26 Siljander P, Farndale RW, Feijge MA , et al. Platelet adhesion enhances the glycoprotein VI-dependent procoagulant response: Involvement of p38 MAP kinase and calpain. Arterioscler Thromb Vasc Biol 2001; 21 (4) 618-627
  • 27 Jackson SP, Schoenwaelder SM. Procoagulant platelets: are they necrotic?. Blood 2010; 116 (12) 2011-2018
  • 28 Gilio K, van Kruchten R, Braun A , et al. Roles of platelet STIM1 and Orai1 in glycoprotein VI- and thrombin-dependent procoagulant activity and thrombus formation. J Biol Chem 2010; 285 (31) 23629-23638
  • 29 Ozaki Y, Suzuki-Inoue K, Inoue O. Novel interactions in platelet biology: CLEC-2/podoplanin and laminin/GPVI. J Thromb Haemost 2009; 7 (Suppl 1) 191-194
  • 30 Brown GT, McIntyre TM. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles. J Immunol 2011; 186 (9) 5489-5496
  • 31 Flaumenhaft R, Dilks JR, Richardson J , et al. Megakaryocyte-derived microparticles: direct visualization and distinction from platelet-derived microparticles. Blood 2009; 113 (5) 1112-1121
  • 32 Sims PJ, Wiedmer T, Esmon CT, Weiss HJ, Shattil SJ. Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: an isolated defect in platelet procoagulant activity. J Biol Chem 1989; 264 (29) 17049-17057
  • 33 Connor DE, Exner T, Ma DD, Joseph JE. The majority of circulating platelet-derived microparticles fail to bind annexin V, lack phospholipid-dependent procoagulant activity and demonstrate greater expression of glycoprotein Ib. Thromb Haemost 2010; 103 (5) 1044-1052
  • 34 Perez-Pujol S, Marker PH, Key NS. Platelet microparticles are heterogeneous and highly dependent on the activation mechanism: studies using a new digital flow cytometer. Cytometry A 2007; 71 (1) 38-45
  • 35 Dale GL, Remenyi G, Friese P. Quantitation of microparticles released from coated-platelets. J Thromb Haemost 2005; 3 (9) 2081-2088
  • 36 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
  • 37 Fox JE, Austin CD, Boyles JK, Steffen PK. Role of the membrane skeleton in preventing the shedding of procoagulant-rich microvesicles from the platelet plasma membrane. J Cell Biol 1990; 111 (2) 483-493
  • 38 Rand ML, Wang H, Bang KW, Packham MA, Freedman J. Rapid clearance of procoagulant platelet-derived microparticles from the circulation of rabbits. J Thromb Haemost 2006; 4 (7) 1621-1623
  • 39 Rank A, Nieuwland R, Crispin A , et al. Clearance of platelet microparticles in vivo. Platelets 2011; 22 (2) 111-116
  • 40 Dasgupta SK, Abdel-Monem H, Niravath P , et al. Lactadherin and clearance of platelet-derived microvesicles. Blood 2009; 113 (6) 1332-1339
  • 41 Abdel-Monem H, Dasgupta SK, Le A, Prakasam A, Thiagarajan P. Phagocytosis of platelet microvesicles and beta2- glycoprotein I. Thromb Haemost 2010; 104 (2) 335-341
  • 42 Hoang TQ, Rampon C, Freyssinet JM, Vriz S, Kerbiriou-Nabias D. A method to assess the migration properties of cell-derived microparticles within a living tissue. Biochim Biophys Acta 2011; 1810 (9) 863-866
  • 43 Italiano Jr JE, Mairuhu AT, Flaumenhaft R. Clinical relevance of microparticles from platelets and megakaryocytes. Curr Opin Hematol 2010; 17 (6) 578-584
  • 44 Gambim MH, do Carmo AdeO, Marti L, Veríssimo-Filho S, Lopes LR, Janiszewski M. Platelet-derived exosomes induce endothelial cell apoptosis through peroxynitrite generation: experimental evidence for a novel mechanism of septic vascular dysfunction. Crit Care 2007; 11 (5) R107
  • 45 Sadallah S, Eken C, Martin PJ, Schifferli JA. Microparticles (ectosomes) shed by stored human platelets downregulate macrophages and modify the development of dendritic cells. J Immunol 2011; 186 (11) 6543-6552
  • 46 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
  • 47 Maroney SA, Haberichter SL, Friese P , et al. Active tissue factor pathway inhibitor is expressed on the surface of coated platelets. Blood 2007; 109 (5) 1931-1937
  • 48 Sims PJ, Faioni EM, Wiedmer T, Shattil SJ. Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J Biol Chem 1988; 263 (34) 18205-18212
  • 49 Gilbert GE, Sims PJ, Wiedmer T, Furie B, Furie BC, Shattil SJ. Platelet-derived microparticles express high affinity receptors for factor VIII. J Biol Chem 1991; 266 (26) 17261-17268
  • 50 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
  • 51 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
  • 52 Diamant M, Nieuwland R, Pablo RF, Sturk A, Smit JW, Radder JK. Elevated numbers of tissue-factor exposing microparticles correlate with components of the metabolic syndrome in uncomplicated type 2 diabetes mellitus. Circulation 2002; 106 (19) 2442-2447
  • 53 Merten M, Pakala R, Thiagarajan P, Benedict CR. Platelet microparticles promote platelet interaction with subendothelial matrix in a glycoprotein IIb/IIIa-dependent mechanism. Circulation 1999; 99 (19) 2577-2582
  • 54 Siljander P, Carpen O, Lassila R. Platelet-derived microparticles associate with fibrin during thrombosis. Blood 1996; 87 (11) 4651-4663
  • 55 Prokopi M, Mayr M. Proteomics: a reality-check for putative stem cells. Circ Res 2011; 108 (4) 499-511
  • 56 Raturi A, Miersch S, Hudson JW, Mutus B. Platelet microparticle-associated protein disulfide isomerase promotes platelet aggregation and inactivates insulin. Biochim Biophys Acta 2008; 1778 (12) 2790-2796
  • 57 Tang K, Liu J, Yang Z , et al. Microparticles mediate enzyme transfer from platelets to mast cells: a new pathway for lipoxin A4 biosynthesis. Biochem Biophys Res Commun 2010; 400 (3) 432-436
  • 58 Maciejewski JP, Young NS, Yu M, Anderson SM, Sloand EM. Analysis of the expression of glycosylphosphatidylinositol anchored proteins on platelets from patients with paroxysmal nocturnal hemoglobinuria. Thromb Res 1996; 83 (6) 433-447
  • 59 Yin W, Ghebrehiwet B, Peerschke EI. Expression of complement components and inhibitors on platelet microparticles. Platelets 2008; 19 (3) 225-233
  • 60 Peerschke EI, Yin W, Ghebrehiwet B. Platelet mediated complement activation. Adv Exp Med Biol 2008; 632: 81-91
  • 61 Hunter MP, Ismail N, Zhang X , et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 2008; 3 (11) e3694
  • 62 Schubert P, Devine DV. De novo protein synthesis in mature platelets: a consideration for transfusion medicine. Vox Sang 2010; 99 (2) 112-122
  • 63 Ramacciotti E, Hawley AE, Wrobleski SK , et al. Proteomics of microparticles after deep venous thrombosis. Thromb Res 2010; 125 (6) e269-e274
  • 64 Chandler WL, Yeung W, Tait JF. A new microparticle size calibration standard for use in measuring smaller microparticles using a new flow cytometer. J Thromb Haemost 2011; 9 (6) 1216-1224
  • 65 Toth B, Nikolajek K, Rank A , et al. Gender-specific and menstrual cycle dependent differences in circulating microparticles. Platelets 2007; 18 (7) 515-521
  • 66 Robert S, Poncelet P, Lacroix R , et al. Standardization of platelet-derived microparticle counting using calibrated beads and a Cytomics FC500 routine flow cytometer: a first step towards multicenter studies?. J Thromb Haemost 2009; 7 (1) 190-197
  • 67 Bretelle F, Sabatier F, Desprez D , et al. Circulating microparticles: a marker of procoagulant state in normal pregnancy and pregnancy complicated by preeclampsia or intrauterine growth restriction. Thromb Haemost 2003; 89 (3) 486-492
  • 68 Chaar V, Romana M, Tripette J , et al. Effect of strenuous physical exercise on circulating cell-derived microparticles. Clin Hemorheol Microcirc 2011; 47 (1) 15-25
  • 69 Sossdorf M, Otto GP, Claus RA, Gabriel HH, Lösche W. Cell-derived microparticles promote coagulation after moderate exercise. Med Sci Sports Exerc 2011; 43 (7) 1169-1176
  • 70 Castaman G, Yu-Feng L, Rodeghiero F. A bleeding disorder characterised by isolated deficiency of platelet microvesicle generation. Lancet 1996; 347 (9002) 700-701
  • 71 Stormorken H, Holmsen H, Sund R , et al. Studies on the haemostatic defect in a complicated syndrome. An inverse Scott syndrome platelet membrane abnormality?. Thromb Haemost 1995; 74 (5) 1244-1251
  • 72 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
  • 73 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
  • 74 Janowska-Wieczorek A, Majka M, Kijowski J , et al. Platelet-derived microparticles bind to hematopoietic stem/progenitor cells and enhance their engraftment. Blood 2001; 98 (10) 3143-3149
  • 75 Prokopi M, Pula G, Mayr U , et al. Proteomic analysis reveals presence of platelet microparticles in endothelial progenitor cell cultures. Blood 2009; 114 (3) 723-732
  • 76 Kim HK, Song KS, Chung JH, Lee KR, Lee SN. Platelet microparticles induce angiogenesis in vitro. Br J Haematol 2004; 124 (3) 376-384
  • 77 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
  • 78 Mause SF, Ritzel E, Liehn EA , et al. Platelet microparticles enhance the vasoregenerative potential of angiogenic early outgrowth cells after vascular injury. Circulation 2010; 122 (5) 495-506
  • 79 Sprague DL, Elzey BD, Crist SA, Waldschmidt TJ, Jensen RJ, Ratliff TL. Platelet-mediated modulation of adaptive immunity: unique delivery of CD154 signal by platelet-derived membrane vesicles. Blood 2008; 111 (10) 5028-5036
  • 80 Jy W, Mao WW, Horstman L, Tao J, Ahn YS. Platelet microparticles bind, activate and aggregate neutrophils in vitro. Blood Cells Mol Dis 1995; 21 (3) 217-231, discussion 231a
  • 81 Thom SR, Yang M, Bhopale VM, Huang S, Milovanova TN. Microparticles initiate decompression-induced neutrophil activation and subsequent vascular injuries. J Appl Physiol 2011; 110 (2) 340-351
  • 82 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
  • 83 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
  • 84 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
  • 85 Mause SF, von Hundelshausen P, Zernecke A, Koenen RR, Weber C. Platelet microparticles: a transcellular delivery system for RANTES promoting monocyte recruitment on endothelium. Arterioscler Thromb Vasc Biol 2005; 25 (7) 1512-1518
  • 86 Baldwin III WM, Kuo HH, Morrell CN. Platelets: versatile modifiers of innate and adaptive immune responses to transplants. Curr Opin Organ Transplant 2010; 16 (1) 41-46
  • 87 Boilard E, Nigrovic PA, Larabee K , et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010; 327 (5965) 580-583
  • 88 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
  • 89 Faille D, Combes V, Mitchell AJ , et al. Platelet microparticles: a new player in malaria parasite cytoadherence to human brain endothelium. FASEB J 2009; 23 (10) 3449-3458
  • 90 Forlow SB, McEver RP, Nollert MU. Leukocyte-leukocyte interactions mediated by platelet microparticles under flow. Blood 2000; 95 (4) 1317-1323
  • 91 Rectenwald JE, Myers Jr DD, Hawley AE , et al. D-dimer, P-selectin, and microparticles: novel markers to predict deep venous thrombosis. A pilot study. Thromb Haemost 2005; 94 (6) 1312-1317
  • 92 Tan KT, Tayebjee MH, Lim HS, Lip GY. Clinically apparent atherosclerotic disease in diabetes is associated with an increase in platelet microparticle levels. Diabet Med 2005; 22 (12) 1657-1662
  • 93 Nomura S, Shouzu A, Omoto S , et al. Effect of cilostazol on soluble adhesion molecules and platelet-derived microparticles in patients with diabetes. Thromb Haemost 1998; 80 (3) 388-392
  • 94 Hugel B, Socié G, Vu T , et al. Elevated levels of circulating procoagulant microparticles in patients with paroxysmal nocturnal hemoglobinuria and aplastic anemia. Blood 1999; 93 (10) 3451-3456
  • 95 Preston RA, Jy W, Jimenez JJ , et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 2003; 41 (2) 211-217
  • 96 Janowska-Wieczorek A, Wysoczynski M, Kijowski J , et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer 2005; 113 (5) 752-760
  • 97 Helley D, Banu E, Bouziane A , et al. Platelet microparticles: a potential predictive factor of survival in hormone-refractory prostate cancer patients treated with docetaxel-based chemotherapy. Eur Urol 2009; 56 (3) 479-484
  • 98 Dashevsky O, Varon D, Brill A. Platelet-derived microparticles promote invasiveness of prostate cancer cells via upregulation of MMP-2 production. Int J Cancer 2009; 124 (8) 1773-1777
  • 99 Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 2006; 46 (7) 1199-1209
  • 100 Toth B, Liebhardt S, Steinig K , et al. Platelet-derived microparticles and coagulation activation in breast cancer patients. Thromb Haemost 2008; 100 (4) 663-669
  • 101 Kim HK, Song KS, Park YS , et al. Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor. Eur J Cancer 2003; 39 (2) 184-191
  • 102 Nomura S, Omoto S, Yokoi T , et al. Effects of miglitol in platelet-derived microparticle, adiponectin, and selectin level in patients with type 2 diabetes mellitus. Int J Gen Med 2011; 4: 539-545
  • 103 Mobarrez F, He S, Bröijersen A , et al. Atorvastatin reduces thrombin generation and expression of tissue factor, P-selectin and GPIIIa on platelet-derived microparticles in patients with peripheral arterial occlusive disease. Thromb Haemost 2011; 106 (2) 344-352
  • 104 Murakami T, Horigome H, Tanaka K , et al. Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity. Thromb Res 2007; 119 (1) 45-53
  • 105 Lacroix R, Robert S, Poncelet P, Kasthuri RS, Key NS, Dignat-George F ; ISTH SSC Workshop. Standardization of platelet-derived microparticle enumeration by flow cytometry with calibrated beads: results of the International Society on Thrombosis and Haemostasis SSC Collaborative workshop. J Thromb Haemost 2010; 8 (11) 2571-2574
  • 106 Orozco AF, Lewis DE. Flow cytometric analysis of circulating microparticles in plasma. Cytometry A 2010; 77 (6) 502-514
  • 107 Yuana Y, Bertina RM, Osanto S. Pre-analytical and analytical issues in the analysis of blood microparticles. Thromb Haemost 2011; 105 (3) 396-408
  • 108 The 56th and 57th Scientific Standardization Vascular Biology Subcommitee Meeting Minutes. Available at: http://isth.org/default/index.cfm/ssc1/ssc-minutes/ . Accessed August 29, 2011
  • 109 Mobarrez F, Antovic J, Egberg N , et al. A multicolor flow cytometric assay for measurement of platelet-derived microparticles. Thromb Res 2010; 125 (3) e110-e116
  • 110 Thery C, Amigorena S, Raposo G, Clayton A . Isolation and characterization of exosomes from cell culture supernatants and biological fluids Curr Protoc Cell Biol 2006; Chapter 3:Unit 3.22
  • 111 van der Pol E, Hoekstra AG, Sturk A, Otto C, van Leeuwen TG, Nieuwland R. Optical and non-optical methods for detection and characterization of microparticles and exosomes. J Thromb Haemost 2010; 8 (12) 2596-2607
  • 112 György B, Módos K, Pállinger E , et al. Detection and isolation of cell-derived microparticles are compromised by protein complexes resulting from shared biophysical parameters. Blood 2011; 117 (4) e39-e48
  • 113 Tesselaar ME, Romijn FP, 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 (3) 520-527
  • 114 Xu Y, Nakane N, Maurer-Spurej E. Novel test for microparticles in platelet-rich plasma and platelet concentrates using dynamic light scattering. Transfusion 2011; 51 (2) 363-370
  • 115 Gabriel DA, Giordano K. Microparticle sizing and counting using light scattering methods. Semin Thromb Hemost 2010; 36 (8) 824-832
  • 116 Filipe V, Hawe A, Jiskoot W. Critical evaluation of Nanoparticle Tracking Analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates. Pharm Res 2010; 27 (5) 796-810
  • 117 Jensen OA, Prause JU, Laursen H. Shrinkage in preparatory steps for SEM. A study on rabbit corneal endothelium. Albrecht Von Graefes Arch Klin Exp Ophthalmol 1981; 215 (4) 233-242
  • 118 Zwicker JI. Tissue factor-bearing microparticles and cancer. Semin Thromb Hemost 2008; 34 (2) 195-198
  • 119 Harrison P, Dragovic R, Albanyan A, Lawrie AS, Murphy M, Sargent I . Application of dynamic light scattering to the measurement of microparticles. J Thromb Haemost 2009 ;7(Suppl 2 Abstract OC-TU-056)
  • 120 Robertson C, Booth SA, Beniac DR, Coulthart MB, Booth TF, McNicol A. Cellular prion protein is released on exosomes from activated platelets. Blood 2006; 107 (10) 3907-3911
  • 121 Ray DM, Spinelli SL, Pollock SJ , et al. Peroxisome proliferator-activated receptor gamma and retinoid X receptor transcription factors are released from activated human platelets and shed in microparticles. Thromb Haemost 2008; 99 (1) 86-95
  • 122 Podor TJ, Singh D, Chindemi P , et al. Vimentin exposed on activated platelets and platelet microparticles localizes vitronectin and plasminogen activator inhibitor complexes on their surface. J Biol Chem 2002; 277 (9) 7529-7539
  • 123 Gelderman MP, Simak J. Flow cytometric analysis of cell membrane microparticles. Methods Mol Biol 2008; 484: 79-93
  • 124 Jimenez JJ, Jy W, Mauro LM, Soderland C, Horstman LL, Ahn YS. Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thromb Res 2003; 109 (4) 175-180
  • 125 Abid Hussein MN, Meesters EW, Osmanovic N, Romijn FP, Nieuwland R, Sturk A. Antigenic characterization of endothelial cell-derived microparticles and their detection ex vivo. J Thromb Haemost 2003; 1 (11) 2434-2443
  • 126 Thiagarajan P, Tait JF. Collagen-induced exposure of anionic phospholipid in platelets and platelet-derived microparticles. J Biol Chem 1991; 266 (36) 24302-24307
  • 127 Pfister SL. Role of platelet microparticles in the production of thromboxane by rabbit pulmonary artery. Hypertension 2004; 43 (2) 428-433
  • 128 Fourcade O, Simon MF, Viodé C , et al. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell 1995; 80 (6) 919-927
  • 129 Holme PA, Brosstad F, Solum NO. The difference between platelet and plasma FXIII used to study the mechanism of platelet microvesicle formation. Thromb Haemost 1993; 70 (4) 681-686
  • 130 Böing AN, Hau CM, Sturk A, Nieuwland R. Platelet microparticles contain active caspase 3. Platelets 2008; 19 (2) 96-103
  • 131 Rozmyslowicz T, Majka M, Kijowski J , et al. Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS 2003; 17 (1) 33-42
  • 132 Nomura S, Komiyama Y, Miyake T , et al. Amyloid beta-protein precursor-rich platelet microparticles in thrombotic disease. Thromb Haemost 1994; 72 (4) 519-522
  • 133 Ueba T, Nomura S, Inami N , et al. Plasma level of platelet-derived microparticles is associated with coronary heart disease risk score in healthy men. J Atheroscler Thromb 2010; 17 (4) 342-349
  • 134 Nomura S, Uehata S, Saito S, Osumi K, Ozeki Y, Kimura Y. Enzyme immunoassay detection of platelet-derived microparticles and RANTES in acute coronary syndrome. Thromb Haemost 2003; 89 (3) 506-512
  • 135 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
  • 136 Bal L, Ederhy S, Di Angelantonio E , et al. Factors influencing the level of circulating procoagulant microparticles in acute pulmonary embolism. Arch Cardiovasc Dis 2010; 103 (6-7) 394-403
  • 137 Azzam H, Zagloul M. Elevated platelet microparticle levels in valvular atrial fibrillation. Hematology 2009; 14 (6) 357-360
  • 138 Zeiger F, Stephan S, Hoheisel G, Pfeiffer D, Ruehlmann C, Koksch M. P-Selectin expression, platelet aggregates, and platelet-derived microparticle formation are increased in peripheral arterial disease. Blood Coagul Fibrinolysis 2000; 11 (8) 723-728
  • 139 Lukasik M, Rozalski M, Luzak B, Michalak S, Kozubski W, Watala C. Platelet activation and reactivity in the convalescent phase of ischaemic stroke. Thromb Haemost 2010; 103 (3) 644-650
  • 140 Lackner P, Dietmann A, Beer R , et al. Cellular microparticles as a marker for cerebral vasospasm in spontaneous subarachnoid hemorrhage. Stroke 2010; 41 (10) 2353-2357
  • 141 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
  • 142 Michelsen AE, Notø AT, Brodin E, Mathiesen EB, Brosstad F, Hansen JB. Elevated levels of platelet microparticles in carotid atherosclerosis and during the postprandial state. Thromb Res 2009; 123 (6) 881-886
  • 143 Shet AS, Aras O, Gupta K , et al. Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood 2003; 102 (7) 2678-2683
  • 144 Tantawy AA, Matter RM, Hamed AA, Shams El Din El Telbany MA. Platelet microparticles in immune thrombocytopenic purpura in pediatrics. Pediatr Hematol Oncol 2010; 27 (4) 283-296
  • 145 Warkentin TE, Hayward CP, Boshkov LK , et al. Sera from patients with heparin-induced thrombocytopenia generate platelet-derived microparticles with procoagulant activity: an explanation for the thrombotic complications of heparin-induced thrombocytopenia. Blood 1994; 84 (11) 3691-3699
  • 146 Castaman G, Yu-Feng L, Battistin E, Rodeghiero F. Characterization of a novel bleeding disorder with isolated prolonged bleeding time and deficiency of platelet microvesicle generation. Br J Haematol 1997; 96 (3) 458-463
  • 147 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
  • 148 Mostefai HA, Meziani F, Mastronardi ML , et al. Circulating microparticles from patients with septic shock exert protective role in vascular function. Am J Respir Crit Care Med 2008; 178 (11) 1148-1155
  • 149 Soriano AO, Jy W, Chirinos JA , et al. Levels of endothelial and platelet microparticles and their interactions with leukocytes negatively correlate with organ dysfunction and predict mortality in severe sepsis. Crit Care Med 2005; 33 (11) 2540-2546
  • 150 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
  • 151 Sellam J, Proulle V, Jüngel A , et al. Increased levels of circulating microparticles in primary Sjögren’s syndrome, systemic lupus erythematosus and rheumatoid arthritis and relation with disease activity. Arthritis Res Ther 2009; 11 (5) R156
  • 152 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
  • 153 Nomura S, Inami N, Ozaki Y, Kagawa H, Fukuhara S. Significance of microparticles in progressive systemic sclerosis with interstitial pneumonia. Platelets 2008; 19 (3) 192-198
  • 154 Guiducci S, Distler JH, Jüngel A , et al. The relationship between plasma microparticles and disease manifestations in patients with systemic sclerosis. Arthritis Rheum 2008; 58 (9) 2845-2853
  • 155 Knijff-Dutmer EA, Koerts J, Nieuwland R, Kalsbeek-Batenburg EM, van de Laar MA. Elevated levels of platelet microparticles are associated with disease activity in rheumatoid arthritis. Arthritis Rheum 2002; 46 (6) 1498-1503
  • 156 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
  • 157 Sabatier F, Darmon P, Hugel B , et al. Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes 2002; 51 (9) 2840-2845
  • 158 Sheremata WA, Jy W, Horstman LL, Ahn YS, Alexander JS, Minagar A. Evidence of platelet activation in multiple sclerosis. J Neuroinflammation 2008; 5: 27
  • 159 Koga H, Sugiyama S, Kugiyama K , et al. Elevated levels of remnant lipoproteins are associated with plasma platelet microparticles in patients with type-2 diabetes mellitus without obstructive coronary artery disease. Eur Heart J 2006; 27 (7) 817-823
  • 160 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
  • 161 Matsubara E, Shoji M, Murakami T, Abe K, Frangione B, Ghiso J. Platelet microparticles as carriers of soluble Alzheimer’s amyloid beta (sAbeta). Ann N Y Acad Sci 2002; 977: 340-348
  • 162 Ando M, Iwata A, Ozeki Y, Tsuchiya K, Akiba T, Nihei H. Circulating platelet-derived microparticles with procoagulant activity may be a potential cause of thrombosis in uremic patients. Kidney Int 2002; 62 (5) 1757-1763
  • 163 Ayers L, Ferry B, Craig S, Nicoll D, Stradling JR, Kohler M. Circulating cell-derived microparticles in patients with minimally symptomatic obstructive sleep apnoea. Eur Respir J 2009; 33 (3) 574-580
  • 164 Lok CA, Van Der Post JA, Sargent IL , et al. Changes in microparticle numbers and cellular origin during pregnancy and preeclampsia. Hypertens Pregnancy 2008; 27 (4) 344-360
  • 165 Lok CA, Nieuwland R, Sturk A , et al. Microparticle-associated P-selectin reflects platelet activation in preeclampsia. Platelets 2007; 18 (1) 68-72
  • 166 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
  • 167 Kaptan K, Beyan C, Ifran A, Pekel A. Platelet-derived microparticle levels in women with recurrent spontaneous abortion. Int J Gynaecol Obstet 2008; 102 (3) 271-274