Platelet-derived microvesicles: Multitalented participants in intercellular communication

Seminars in Thrombosis and Hemostasis

Volumn 38, Issue 1, 2012, Pages 102-113

  Aatonen, Maria ^a   Grönholm, Mikaela ^a   Siljander, Piar M ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

exosome; microparticle; microvesicle; nanoparticle tracking analysis; platelet; transmission electron microscopy

Indexed keywords

CANCER GROWTH; CELL COMMUNICATION; CONFERENCE PAPER; EXOSOME; HEMOSTASIS; INFLAMMATORY DISEASE; PLATELET DERIVED MICROVESICLE; PLATELET MICROPARTICLE; PRIORITY JOURNAL; THROMBOSIS;

EID: 84857022406     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0031-1300956     Document Type: Conference Paper

References (167)

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. Thry 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, Bir 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. Bir 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 (Pubitemid 41819805)
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 (Pubitemid 41464776)
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 (Pubitemid 46242388)
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, Resndiz 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 GPIb-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 Glanzmanns thrombasthenia defect. J Biol Chem: 1993; 268 20 14586 14589 (Pubitemid 23206590)
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 (Pubitemid 29216567)
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 (Pubitemid 32323397)
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-1-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 (Pubitemid 19255533)
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 (Pubitemid 46207382)
35. Dale GL, Remenyi G, Friese P. Quantitation of microparticles released from coated-platelets. J Thromb Haemost: 2005; 3 9 2081 2088 (Pubitemid 43086067)
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 (Pubitemid 34556736)
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 JE Jr, 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, Verssimo-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 (Pubitemid 46348189)
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 (Pubitemid 19005097)
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 (Pubitemid 21907934)
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 (Pubitemid 46437805)
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 (Pubitemid 36682554)
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 (Pubitemid 35278799)
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 (Pubitemid 29228290)
54. Siljander P, Carpen O, Lassila R. Platelet-derived microparticles associate with fibrin during thrombosis. Blood: 1996; 87 11 4651 4663 (Pubitemid 26162364)
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 (Pubitemid 26328716)
59. Yin W, Ghebrehiwet B, Peerschke EI. Expression of complement components and inhibitors on platelet microparticles. Platelets: 2008; 19 3 225 233 (Pubitemid 351574446)
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 (Pubitemid 350034853)
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 (Pubitemid 36329239)
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 (Pubitemid 26076165)
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 (Pubitemid 32913636)
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 (Pubitemid 32293699)
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 (Pubitemid 38167990)
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 (Pubitemid 40798290)
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 (Pubitemid 26083518)
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 (Pubitemid 27203768)
83. Barry OP, Kazanietz MG, Pratic 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, Pratic D, Savani RC, FitzGerald GA. Modulation of monocyte-endothelial cell interactions by platelet microparticles. J Clin Invest: 1998; 102 1 136 144 (Pubitemid 28323840)
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 (Pubitemid 40923377)
86. Baldwin WM III, 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 (Pubitemid 30319319)
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 (Pubitemid 30099841)
91. Rectenwald JE, Myers DD Jr, 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 (Pubitemid 41819632)
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 (Pubitemid 43046464)
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 (Pubitemid 28438730)
94. Hugel B, Soci 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 (Pubitemid 29220912)
95. Preston RA, Jy W, Jimenez JJ., et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension: 2003; 41 2 211 217 (Pubitemid 36204891)
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 (Pubitemid 40101256)
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 (Pubitemid 44139495)
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 (Pubitemid 36057068)
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 (Pubitemid 44716205)
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, Mdos K, Pllinger 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 (Pubitemid 46680685)
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 (Pubitemid 11137547)
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 (Pubitemid 43726795)
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 (Pubitemid 34953151)
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 (Pubitemid 36712905)
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 (Pubitemid 21908941)
127. Pfister SL. Role of platelet microparticles in the production of thromboxane by rabbit pulmonary artery. Hypertension: 2004; 43 2 428 433 (Pubitemid 38174150)
128. Fourcade O, Simon MF, Viod 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 (Pubitemid 23310578)
130. Böing AN, Hau CM, Sturk A, Nieuwland R. Platelet microparticles contain active caspase 3. Platelets: 2008; 19 2 96 103 (Pubitemid 351302378)
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 (Pubitemid 36106296)
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 (Pubitemid 24305642)
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 (Pubitemid 36329242)
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 (Pubitemid 32010206)
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 (Pubitemid 23329372)
142. Michelsen AE, Not 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 (Pubitemid 37193612)
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 (Pubitemid 27087227)
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 (Pubitemid 32421813)
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 (Pubitemid 41682106)
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 Sjögrens 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 (Pubitemid 351574449)
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 (Pubitemid 34620195)
156. Daniel L, Fakhouri F, Joly D., et al. Increase of circulating neutrophil
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 (Pubitemid 34970939)
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 Alzheimers amyloid beta (sAbeta). Ann N Y Acad Sci: 2002; 977 340 348 (Pubitemid 35418174)
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 (Pubitemid 35286284)
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 (Pubitemid 34925587)
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