On the origin of microparticles: From “platelet dust” to mediators of intercellular communication

Pulmonary Circulation

Volumn 3, Issue 2, 2013, Pages 329-340

  Hargett, Leslie A ^a   Bauer, Natalie N ^a  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

Coagulation; Microparticles; Pulmonary circulation

Indexed keywords

EID: 84922266697     PISSN: 20458932     EISSN: 20458940     Source Type: Journal    
DOI: 10.4103/2045-8932.114760     Document Type: Review

References (98)

1. Burnier L, Fontana P, Kwak BR, Angelillo-Scherrer A. Cell-derived microparticles in haemostasis and vascular medicine. Thromb Haemost 2009;101:439-51.
2. Mackman N. On the trail of microparticles. Circ Res 2009;104:925-7.
3. Chou J, Mackman N, Merrill-Skoloff G, Pedersen B, Furie BC, Furie B. Hematopoietic cell-derived microparticle tissue factor contributes to fibrin formation during thrombus propagation. Blood 2004;104:3190-7.
4. Flaumenhaft R. Formation and fate of platelet microparticles. Blood Cells Mol Dis 2006;36:182-7.
5. Horstman LL, Ahn YS. Platelet microparticles: A wide-angle perspective. Crit Rev Oncol Hematol 1999;30:111-42.
6. Joop K, Berckmans RJ, Nieuwland R, Berkhout J, Romijn FP, Hack CE, et al. Microparticles from patients with multiple organ dysfunction syndrome and sepsis support coagulation through multiple mechanisms. Thromb Haemost 2001;85:810-20.
7. Berckmans RJ, Nieuwland R, Boing AN, Romijn FP, Hack CE, Sturk A. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost 2001;85:639-46.
8. Bastarache JA, Fremont RD, Kropski JA, Bossert FR, Ware LB. Procoagulant alveolar microparticles in the lungs of patients with acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol 2009;297:L1035-41.
9. Davila M, Amirkhosravi A, Coll E, Desai H, Robles L, Colon J, et al. Tissue factor-bearing microparticles derived from tumor cells: Impact on coagulation activation. J Thromb Haemost 2008;6:1517-24.
10. Quick AJ. Hemorrhagic diseases and thrombosis. 2nd ed. Philadelphia: Lea and Febiger;1966.
11. Doyle D. William Hewson (1739-74): The father of haematology. Br J Haematol 2006;133:375-81.
12. Monroe DM, Hoffman M, Roberts HR. Platelets and thrombin generation. Arterioscler Thromb Vasc Biol 2002;22:1381-9.
13. Ogston D. The physiology of hemostasis. Cambridge, Massachusetts: Harvard University Press; 1983.
14. Hougie C. The activation of platelets by plasma. Br J Haematol 1955;1:213-22.
15. Macfarlane RG. An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature 1964;202:498-9.
16. Davie EW, Ratnoff OD. Waterfall sequence for intrinsic blood clotting. Science 1964;145:1310-2.
17. Hougie C. A review of the scientific and literary accomplishments of Professor R.G. Macfarlane CBE, FRS. Br J Haematol 2006;133:581-90.
18. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967;13:269-88.
19. Chargaff E, West R. The biological significance of the thromboplastic protein of blood. J Biol Chem 1946;166:189-97.
20. O’Brien JR. The platelet-like activity of serum. Br J Haematol 1955;1:223-8.
21. Webber AJ, Johnson SA. Platelet participation in blood coagulation aspects of hemostasis. Am J Pathol 1970;60:19-42.
22. Crawford N. The presence of contractile proteins in platelet microparticles isolated from human and animal platelet-free plasma. Br J Haematol 1971;21:53-69.
23. George JN, Thoi LL, McManus LM, Reimann TA. Isolation of human platelet membrane microparticles from plasma and serum. Blood 1982;60:834-40.
24. Nemerson Y. Tissue factor and hemostasis. Blood 1988;71:1-8.
25. Dvorak HF, Quay SC, Orenstein NS, Dvorak AM, Hahn P, Bitzer AM, et al. Tumor shedding and coagulation. Science 1981;212:923-4.
26. Dvorak HF, Van DeWater L, Bitzer AM, Dvorak AM, Anderson D, Harvey VS, et al. Procoagulant activity associated with plasma membrane vesicles shed by cultured tumor cells. Cancer Res 1983;43:4434-42.
27. Satta N, Toti F, Feugeas O, Bohbot A, Dachary-Prigent J, Eschwège V, et al. Monocyte vesiculation is a possible mechanism for dissemination of membrane-associated procoagulant activities and adhesion molecules after stimulation by lipopolysaccharide. J Immunol 1994;153:3245-55.
28. Falati S, Liu Q, Gross P, Merrill-Skoloff G, Chou J, Vandendries E, 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;197:1585-98.
29. Matsumoto N, Nomura S, Kamihata H, Kimura Y, Iwasaka T. Increased level of oxidized LDL-dependent monocyte-derived microparticles in acute coronary syndrome. Thromb Haemost 2004;91:146-54.
30. Tilley RE, Holscher T, Belani R, Nieva J, Mackman N. Tissue factor activity is increased in a combined platelet and microparticle sample from cancer patients. Thromb Res 2008;122:604-9.
31. Schecter AD, Spirn B, Rossikhina M, Giesen PL, Bogdanov V, Fallon JT, et al. Release of active tissue factor by human arterial smooth muscle cells. Circ Res 2000;87:126-32.
32. 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;106:2442-7.
33. Nieuwland R, Berckmans RJ, McGregor S, Böing AN, Romijn FP, Westendorp RG, et al. Cellular origin and procoagulant properties of microparticles in meningococcal sepsis. Blood 2000;95:930-5.
34. Bakouboula B, Morel O, Faure A, Zobairi F, Jesel L, Trinh A, et al. Procoagulant membrane microparticles correlate with the severity of pulmonary arterial hypertension. Am J Respir Crit Care Med 2008;177:536-43.
35. Del Conde I, Shrimpton CN, Thiagarajan P, Lopez JA. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005;106:1604-11.
36. Reutelingsperger CP, van Heerde WL. Annexin V, the regulator of phosphatidylserine-catalyzed inflammation and coagulation during apoptosis. Cell Mol Life Sci 1997;53:527-32.
37. Lentz BR. Exposure of platelet membrane phosphatidylserine regulates blood coagulation. Prog Lipid Res 2003;42:423-38.
38. Comfurius P, Senden JM, Tilly RH, Schroit AJ, Bevers EM, Zwaal RF. Loss of membrane phospholipid asymmetry in platelets and red cells may be associated with calcium-induced shedding of plasma membrane and inhibition of aminophospholipid translocase. Biochim Biophys Acta 1990;1026:153-60.
39. Dachary-Prigent J, Freyssinet JM, Pasquet JM, Carron JC, Nurden AT. Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: A flow cytometry study showing a role for free sulfhydryl groups. Blood 1993;81:2554-65.
40. Freyssinett JM. Meeting of The International Society on Thrombosis and Haemostasis: 51st Annual Scientific and Standardization Committee Meeting. In: ISTH Working Group on Vascular Biology; 2005 August 6-7. Sydney, Australia; 2005. p. 78-81.
41. 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;109:175-80.
42. Jy W, Horstman LL, Jimenez JJ, Ahn YS, Biró E, Nieuwland R, et al. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004;2:1842-51.
43. Enjeti AK, Lincz LF, Seldon M. Detection and measurement of microparticles: An evolving research tool for vascular biology. Semin Thromb Hemost 2007;33:771-9.
44. Amabile N, Heiss C, Real WM, Minasi P, McGlothlin D, Rame EJ, et al. Circulating endothelial microparticle levels predict hemodynamic severity of pulmonary hypertension. Am J Respir Crit Care Med 2008;177:1268-75.
45. Amabile N, Heiss C, Chang V, Angeli FS, Damon L, Rame EJ, et al. Increased CD62e(+) endothelial microparticle levels predict poor outcome in pulmonary hypertension patients. J Heart Lung Transplant 2009;28:1081-6.
46. Cauwenberghs S, Feijge MA, Harper AG, Sage SO, Curvers J, Heemskerk JW. Shedding of procoagulant microparticles from unstimulated platelets by integrin-mediated destabilization of actin cytoskeleton. FEBS Lett 2006;580:5313-20.
47. Peterson DB, Sander T, Kaul S, Wakim BT, Halligan B, Twigger S, et al. Comparative proteomic analysis of PAI-1 and TNF-alpha-derived endothelial microparticles. Proteomics 2008;8:2430-46.
48. Visovatti SH, Hyman MC, Bouis D, Neubig R, McLaughlin VV, Pinsky DJ. Increased CD39 nucleotidase activity on microparticles from patients with idiopathic pulmonary arterial hypertension. PloS One 2012;7:e40829.
49. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987;262:9412-20.
50. Raposo G, Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol 2013;200:373-83.
51. Lakkaraju A, Rodriguez-Boulan E. Itinerant exosomes: Emerging roles in cell and tissue polarity. Trends Cell Biol 2008;18:199-209.
52. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183:1161-72.
53. Thery C, Regnault A, Garin J, Wolfers J, Zitvogel L, Ricciardi-Castagnoli P, et al. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol 1999;147:599-610.
54. Stein JM, Luzio JP. Ectocytosis caused by sublytic autologous complement attack on human neutrophils. The sorting of endogenous plasma-membrane proteins and lipids into shed vesicles. Biochem J 1991;274 (Pt 2):381-6.
55. Timar CI, Lorincz AM, Csepanyi-Komi R, Vályi-Nagy A, Nagy G, Buzás EI, et al. Antibacterial effect of microvesicles released from human neutrophilic granulocytes. Blood 2013;121:510-8.
56. Morel O, Jesel L, Freyssinet JM, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol 2011;31:15-26.
57. Hugel B, Martinez MC, Kunzelmann C, Freyssinet JM. Membrane microparticles: Two sides of the coin. Physiology (Bethesda) 2005;20:22-7.
58. Chironi G N, Boulanger C M, Simon A, Dignat-George F, Freyssinet JM, Tedgui A. Endothelial microparticles in diseases. Cell Tissue Res 2009;335:143-51.
59. Abid Hussein MN, Boing AN, Sturk A, Hau CM, Nieuwland R. Inhibition of microparticle release triggers endothelial cell apoptosis and detachment. Thromb Haemost 2007;98:1096-107.
60. 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;4:1621-3.
61. Dasgupta SK, Abdel-Monem H, Niravath P, Le A, Bellera RV, Langlois K, et al. Lactadherin and clearance of platelet-derived microvesicles. Blood 2009;113:1332-9.
62. Dasgupta SK, Le A, Chavakis T, Rumbaut RE, Thiagarajan P. Developmental endothelial locus-1 (Del-1) mediates clearance of platelet microparticles by the endothelium. Circulation 2012;125:1664-72.
63. Rank A, Nieuwland R, Crispin A, Grützner S, Iberer M, Toth B, et al. Clearance of platelet microparticles in vivo. Platelets 2011;22:111-6.
64. Hamilton KK, Hattori R, Esmon CT, Sims PJ. Complement proteins C5b-9 induce vesiculation of the endothelial plasma membrane and expose catalytic surface for assembly of the prothrombinase enzyme complex. J Biol Chem 1990;265:3809-14.
65. Horstman LL, Valle-Riestra BJ, Jy W, Wang F, Mao W, Ahn YS. Desmopressin (DDAVP) acts on platelets to generate platelet microparticles and enhanced procoagulant activity. Thromb Res 1995;79:163-74.
66. Holme PA, Orvim U, Hamers MJ, Solum NO, Brosstad FR, Barstad RM, et al. Shear-induced platelet activation and platelet microparticle formation at blood flow conditions as in arteries with a severe stenosis. Arterioscler Thromb Vasc Biol 1997;17:646-53.
67. Vasina EM, Cauwenberghs S, Feijge MA, Heemskerk JW, Weber C, Koenen RR. Microparticles from apoptotic platelets promote resident macrophage differentiation. Cell Death Dis 2011;2:e211.
68. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, et al. Detection of microRNA expression in human peripheral blood microvesicles. PloS One 2008;3:e3694.
69. Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, Biancone L, et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007;110:2440-8.
70. Albanese J, Meterissian S, Kontogiannea M, Dubreuil C, Hand A, Sorba S, et al. Biologically active Fas antigen and its cognate ligand are expressed on plasma membrane-derived extracellular vesicles. Blood 1998;91:3862-74.
71. 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;111:5028-36.
72. Agouni A, Ducluzeau PH, Benameur T, Faure S, Sladkova M, Duluc L, et al. Microparticles from patients with metabolic syndrome induce vascular hypo-reactivity via Fas/Fas-ligand pathway in mice. PloS One 2011;6:e27809.
73. Preston RA, Jy W, Jimenez JJ, Mauro LM, Horstman LL, Valle M, et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 2003;41:211-7.
74. Perez-Casal M, Downey C, Fukudome K, Marx G, Toh CH. Activated protein C induces the release of microparticle-associated endothelial protein C receptor. Blood 2005;105:1515-22.
75. Perez-Casal M, Downey C, Cutillas-Moreno B, Zuzel M, Fukudome K, Toh CH. Microparticle-associated endothelial protein C receptor and the induction of cytoprotective and anti-inflammatory effects. Haematologica 2009;94:387-94.
76. 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;264:17049-57.
77. Boulanger CM, Scoazec A, Ebrahimian T, Henry P, Mathieu E, Tedgui A, et al. Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation 2001;104:2649-52.
78. Mallat Z, Benamer H, Hugel B, Benessiano J, Steg PG, Freyssinet JM, et al. Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 2000;101:841-3.
79. Bernal-Mizrachi L, Jy W, Jimenez JJ, Pastor J, Mauro LM, Horstman LL, et al. High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am Heart J 2003;145:962-70.
80. Gordon C, Gudi K, Krause A, Sackrowitz R, Harvey BG, Strulovici-Barel Y, et al. Circulating endothelial microparticles as a measure of early lung destruction in cigarette smokers. Am J Respir Crit Care Med 2011;184:224-32.
81. McVey M, Tabuchi A, Kuebler WM. Microparticles and acute lung injury. Am J Physiol Lung Cell Mol Physiol 2012;303:L364-81.
82. Tantawy AA, Adly AA, Ismail EA, Habeeb NM, Farouk A. Circulating platelet and erythrocyte microparticles in young children and adolescents with sickle cell disease: Relation to cardiovascular complications. Platelets 2012.
83. Diehl P, Aleker M, Helbing T, Sossong V, Germann M, Sorichter S, et al. Increased platelet, leukocyte and endothelial microparticles predict enhanced coagulation and vascular inflammation in pulmonary hypertension. J Thromb Thrombolysis 2011;31:173-9.
84. Nadaud S, Poirier O, Girerd B, Blanc C, Montani D, Eyries M, et al. Small platelet microparticle levels are increased in pulmonary arterial hypertension. Eur J Clin Invest 2013;43:64-71.
85. Tual-Chalot S, Guibert C, Muller B, Savineau JP, Andriantsitohaina R, Martinez MC. Circulating microparticles from pulmonary hypertensive rats induce endothelial dysfunction. Am J Respir Crit Care Med 2010;182:261-8.
86. Banz Y, Beldi G, Wu Y, Atkinson B, Usheva A, Robson SC. CD39 is incorporated into plasma microparticles where it maintains functional properties and impacts endothelial activation. Br J Haematol 2008;142:627-37.
87. Benson AB, Moss M, Silliman CC. Transfusion-related acute lung injury (TRALI): A clinical review with emphasis on the critically ill. Br J Haematol 2009;147:431-43.
88. Pascual M, Lutz HU, Steiger G, Stammler P, Schifferli JA. Release of vesicles enriched in complement receptor 1 from human erythrocytes. J Immunol 1993;151:397-404.
89. Tung JP, Fung YL, Nataatmadja M, Colebourne KI, Esmaeel HM, Wilson K, et al. A novel in vivo ovine model of transfusion-related acute lung injury (TRALI). Vox Sang 2011;100:219-30.
90. Jy W, Mao WW, Horstman L, Tao J, Ahn YS. Platelet microparticles bind, activate and aggregate neutrophils in vitro. Blood Cells Mol Dis 1995;21:217-31.
91. Brogan PA, Shah V, Brachet C, Harnden A, Mant D, Klein N, et al. Endothelial and platelet microparticles in vasculitis of the young. Arthritis Rheum 2004;50:927-36.
92. Dalli J, Norling LV, Renshaw D, Cooper D, Leung KY, Perretti M. Annexin 1 mediates the rapid anti-inflammatory effects of neutrophilderived microparticles. Blood 2008;112:2512-9.
93. Gasser O, Schifferli JA. Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood 2004;104:2543-8.
94. Tang K, Liu J, Yang Z, Zhang B, Zhang H, Huang C, et al. Microparticles mediate enzyme transfer from platelets to mast cells: A new pathway for lipoxin A4 biosynthesis. Biochem Biophys Res Commun 2010;400:432-6.
95. Steppich B, Mattisek C, Sobczyk D, Kastrati A, Schomig A, Ott I. Tissue factor pathway inhibitor on circulating microparticles in acute myocardial infarction. Thromb Haemost 2005;93:35-9.
96. Capriotti AL, Caruso G, Cavaliere C, Piovesana S, Samperi R, Lagana A. Proteomic characterization of human platelet-derived microparticles. Anal Chim Acta 2013;776:57-63.
97. Watts JA, Lee YY, Gellar MA, Fulkerson MB, Hwang SI, Kline JA. Proteomics of microparticles after experimental pulmonary embolism. Thromb Res 2012;130:122-8.
98. Saas P, Angelot F, Bardiaux L, Seilles E, Garnache-Ottou F, Perruche S. Phosphatidylserine-expressing cell by-products in transfusion: A pro-inflammatory or an anti-inflammatory effect? Transfus Clin Biol 2012;19:90-7