MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease

Cardiovascular Research

Volumn 100, Issue 1, 2013, Pages 7-18

  Hulsmans, Maarten ^a   Holvoet, Paul ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Atherosclerotic disease; Cell to cell communication; Inflammation; MicroRNAs; Microvesicles

Indexed keywords

BIOLOGICAL MARKER; CATALASE; CD31 ANTIGEN; LIPID; MICRORNA; MICRORNA 125B; MICRORNA 126; MICRORNA 133; MICRORNA 146; MICRORNA 155; MICRORNA 17; MICRORNA 196; MICRORNA 21; MICRORNA 210; MICRORNA 29; P SELECTIN GLYCOPROTEIN LIGAND 1; PROTEIN; PROTEIN C MYB; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ATHEROSCLEROSIS; BLOOD CLOTTING; CARDIOVASCULAR DISEASE; CELL COMMUNICATION; CHRONIC INFLAMMATION; DENDRITIC CELL; DIAGNOSTIC VALUE; DISEASE ASSOCIATION; ENDOTHELIUM CELL; EXOSOME; FIBRIN FORMATION; GENE THERAPY; HUMAN; INFLAMMATORY CELL; INNATE IMMUNITY; LIPID COMPOSITION; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; REVIEW; THROMBOCYTE; THROMBOSIS; TISSUE REGENERATION;

ATHEROSCLEROTIC DISEASE; CELL-TO-CELL COMMUNICATION; INFLAMMATION; MICRORNAS; MICROVESICLES;

ANIMALS; ATHEROSCLEROSIS; BLOOD PLATELETS; CELL COMMUNICATION; CELL-DERIVED MICROPARTICLES; DENDRITIC CELLS; ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; MACROPHAGES; MICRORNAS; NEOPLASMS;

EID: 84880906480     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt161     Document Type: Review

References (161)

1. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9: 581-593.
2. Wickman G, Julian L, Olson MF. How apoptotic cells aidinthe removal of their owncold dead bodies. Cell Death Differ 2012; 19: 735-742.
3. Rosell R, Wei J, Taron M. Circulating microRNA signatures of tumor-derived exosomes for early diagnosis of non-small-cell lung cancer. Clin Lung Cancer 2009; 10: 8-9.
4. Kuwabara Y, Ono K, Horie T., Nishi H, Nagao K, Kinoshita M et al. Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate myocardial damage. Circ Cardiovasc Genet 2011; 4: 446-454.
5. Lachenal G, Pernet-Gallay K, Chivet M., Hemming FJ, Belly A, Bodon G et al. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol Cell Neurosci 2011; 46: 409-418.
6. Vrijsen KR, Sluijter JP, Schuchardt M.W., van Balkom BW, Noort WA, Chamuleau SA et al. Cardiomyocyte progenitor cell-derived exosomes stimulate migration of endo-thelial cells. J Cell Mol Med 2010; 14: 1064-1070.
7. Valadi H, Ekstrom K, Bossios A., Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007; 9: 654-659.
8. Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967; 13: 269-288.
9. Horstman LL, Ahn YS. Platelet microparticles: a wide-angle perspective. Crit Rev Oncol Hematol 1999; 30: 111-142.
10. VanWijk MJ, VanBavel E, Sturk A., Nieuwland R. Microparticles in cardiovascular diseases. Cardiovasc Res 2003; 59: 277-287.
11. Burnier L, Fontana P, Kwak B.R., Angelillo-Scherrer A. Cell-derived microparticles in haemostasis and vascular medicine. Thromb Haemost 2009; 101: 439-451.
12. Nomura S, Ozaki Y, Ikeda Y. Function and role of microparticles in various clinical settings. Thromb Res 2008; 123: 8-23.
13. Angelillo-Scherrer A. Leukocyte-derived microparticles in vascular homeostasis. Circ Res 2012; 110: 356-369.
14. Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006; 444: 860-867.
15. Hulsmans M, Holvoet P. The vicious circle between oxidative stress and inflammation in atherosclerosis. J Cell Mol Med 2010; 14: 70-78.
16. Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: current perspectives. Proteomics 2008; 8: 4083-4099.
17. van Niel G., Porto-Carreiro I, Simoes S., Raposo G. Exosomes: acommon pathway for a specialized function. J Biochem 2006; 140: 13-21.
18. Trajkovic K, Hsu C, Chiantia S., Rajendran L, Wenzel D, Wieland F et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008; 319: 1244-1247.
19. Subra C, Laulagnier K, Perret B., Record M. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie 2007; 89: 205-212.
20. Alonso R, Mazzeo C, Rodriguez M.C., Marsh M., Fraile-Ramos A, Calvo V et al. Diacylgly-cerol kinase alpha regulates the formation and polarisation of mature multivesicular bodies involved in the secretion of Fas ligand-containing exosomes in T lymphocytes. Cell Death Differ 2011; 18: 1161-1173.
21. Schutters K, Reutelingsperger C. Phosphatidylserine targeting for diagnosis and treatment of human diseases. Apoptosis 2010; 15: 1072-1082.
22. Morel O, Jesel L, Freyssinet J.M., Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol 2011; 31: 15-26.
23. Wu Z, Nakanishi H. Phosphatidylserine-containing liposomes: potential pharmacological interventions against inflammatory and immune diseases through the production of prostaglandin E(2) after uptake by myeloid derived phagocytes. Arch Immunol Ther Exp (Warsz) 2011; 59: 195-201.
24. Schneider A, Simons M. Exosomes: vesicular carriers for intercellular communication in neurodegenerative disorders. Cell Tissue Res 2012; 352: 33-47.
25. Simons M, Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009; 21: 575-581.
26. Barteneva NS, Fasler-Kan E, Bernimoulin M., Stern JN, Ponomarev ED, Duckett L et al. Circulating microparticles: square the circle. BMC Cell Biol 2013; 14: 23.
27. Zwaal RF, Schroit AJ. Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 1997; 89: 1121-1132.
28. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol 2009; 19: 43-51.
29. Thery C, Boussac M, Veron P., Ricciardi-Castagnoli P, Raposo G, Garin J et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001; 166: 7309-7318.
30. Amabile N, Rautou PE, Tedgui A, Boulanger CM. Microparticles: key protagonists in cardiovascular disorders. Semin Thromb Hemost 2010; 36: 907-916.
31. Jy W, Horstman LL, Jimenez J.J., Ahn YS, Biro E, Nieuwland R et al. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2: 1842-1851.
32. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002; 2: 569-579.
33. 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.
34. Walenta K, Schwarz V, Schirmer S.H., Kindermann I., Friedrich EB, Solomayer EF et al. Circulating microparticles as indicators of peripartum cardiomyopathy. Eur Heart J 2012; 33: 1469-1479.
35. Heijnen HF, Schiel AE, Fijnheer R, Geuze H.J., 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: 3791-3799.
36. Thery C, Amigorena S, Raposo G., Clayton A. Isolation and characterization of exo-somes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006; Chapter 3:Unit3.22.
37. Lamparski HG, Metha-Damani A, Yao J.Y., Patel S., Hsu DH, Ruegg C et al. Production and characterization of clinical grade exosomes derived from dendritic cells. J Immunol Methods 2002; 270: 211-226.
38. Amabile N, Guerin AP, Leroyer A, Mallat Z., Nguyen C, Boddaert J et al. Circulating endothelial microparticles are associated with vascular dysfunction in patients with end-stage renal failure. J Am Soc Nephrol 2005; 16: 3381-3388.
39. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008; 110: 13-21.
40. van Ierssel S.H., Van Craenenbroeck EM, Conraads VM, Van Tendeloo VF, Vrints CJ, Jorens PG et al. Flow cytometric detection of endothelial microparticles (EMP): effects of centrifugation and storage alter with the phenotype studied. Thromb Res 2010; 125: 332-339.
41. Camussi G, Deregibus MC, Bruno S, Cantaluppi V., Biancone L. Exosomes/microvesi-cles as a mechanism of cell-to-cell communication. Kidney Int 2010; 78: 838-848.
42. Mathivanan S, Lim JW, Tauro B.J., Ji H., Moritz RL, Simpson RJ. Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol Cell Proteomics 2010; 9: 197-208.
43. Martinez MC, Larbret F, Zobairi F., Coulombe J, Debili N, Vainchenker W et al. Transfer of differentiation signal by membrane microvesicles harboring hedgehog morphogens. Blood 2006; 108: 3012-3020.
44. Montecalvo A, Larregina AT, Shufesky W.J., Stolz DB, Sullivan ML, Karlsson JM et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 2012; 119: 756-766.
45. Taylor DD, Gercel-Taylor C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin Immunopathol 2011; 33: 441-454.
46. Diehl P, Fricke A, Sander L., Stamm J, Bassler N, Htun N et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res 2012; 93: 633-644.
47. Tetta C, Ghigo E, Silengo L., Deregibus MC, Camussi G. Extracellular vesicles as an emerging mechanism of cell-to-cell communication. Endocrine 2012; doi: 10.1007/s12020-012-9839-0.
48. Lee Y, El Andaloussi S, Wood MJ. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 2012; 21: R125-R134.
49. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA et al. Unidirectional transferofmicroRNA-loaded exosomes fromTcells to antigen-presenting cells. Nat Commun 2011; 2: 282.
50. Mause SF, Weber C. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res 2010; 107: 1047-1057.
51. Morelli AE, Larregina AT, Shufesky W.J., Sullivan ML, Stolz DB, Papworth GD et al. Endo-cytosis, intracellular sorting, and processingofexosomes by dendritic cells. Blood 2004; 104: 3257-3266.
52. Nolte-'t Hoen EN, Buschow SI, Anderton SM, Stoorvogel W, Wauben MH. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1. Blood 2009; 113: 1977-1981.
53. Aoki N, Yokoyama R, Asai N., Ohki M, Ohki Y, Kusubata K et al. Adipocyte-derived microvesicles are associated with multiple angiogenic factors and induce angiogenesis in vivo and in vitro. Endocrinology 2010; 151: 2567-2576.
54. Hulsmans M, De Keyzer D, Holvoet P. MicroRNAs regulating oxidative stress and inflammation in relation to obesity and atherosclerosis. FASEB J 2011; 25: 2515-2527.
55. Zhang Y, Liu D, Chen X., Li J, Li L, Bian Z et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010; 39: 133-144.
56. Akao Y, Iio A, Itoh T., Noguchi S, Itoh Y, Ohtsuki Y et al. Microvesicle-mediated RNA molecule delivery system using monocytes/macrophages. Mol Ther 2011; 19: 395-399.
57. Habersberger J, Strang F, Scheichl A., Htun N, Bassler N, Merivirta RM et al. Circulating microparticles generate and transport monomeric C-reactive protein in patients with myocardial infarction. Cardiovasc Res 2012; 96: 64-72.
58. Aatonen M, Gronholm M, Siljander PR. Platelet-derived microvesicles: multitalented participants in intercellular communication. Semin Thromb Hemost 2012; 38: 102-113.
59. Tan KT, Lip GY. The potential role of platelet microparticles in atherosclerosis. Thromb Haemost 2005; 94: 488-492.
60. Tan KT, Tayebjee MH, Macfadyen R.J., Lip GY, Blann AD. Elevated platelet microparticles in stable coronary artery disease are unrelated to disease severity or to indices of inflammation. Platelets 2005; 16: 368-371.
61. Tan KT, Tayebjee MH, Lynd C, Blann A.D., Lip GY. Platelet microparticles and soluble P selectin in peripheral artery disease: relationship to extent of disease and platelet activation markers. Ann Med 2005; 37: 61-66.
62. 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: 2577-2582.
63. Barry OP, Pratico D, Savani R.C., FitzGerald GA. Modulation of monocyte-endothelial cell interactions by platelet microparticles. J Clin Invest 1998; 102: 136-144.
64. Kaneider NC, Kaser A, Tilg H., Ricevuti G, Wiedermann CJ. CD40 ligand-dependent maturationofhuman monocyte-derived dendritic cellsbyactivated platelets. IntJImmu-nopathol Pharmacol 2003; 16: 225-231.
65. Sadallah S, Eken C, Martin P.J., Schifferli JA. Microparticles (ectosomes) shed by stored human platelets downregulate macrophages and modify the development of dendritic cells. J Immunol 2011; 186: 6543-6552.
66. Sadallah S, Eken C, Schifferli JA. Ectosomes as modulators of inflammation and immunity. Clin Exp Immunol 2011; 163: 26-32.
67. Weber A, Koppen HO, Schror K. Platelet-derived microparticles stimulate coronary artery smooth muscle cell mitogenesis by a PDGF-independent mechanism. Thromb Res 2000; 98: 461-466.
68. Liu ML, Williams KJ. Microvesicles: potential markers and mediators of endothelial dysfunction. Curr Opin Endocrinol Diabetes Obes 2012; 19: 121-127.
69. Esposito K, Ciotola M, Schisano B., Gualdiero R, Sardelli L, Misso L et al. Endothelial microparticles correlate with endothelial dysfunction in obese women. J Clin Endocrinol Metab 2006; 91: 3676-3679.
70. Navasiolava NM, Dignat-George F, Sabatier F., Larina IM, Demiot C, Fortrat JO et al. Enforced physical inactivity increases endothelial microparticle levels in healthy volunteers. Am J Physiol Heart Circ Physiol 2010; 299:H248-H256.
71. Feng B, Chen Y, Luo Y., Chen M, Li X, Ni Y. Circulating level of microparticles and their correlation with arterial elasticity and endothelium-dependent dilation in patients with type 2 diabetes mellitus. Atherosclerosis 2010; 208: 264-269.
72. Bulut D, Maier K, Bulut-Streich N, Borgel J., Hanefeld C, Mugge A. Circulating endothe-lial microparticles correlate inversely with endothelial function in patients with ische-mic left ventricular dysfunction. J Card Fail 2008; 14: 336-340.
73. Werner N, Wassmann S, Ahlers P., Kosiol S, Nickenig G. Circulating CD31+/annexin V+ apoptotic microparticles correlate with coronary endothelial function in patients with coronary artery disease. Arterioscler Thromb Vasc Biol 2006; 26: 112-116.
74. Nomura S, Inami N, Shouzu A., Urase F, Maeda Y. Correlation and association between plasma platelet-, monocyte- and endothelial cell-derived microparticles in hypertensive patients with type 2 diabetes mellitus. Platelets 2009; 20: 406-414.
75. Preston RA, Jy W, Jimenez J.J., Mauro LM, Horstman LL, Valle M et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 2003; 41: 211-217.
76. Angelot F, Seilles E, Biichle S., Berda Y, Gaugler B, Plumas J et al. Endothelial cell-derived microparticles induce plasmacytoid dendritic cell maturation: potential implications in inflammatory diseases. Haematologica 2009; 94: 1502-1512.
77. Jansen F, Yang X, Franklin B.S., Hoelscher M., Schmitz T, Bedorf J et al. High glucose condition increases NADPH oxidase activity in endothelial microparticles that promote vascular inflammation. Cardiovasc Res 2013; 98: 94-106.
78. Mallat Z, Hugel B, Ohan J., Leseche G, Freyssinet JM, Tedgui A. Shed membrane micro-particles with procoagulant potentialinhuman atherosclerotic plaques: arole for apop-tosis in plaque thrombogenicity. Circulation 1999; 99: 348-353.
79. Ismail N, Wang Y, Dakhlallah D., Moldovan L, Agarwal K, Batte K et al. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 2013; 121: 984-995.
80. Watanabe J, Marathe GK, Neilsen P.O., Weyrich AS, Harrison KA, Murphy RC et al. Endotoxins stimulate neutrophil adhesion followed by synthesis and release of platelet-activating factor in microparticles. J Biol Chem 2003; 278: 33161-33168.
81. Li M, Yu D, Williams K.J., Liu ML. Tobacco smoke induces the generation of procoagulant microvesicles from human monocytes/macrophages. Arterioscler Thromb Vasc Biol 2010; 30: 1818-1824.
82. Freyssinet JM. Cellular microparticles: what are they bad orgood for? J Thromb Haemost 2003; 1: 1655-1662.
83. Liu ML, Scalia R, Mehta J.L., Williams KJ. Cholesterol-induced membrane microvesicles as novel carriers of damage-associated molecular patterns: mechanisms of formation, action, and detoxification. Arterioscler Thromb Vasc Biol 2012; 32: 2113-2121.
84. Neri T, Cordazzo C, Carmazzi Y., Petrini S, Balia C, Stefanelli F et al. Effects of peroxi-some proliferator-activated receptor-gamma agonists on the generation of micropar-ticles by monocytes/macrophages. Cardiovasc Res 2012; 94: 537-544.
85. Morel O, Luca F, Grunebaum L., Jesel L, Meyer N, Desprez D et al. Short-term very low-calorie diet in obese females improves the haemostatic balance through the reduction ofleptin levels, PAI-1concentrations and adiminished release of platelet and leukocyte-derived microparticles. Int J Obes (Lond) 2011; 35: 1479-1486.
86. Soleti R, Lauret E, Andriantsitohaina R., Carmen Martinez M. Internalization and induction of antioxidant messages by microvesicles contribute to the antiapoptotic effects on human endothelial cells. Free Radic Biol Med 2012; 53: 2159-2170.
87. Biro E, Sturk-Maquelin KN, Vogel G.M., Meuleman DG, Smit MJ, Hack CE et al. Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost 2003; 1: 2561-2568.
88. 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: 3190-3197.
89. Furie B, Furie BC. Role of platelet P-selectin and microparticle PSGL-1 inthrombus formation. Trends Mol Med 2004; 10: 171-178.
90. Djuranovic S, Nahvi A, Green R. Aparsimonious model for gene regulationby miRNAs. Science 2011; 331: 550-553.
91. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-297.
92. Fernandez-Hernando C., Ramirez CM, Goedeke L, Suarez Y. MicroRNAs in metabolic disease. Arterioscler Thromb Vasc Biol 2013; 33: 178-185.
93. Liu G, Abraham E. MicroRNAs in immune response and macrophage polarization. Arterioscler Thromb Vasc Biol 2013; 33: 170-177.
94. Schroen B, Heymans S. Small but smart-microRNAs in the centre of inflammatory processes during cardiovascular diseases, the metabolic syndrome, and ageing. Cardiovasc Res 2012; 93: 605-613.
95. Thum T, Mayr M. Review focus on the role of microRNA in cardiovascular biology and disease. Cardiovasc Res 2012; 93: 543-544.
96. Wei Y, Nazari-Jahantigh M, Neth P., Weber C, Schober A. MicroRNA-126, -145, and -155: a therapeutic triad in atherosclerosis? Arterioscler Thromb Vasc Biol 2013; 33: 449-454.
97. Gilad S, Meiri E, Yogev Y., Benjamin S, Lebanony D, Yerushalmi N et al. Serum micro-RNAs are promising novel biomarkers. PLoS One 2008; 3:e3148.
98. Mitchell PS, Parkin RK, Kroh E.M., Fritz BR, Wyman SK, Pogosova-Agadjanyan EL et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105: 10513-10518.
99. Weber JA, Baxter DH, Zhang S, Huang D.Y., Huang KH, Lee MJ et al. The microRNA spectrum in 12 body fluids. Clin Chem 2010; 56: 1733-1741.
100. Ohshima K, Inoue K, Fujiwara A., Hatakeyama K, Kanto K, Watanabe Y et al. Let-7 micro-RNA family isselectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One 2010; 5:e13247.
101. Pigati L, Yaddanapudi SC, Iyengar R, Kim D.J., Hearn SA, Danforth D et al. Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS One 2010; 5:e13515.
102. Xu L, Yang BF, Ai J. MicroRNA transport: a new way in cell communication. J Cell Physiol 2013; 228: 1713-1719.
103. Hergenreider E, Heydt S, Treguer K., Boettger T, Horrevoets AJ, Zeiher AM et al. Ather-oprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 2012; 14: 249-256.
104. Gallo A, Tandon M, Alevizos I., Illei GG. The majority of microRNAs detectablein serum and saliva is concentrated in exosomes. PLoS One 2012; 7:e30679.
105. Muralidharan-Chari V., Clancy J, Plou C., Romao M, Chavrier P, Raposo G et al. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 2009; 19: 1875-1885.
106. Vickers KC, Remaley AT. Lipid-based carriers of microRNAs and intercellular communication. Curr Opin Lipidol 2012; 23: 91-97.
107. Arroyo JD, Chevillet JR, Kroh E.M., Ruf IK, Pritchard CC, Gibson DF et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011; 108: 5003-5008.
108. Vickers KC, Palmisano BT, Shoucri B.M., Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011; 13: 423-433.
109. Turchinovich A, Weiz L, Langheinz A., Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res 2011; 39: 7223-7233.
110. Li L, Zhu D, Huang L., Zhang J, Bian Z, Chen X et al. Argonaute 2 complexes selectively protect the circulating microRNAs in cell-secreted microvesicles. PLoS One 2012; 7: e46957.
111. Boilard E, Nigrovic PA, Larabee K, Watts G.F., Coblyn JS, Weinblatt ME et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010; 327: 580-583.
112. Laffont B, Corduan A, Ple H., Duchez AC, Cloutier N, Boilard E et al. Activated platelets can deliver mRNA regulatory Ago2{middle dot}microRNA complexes to endothelial cells via microparticles. Blood 2013; doi: 10.1182/blood-2013-03-492801.
113. Willeit P, Zampetaki A, Dudek K., Kaudewitz D, King A, Kirkby NS et al. Circulating microRNAs as novel biomarkers for platelet activation. Circ Res 2013; 112: 595-600.
114. Zernecke A, Bidzhekov K, Noels H., Shagdarsuren E, Gan L, Denecke B et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2009; 2:ra81.
115. Harris TA, Yamakuchi M, Ferlito M., Mendell JT, Lowenstein CJ. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA 2008; 105: 1516-1521.
116. Mocharla P, Briand S, Giannotti G., Dorries C, Jakob P, Paneni F et al. AngiomiR-126 expression and secretion from circulating CD34(+) and CD14(+) PBMCs: role for proangiogenic effects and alterations in type 2 diabetics. Blood 2013; 121: 226-236.
117. Zhuang G, Meng C, Guo X., Cheruku PS, Shi L, Xu H et al. A novel regulator of macrophage activation: miR-223 in obesity-associated adiposetissue inflammation. Circulation 2012; 125: 2892-2903.
118. Solinas G, Germano G, Mantovani A., Allavena P. Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 2009; 86: 1065-1073.
119. De Marzo A.M., Platz EA, Sutcliffe S, Xu J., Gronberg H, Drake CG et al. Inflammation in prostate carcinogenesis. Nat Rev Cancer 2007; 7: 256-269.
120. Tili E, Michaille JJ, Croce CM. MicroRNAs play a central role in molecular dysfunctions linking inflammation with cancer. Immunol Rev 2013; 253: 167-184.
121. * against metastasis. Nat Cell Biol 2013; 15: 231-233.
122. Rak J. Extracellular vesicles - biomarkers and effectors of the cellular interactome in cancer. Front Pharmacol 2013; 4: 21.
123. Lee TH, D'Asti E, Magnus N, Al-Nedawi K, Meehan B., Rak J. Microvesicles as mediators of intercellular communication in cancer - the emerging science of cellular 'debris'. Semin Immunopathol 2011; 33: 455-467.
124. Valenti R, Huber V, Filipazzi P., Pilla L, Sovena G, Villa A et al. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res 2006; 66: 9290-9298.
125. Valenti R, Huber V, Iero M., Filipazzi P, Parmiani G, Rivoltini L. Tumor-released micro-vesicles as vehicles of immunosuppression. Cancer Res 2007; 67: 2912-2915.
126. Andreola G, Rivoltini L, Castelli C., Huber V, Perego P, Deho P et al. Induction of lympho-cyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 2002; 195: 1303-1316.
127. Huber V, Fais S, Iero M., Lugini L, Canese P, Squarcina P et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: roleinimmune escape. Gastroenterology 2005; 128: 1796-1804.
128. Zeelenberg IS, Ostrowski M, Krumeich S., Bobrie A, Jancic C, Boissonnas A et al. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res 2008; 68: 1228-1235.
129. Jaiswal R, Luk F, Gong J., Mathys JM, Grau GE, Bebawy M. Microparticle conferred micro-RNA profiles-implications in the transfer and dominance of cancer traits. Mol Cancer 2012; 11: 37.
130. Hornung V, Guenthner-Biller M, Bourquin C., Ablasser A, Schlee M, Uematsu S et al. Sequence-specific potent induction of IFN-alpha byshort interfering RNA inplasmacy-toid dendritic cells through TLR7. Nat Med 2005; 11: 263-270.
131. Judge AD, Sood V, Shaw J.R., Fang D., McClintock K, MacLachlan I. Sequence-dependent stimulation of the mammalian innate immune responsebysynthetic siRNA. Nat Biotech-nol 2005; 23: 457-462.
132. Yang M, Chen J, Su F., Yu B, Su F, Lin L et al. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 2011; 10: 117.
133. Jaiswal R, Gong J, Sambasivam S., Combes V, Mathys JM, Davey R et al. Microparticle-associated nucleic acids mediate trait dominance in cancer. FASEB J 2012; 26: 420-429.
134. Nair N, Kumar S, Gongora E., Gupta S. Circulating miRNAas novel markers for diastolic dysfunction. Mol Cell Biochem 2013; 376: 33-40.
135. Bonauer A, Boon RA, Dimmeler S. Vascular microRNAs. Curr Drug Targets 2010; 11: 943-949.
136. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 2008; 79: 581-588.
137. Zhou M, Cai J, Tang Y., Zhao Q. MiR-17-92 cluster is a novel regulatory gene of cardiac ischemic/reperfusion injury. Med Hypotheses 2013; 81: 108-110.
138. Fabbri M, Paone A, Calore F., Galli R, Croce CM. Anew role for microRNAs, asligands of Toll-like receptors. RNA Biol 2013; 10: 169-174.
139. Li D, Jia H, Zhang H., Lv M, Liu J, Zhang Y et al. TLR4 signaling induces the release of microparticles by tumor cells that regulate inflammatory cytokine IL-6 of macrophages via microRNA let-7b. Oncoimmunology 2012; 1: 687-693.
140. Leitinger N, Schulman IG. Phenotypic polarization of macrophages in atherosclerosis. Arterioscler Thromb Vasc Biol 2013; 33: 1120-1126.
141. Seneviratne A, Hulsmans M, Holvoet P., Monaco C. Biomechanical factors and macrophages in plaque stability. Cardiovasc Res 2013; 99: 284-293.
142. He H, Xu J, Warren C.M., Duan D., Li X, Wu L et al. Endothelial cells provide an instructive niche for the differentiation and functional polarization of M2-like macrophages. Blood 2012; 120: 3152-3162.
143. Alfano M, Graziano F, Genovese L., Poli G. Macrophage polarization at the crossroad between HIV-1 infection and cancer development. Arterioscler Thromb Vasc Biol 2013; 33: 1145-1152.
144. Hulsmans M, Holvoet P. MicroRNAs as early biomarkers in obesity and related metabolic and cardiovascular diseases. Curr Pharm Des 2013; doi:CPD-EPUB-20130220-12.
145. Puntmann VO. How-to guide on biomarkers: biomarker definitions, validation and applications with examples from cardiovascular disease. Postgrad Med J 2009; 85: 538-545.
146. Chen C, Skog J, Hsu C.H., Lessard RT, Balaj L, Wurdinger T et al. Microfluidic isolation and transcriptome analysis of serum microvesicles. Lab Chip 2010; 10: 505-511.
147. Lakhal S, Wood MJ. Exosome nanotechnology: an emerging paradigm shift in drug delivery: exploitation of exosome nanovesicles for systemic in vivo delivery of RNAi heralds new horizons for drug delivery across biological barriers. Bioessays 2011; 33: 737-741.
148. Kooijmans SA, Vader P, van Dommelen SM, van Solinge WW, Schiffelers RM. Exosome mimetics: a novel class of drug delivery systems. Int J Nanomedicine 2012; 7: 1525-1541.
149. Hess C, Sadallah S, Hefti A., Landmann R, Schifferli JA. Ectosomes released by human neutrophils are specialized functional units. J Immunol 1999; 163: 4564-4573.
150. Piccin A, Murphy WG, Smith OP. Circulating microparticles: pathophysiology and clinical implications. Blood Rev 2007; 21: 157-171.
151. Gawaz M, Neumann FJ, Dickfeld T, Reininger A., Adelsberger H, Gebhardt A et al. Vitro-nectin receptor (alpha(v)beta3) mediates platelet adhesion to the luminal aspect of endothelial cells: implications for reperfusion in acute myocardial infarction. Circulation 1997; 96: 1809-1818.
152. Wang H, Wang ZH, Kong J, Yang M.Y., Jiang GH, Wang XP et al. Oxidized low-density lipoprotein-dependent platelet-derived microvesicles trigger procoagulant effects and amplify oxidative stress. Mol Med 2012; 18: 159-166.
153. MacKenzie A, Wilson HL, Kiss-Toth E, Dower S.K., North RA, Surprenant A. Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 2001; 15: 825-835.
154. Li S, Zhu J, Zhang W., Chen Y, Zhang K, Popescu LM et al. Signature microRNA expression profileofessential hypertension and its novel link to human cytomegalovirus infection. Circulation 2011; 124: 175-184.
155. Fichtlscherer S, de Rosa S, Fox H, Schwietz T., Fischer A, Liebetrau C et al. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010; 107: 677-684.
156. Taurino C, Miller WH, McBride M.W., McClure JD, Khanin R, Moreno MU et al. Gene expression profiling in whole blood of patients with coronary artery disease. Clin Sci (Lond) 2010; 119: 335-343.
157. Zampetaki A, Kiechl S, Drozdov I., Willeit P, Mayr U, Prokopi M et al. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ Res 2010; 107: 810-817.
158. D'Alessandra Y., Devanna P, Limana F., Straino S, Di CA, Brambilla PG et al. Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur Heart J 2010; 31: 2765-2773.
159. Corsten MF, Dennert R, Jochems S., Kuznetsova T, Devaux Y, Hofstra L et al. Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet 2010; 3: 499-506.
160. Hulsmans M, Van Dooren E, Mathieu C, Holvoet P. Decrease of miR-146b-5p in mono-cytes during obesity is associated with loss of the anti-inflammatory but not insulin signaling action of adiponectin. PLoS One 2012; 7:e32794.
161. Guo M, Mao X, Ji Q., Lang M, Li S, Peng Y et al. miR-146a in PBMCs modulates Th1 function in patients with acute coronary syndrome. Immunol Cell Biol 2010; 88: 555-564.