Activated platelets can deliver mRNA regulatory Ago2•microRNA complexes to endothelial cells via microparticles

Blood

Volumn 122, Issue 2, 2013, Pages 253-261

  Laffont, Benoit ^a,b   Corduan, Aurélie ^a,b   Pĺe, Hél̀ene ^a,b   Duchez, Anne Claire ^a,b   Cloutier, Nathalie ^a,b   Boilard, Eric ^a,b   Provost, Patrick ^a,b  

^a Université Laval   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; MESSENGER RNA; MICRORNA 223; THROMBIN; ARGONAUTE PROTEIN; EIF2C2 PROTEIN, HUMAN; MICRORNA; MIRN223 MICRORNA, HUMAN;

ADULT; ARTICLE; BIOACCUMULATION; CIRCULATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INTERNALIZATION; MALE; NORMAL HUMAN; PLATELET MICROPARTICLE; PRIORITY JOURNAL; REPORTER GENE; THROMBOCYTE ACTIVATION; UMBILICAL VEIN ENDOTHELIAL CELL; ENDOTHELIUM CELL; GENETICS; MACROMOLECULE; MEMBRANE MICROPARTICLE; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE; THROMBOCYTE; TRANSPORT AT THE CELLULAR LEVEL;

ARGONAUTE PROTEINS; BIOLOGICAL TRANSPORT; BLOOD PLATELETS; CELL-DERIVED MICROPARTICLES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MACROMOLECULAR SUBSTANCES; MICRORNAS; PLATELET ACTIVATION; RNA INTERFERENCE; RNA, MESSENGER;

EID: 84884490899     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-03-492801     Document Type: Article

References (49)

1. Michelson AD. How platelets work: platelet function and dysfunction. J Thromb Thrombolysis. 2003;16(1-2):7-12. (Pubitemid 38477217)
2. PléH, Landry P, Benham A, Coarfa C, Gunaratne PH, Provost P. The repertoire and features of human platelet microRNAs. PLoS ONE. 2012;7(12):e50746.
3. Landry P, Plante I, Ouellet DL, Perron MP, Rousseau G, Provost P. Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol. 2009;16(9):961-966.
4. Kondkar AA, Bray MS, Leal SM, et al. VAMP8/endobrevin is overexpressed in hyperreactive human platelets: suggested role for platelet microRNA. J Thromb Haemost. 2010;8(2):369-378.
5. Nagalla S, Shaw C, Kong X, et al. Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood. 2011;117(19):5189-5197.
6. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001;294(5543):853-858. (Pubitemid 33032103)
7. Lau NC, Lim LP, Weinstein EG, Bartel DP. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science. 2001;294(5543):858-862. (Pubitemid 33032104)
8. Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Rådmark O. Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J. 2002;21(21):5864-5874. (Pubitemid 35315284)
9. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell. 2004;15(2):185-197. (Pubitemid 38950966)
10. Pillai RS, Bhattacharyya SN, Artus CG, et al. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science. 2005;309(5740):1573-1576. (Pubitemid 41266485)
11. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215-233.
12. Chang TC, Mendell JT. microRNAs in vertebrate physiology and human disease. Annu Rev Genomics Hum Genet. 2007;8:215-239.
13. Kloosterman WP, Plasterk RH. The diverse functions of microRNAs in animal development and disease. Dev Cell. 2006;11(4):441-450. (Pubitemid 44430905)
14. Chen X, Ba Y, Ma L, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18(10):997-1006.
15. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9(6):654-659. (Pubitemid 47214727)
16. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009;19(2):43-51.
17. Zernecke A, Bidzhekov K, Noels H, et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal. 2009;2(100):ra81.
18. Arroyo JD, Chevillet JR, Kroh EM, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA. 2011;108(12):5003-5008.
19. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13(4):423-433.
20. 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)
21. Boilard E, Nigrovic PA, Larabee K, et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science. 2010;327(5965):580-583.
22. Rautou PE, Vion AC, Amabile N, Chironi G, Simon A, Tedgui A, Boulanger CM. Microparticles, vascular function, and atherothrombosis. Circ Res. 2011;109(5):593-606.
23. Risitano A, Beaulieu LM, Vitseva O, Freedman JE. Platelets and platelet-like particles mediate intercellular RNA transfer. Blood. 2012;119(26):6288-6295.
24. Diehl P, Fricke A, Sander L, et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res. 2012;93(4):633-644.
25. Hunter MP, Ismail N, Zhang X, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE. 2008;3(11):e3694.
26. Willeit P, Zampetaki A, Dudek K, et al. Circulating microRNAs as novel biomarkers for platelet activation. Circ Res. 2013;112(4):595-600.
27. Schaefer A, Jung M, Miller K, Lein M, Kristiansen G, Erbersdobler A, Jung K. Suitable reference genes for relative quantification of miRNA expression in prostate cancer. Exp Mol Med. 2010;42(11):749-758.
28. Perron MP, Landry P, Plante I, Provost P. Detection of human Dicer and Argonaute 2 catalytic activity. Methods Mol Biol. 2011;725:121-141.
29. Pépin G, Perron MP, Provost P. Regulation of human Dicer by the resident ER membrane protein CLIMP-63. Nucleic Acids Res. 2012;40(22):11603- 11617.
30. Plé H, Maltais M, Corduan A, Rousseau G, Madore F, Provost P. Alteration of the platelet transcriptome in chronic kidney disease. Thromb Haemost. 2012;108(4):605-615.
31. Cloutier N, Tan S, Boudreau LH, et al. The exposure of autoantigens by microparticles underlies the formation of potent inflammatory components: the microparticle-associated immune complexes. EMBO Mol Med. 2013;5(2):235-249.
32. Voellenkle C, Rooij J, Guffanti A, et al. Deep-sequencing of endothelial cells exposed to hypoxia reveals the complexity of known and novel microRNAs. RNA. 2012;18(3):472-484.
33. Moberg KH, Bell DW, Wahrer DC, Haber DA, Hariharan IK. Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature. 2001;413(6853):311-316. (Pubitemid 32905852)
34. Hirai H, Maru Y, Hagiwara K, Nishida J, Takaku F. A novel putative tyrosine kinase receptor encoded by the eph gene. Science. 1987;238(4834):1717- 1720. (Pubitemid 18046274)
35. Xu Y, Sengupta T, Kukreja L, Minella AC. MicroRNA-223 regulates cyclin E activity by modulating expression of F-box and WD-40 domain protein 7. J Biol Chem. 2010;285(45):34439-34446.
36. 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.
37. Mause SF, Weber C. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res. 2010;107(9):1047-1057.
38. Rak J. Microparticles in cancer. Semin Thromb Hemost. 2010;36(8):888-906.
39. Cloutier N, Paré A, Farndale RW, Schumacher HR, Nigrovic PA, Lacroix S, Boilard E. Platelets can enhance vascular permeability. Blood. 2012;120(6):1334-1343.
40. Owens AP III, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res. 2011;108(10):1284-1297.
41. Ismail N, Wang Y, Dakhlallah D, et al. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood. 2013;121(6):984-995.
42. Iida H, Honda M, Kawai HF, et al. Ephrin-A1 expression contributes to the malignant characteristics of alpha-fetoprotein producing hepatocellular carcinoma. Gut. 2005;54(6):843-851. (Pubitemid 40732104)
43. Calhoun ES, Jones JB, Ashfaq R, et al. BRAF and FBXW7 (CDC4, FBW7, AGO, SEL10) mutations in distinct subsets of pancreatic cancer: potential therapeutic targets. Am J Pathol. 2003;163(4):1255-1260. (Pubitemid 37175075)
44. Wu L, Li H, Jia CY, et al. MicroRNA-223 regulates FOXO1 expression and cell proliferation. FEBS Lett. 2012;586(7):1038-1043.
45. Sugatani T, Hruska KA. MicroRNA-223 is a key factor in osteoclast differentiation. J Cell Biochem. 2007;101(4):996-999. (Pubitemid 47040879)
46. Yuan JY, Wang F, Yu J, Yang GH, Liu XL, Zhang JW. MicroRNA-223 reversibly regulates erythroid and megakaryocytic differentiation of K562 cells. J Cell Mol Med. 2009;13(11-12):4551-4559.
47. Li J, Guo Y, Liang X, Sun M, Wang G, De W, Wu W. MicroRNA-223 functions as an oncogene in human gastric cancer by targeting FBXW7/hCdc4. J Cancer Res Clin Oncol. 2012;138(5):763-774.
48. Gidlöf O, van der Brug M, Ohman J, Gilje P, Olde B, Wahlestedt C, Erlinge D. Platelets activated during myocardial infarction release functional miRNA which can be taken up by endothelial cells and regulate ICAM1 expression. Blood. 2013. In press.
49. Beyer C, Pisetsky DS. The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev Rheumatol. 2010;6(1):21-29.