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Semin Thromb Hemost 2018; 44(03): 206-215
DOI: 10.1055/s-0037-1606568
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Circulating MicroRNA as Thrombosis Sentinels: Caveats and Considerations

Jasmine Tay
1   Western Australian Centre for Thrombosis and Haemostasis (WACTH), Murdoch University, Murdoch, Australia
2   Perth Blood Institute, Nedlands, Australia
,
Jim Tiao
1   Western Australian Centre for Thrombosis and Haemostasis (WACTH), Murdoch University, Murdoch, Australia
2   Perth Blood Institute, Nedlands, Australia
,
Quintin Hughes
1   Western Australian Centre for Thrombosis and Haemostasis (WACTH), Murdoch University, Murdoch, Australia
2   Perth Blood Institute, Nedlands, Australia
,
Jessica Jorritsma
1   Western Australian Centre for Thrombosis and Haemostasis (WACTH), Murdoch University, Murdoch, Australia
,
Grace Gilmore
1   Western Australian Centre for Thrombosis and Haemostasis (WACTH), Murdoch University, Murdoch, Australia
2   Perth Blood Institute, Nedlands, Australia
,
Ross Baker
1   Western Australian Centre for Thrombosis and Haemostasis (WACTH), Murdoch University, Murdoch, Australia
2   Perth Blood Institute, Nedlands, Australia
› Author Affiliations
Further Information

Publication History

Publication Date:
19 September 2017 (online)

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Abstract

The small noncoding RNAs, microRNAs (or miRNAs), have been implicated in a myriad of diseases and accumulating evidence indicate their potential high value as diagnostic biomarkers. Although their roles in hemostasis and coagulation pathways are less defined, many studies have demonstrated their participation in regulating key factors of hemostasis. However, the mounting challenges associated with the accurate measurement of circulating miRNAs and the involvement of platelet activation in contributing to the circulating miRNA expression profile introduce further complexity to the study of thrombosis-associated miRNAs. This review outlines the current knowledge of miRNAs that have been postulated to regulate key hemostatic factors, and miRNA diagnostic panels in thrombotic disease, with a focus on experimental fundamentals, such as selecting condition-specific reference controls, considerations that are crucial for accurate evaluation of miRNAs in the context of disease biomarkers.

Keywords

microRNAs - thrombosis - circulating miRNAs - miR-494 - biomarkers
 

  • References

  • 1 Ambros V. The functions of animal microRNAs. Nature 2004; 431 (7006): 350-355
    CrossrefPubMedSearch in Google Scholar
  • 2 He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5 (07) 522-531
    CrossrefPubMedSearch in Google Scholar
  • 3 Carthew RW. Gene regulation by microRNAs. Curr Opin Genet Dev 2006; 16 (02) 203-208
    CrossrefPubMedSearch in Google Scholar
  • 4 Ouellet DL, Perron MP, Gobeil LA, Plante P, Provost P. MicroRNAs in gene regulation: when the smallest governs it all. J Biomed Biotechnol 2006; 2006 (04) 69616
    PubMedSearch in Google Scholar
  • 5 Chen HH, Huang WT, Yang LW, Lin CW. The PTEN-AKT-mTOR/RICTOR Pathway in nasal natural killer cell lymphoma is activated by miR-494-3p via PTEN but inhibited by miR-142-3p via RICTOR. Am J Pathol 2015; 185 (05) 1487-1499
    CrossrefPubMedSearch in Google Scholar
  • 6 Nie J, Liu L, Zheng W. , et al. microRNA-365, down-regulated in colon cancer, inhibits cell cycle progression and promotes apoptosis of colon cancer cells by probably targeting Cyclin D1 and Bcl-2. Carcinogenesis 2012; 33 (01) 220-225
    CrossrefPubMedSearch in Google Scholar
  • 7 Takagi S, Nakajima M, Kida K, Yamaura Y, Fukami T, Yokoi T. MicroRNAs regulate human hepatocyte nuclear factor 4alpha, modulating the expression of metabolic enzymes and cell cycle. J Biol Chem 2010; 285 (07) 4415-4422
    CrossrefPubMedSearch in Google Scholar
  • 8 Gounaris-Shannon S, Chevassut T. The role of miRNA in haematological malignancy. Bone Marrow Res 2013; 2013: 269107
    PubMedSearch in Google Scholar
  • 9 Bronze-da-Rocha E. MicroRNAs expression profiles in cardiovascular diseases. BioMed Res Int 2014; 2014: 985408
    PubMedSearch in Google Scholar
  • 10 Nishiguchi T, Imanishi T, Akasaka T. MicroRNAs and cardiovascular diseases. BioMed Res Int 2015; 2015: 682857
    PubMedSearch in Google Scholar
  • 11 Chen XM, Huang QC, Yang SL. , et al. Role of microRNAs in the pathogenesis of rheumatoid arthritis: novel perspectives based on review of the literature. Medicine (Baltimore) 2015; 94 (31) e1326
    CrossrefPubMedSearch in Google Scholar
  • 12 Pauley KM, Cha S, Chan EK. MicroRNA in autoimmunity and autoimmune diseases. J Autoimmun 2009; 32 (3-4): 189-194
    CrossrefPubMedSearch in Google Scholar
  • 13 Falanga A, Marchetti M, Vignoli A. Coagulation and cancer: biological and clinical aspects. J Thromb Haemost 2013; 11 (02) 223-233
    CrossrefPubMedSearch in Google Scholar
  • 14 Tracy RP. Thrombin, inflammation, and cardiovascular disease: an epidemiologic perspective. Chest 2003; 124 (3, Suppl): 49S-57S
    CrossrefPubMedSearch in Google Scholar
  • 15 Anglés-Cano E, Guillin MC. Antiphospholipid antibodies and the coagulation cascade. Rheum Dis Clin North Am 2001; 27 (03) 573-586
    CrossrefPubMedSearch in Google Scholar
  • 16 Lee Y, Ahn C, Han J. , et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003; 425 (6956): 415-419
    CrossrefPubMedSearch in Google Scholar
  • 17 Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005; 123 (04) 631-640
    CrossrefPubMedSearch in Google Scholar
  • 18 Witkos TM, Koscianska E, Krzyzosiak WJ. Practical aspects of microRNA target prediction. Curr Mol Med 2011; 11 (02) 93-109
    CrossrefPubMedSearch in Google Scholar
  • 19 Brennecke J, Stark A, Russell RB, Cohen SM. Principles of microRNA-target recognition. PLoS Biol 2005; 3 (03) e85
    CrossrefPubMedSearch in Google Scholar
  • 20 Pasquinelli AE. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 2012; 13 (04) 271-282
    CrossrefPubMedSearch in Google Scholar
  • 21 Ludwig N, Leidinger P, Becker K. , et al. Distribution of miRNA expression across human tissues. Nucleic Acids Res 2016; 44 (08) 3865-3877
    CrossrefPubMedSearch in Google Scholar
  • 22 Diehl P, Fricke A, Sander L. , et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res 2012; 93 (04) 633-644
    CrossrefPubMedSearch in Google Scholar
  • 23 Tay JW, Romeo G, Hughes QW, Baker RI. Micro-ribonucleic acid 494 regulation of protein S expression. J Thromb Haemost 2013; 11 (08) 1547-1555
    CrossrefPubMedSearch in Google Scholar
  • 24 Tay J, Tiao J, Hughes Q, Gilmore G, Baker R. Therapeutic potential of miR-494 in thrombosis and other diseases: a review. Aust J Chem 2016; 69 (10) 1078-1093
    CrossrefPubMedSearch in Google Scholar
  • 25 Ali HO, Arroyo AB, González-Conejero R. , et al. The role of microRNA-27a/b and microRNA-494 in estrogen-mediated downregulation of tissue factor pathway inhibitor α. J Thromb Haemost 2016; 14 (06) 1226-1237
    CrossrefPubMedSearch in Google Scholar
  • 26 Gerrits AJ, Koekman CA, van Haeften TW, Akkerman JW. Increased tissue factor expression in diabetes mellitus type 2 monocytes caused by insulin resistance. J Thromb Haemost 2011; 9 (04) 873-875
    CrossrefPubMedSearch in Google Scholar
  • 27 Rak J, Milsom C, Magnus N, Yu J. Tissue factor in tumour progression. Best Pract Res Clin Haematol 2009; 22 (01) 71-83
    CrossrefPubMedSearch in Google Scholar
  • 28 Funderburg NT, Mayne E, Sieg SF. , et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: relationship to in vivo coagulation and immune activation. Blood 2010; 115 (02) 161-167
    CrossrefPubMedSearch in Google Scholar
  • 29 Holy EW, Tanner FC. Tissue factor in cardiovascular disease pathophysiology and pharmacological intervention. Adv Pharmacol 2010; 59: 259-292
    CrossrefPubMedSearch in Google Scholar
  • 30 Zhang X, Yu H, Lou JR. , et al. MicroRNA-19 (miR-19) regulates tissue factor expression in breast cancer cells. J Biol Chem 2011; 286 (02) 1429-1435
    CrossrefPubMedSearch in Google Scholar
  • 31 Yu G, Li H, Wang X. , et al. MicroRNA-19a targets tissue factor to inhibit colon cancer cells migration and invasion. Mol Cell Biochem 2013; 380 (1-2): 239-247
    CrossrefPubMedSearch in Google Scholar
  • 32 Li S, Ren J, Xu N. , et al. MicroRNA-19b functions as potential anti-thrombotic protector in patients with unstable angina by targeting tissue factor. J Mol Cell Cardiol 2014; 75: 49-57
    CrossrefPubMedSearch in Google Scholar
  • 33 Teruel R, Pérez-Sánchez C, Corral J. , et al. Identification of miRNAs as potential modulators of tissue factor expression in patients with systemic lupus erythematosus and antiphospholipid syndrome. J Thromb Haemost 2011; 9 (10) 1985-1992
    CrossrefPubMedSearch in Google Scholar
  • 34 Li S, Chen H, Ren J. , et al. MicroRNA-223 inhibits tissue factor expression in vascular endothelial cells. Atherosclerosis 2014; 237 (02) 514-520
    CrossrefPubMedSearch in Google Scholar
  • 35 Chuang TD, Luo X, Panda H, Chegini N. miR-93/106b and their host gene, MCM7, are differentially expressed in leiomyomas and functionally target F3 and IL-8. Mol Endocrinol 2012; 26 (06) 1028-1042
    CrossrefPubMedSearch in Google Scholar
  • 36 Eisenreich A, Rauch U. Regulation of the Tissue Factor Isoform Expression and Thrombogenicity of HMEC-1 by miR-126 and miR-19a. Cell Biol: Res Ther 2013; 2 (01)
    CrossrefPubMedSearch in Google Scholar
  • 37 Foekens JA, Peters HA, Look MP. , et al. The urokinase system of plasminogen activation and prognosis in 2780 breast cancer patients. Cancer Res 2000; 60 (03) 636-643
    PubMedSearch in Google Scholar
  • 38 Nielsen HJ, Christensen IJ, Sørensen S, Moesgaard F, Brünner N. Preoperative plasma plasminogen activator inhibitor type-1 and serum C-reactive protein levels in patients with colorectal cancer. The RANX05 Colorectal Cancer Study Group. Ann Surg Oncol 2000; 7 (08) 617-623
    CrossrefPubMedSearch in Google Scholar
  • 39 Andreasen PA. PAI-1 - a potential therapeutic target in cancer. Curr Drug Targets 2007; 8 (09) 1030-1041
    CrossrefPubMedSearch in Google Scholar
  • 40 Palmieri D, Lee JW, Juliano RL, Church FC. Plasminogen activator inhibitor-1 and -3 increase cell adhesion and motility of MDA-MB-435 breast cancer cells. J Biol Chem 2002; 277 (43) 40950-40957
    CrossrefPubMedSearch in Google Scholar
  • 41 Stefansson S, McMahon GA, Petitclerc E, Lawrence DA. Plasminogen activator inhibitor-1 in tumor growth, angiogenesis and vascular remodeling. Curr Pharm Des 2003; 9 (19) 1545-1564
    CrossrefPubMedSearch in Google Scholar
  • 42 Villadsen SB, Bramsen JB, Ostenfeld MS. , et al. The miR-143/-145 cluster regulates plasminogen activator inhibitor-1 in bladder cancer. Br J Cancer 2012; 106 (02) 366-374
    CrossrefPubMedSearch in Google Scholar
  • 43 Patel N, Tahara SM, Malik P, Kalra VK. Involvement of miR-30c and miR-301a in immediate induction of plasminogen activator inhibitor-1 by placental growth factor in human pulmonary endothelial cells. Biochem J 2011; 434 (03) 473-482
    CrossrefPubMedSearch in Google Scholar
  • 44 Luo M, Li R, Ren M. , et al. Hyperglycaemia-induced reciprocal changes in miR-30c and PAI-1 expression in platelets. Sci Rep 2016; 6: 36687
    CrossrefPubMedSearch in Google Scholar
  • 45 Fort A, Borel C, Migliavacca E, Antonarakis SE, Fish RJ, Neerman-Arbez M. Regulation of fibrinogen production by microRNAs. Blood 2010; 116 (14) 2608-2615
    CrossrefPubMedSearch in Google Scholar
  • 46 Salloum-Asfar S, Teruel-Montoya R, Arroyo AB. , et al. Regulation of coagulation factor XI expression by microRNAs in the human liver. PLoS One 2014; 9 (11) e111713
    CrossrefPubMedSearch in Google Scholar
  • 47 Zhao L, Hua C, Li Y, Sun Q, Wu W. miR-525-5p inhibits ADAMTS13 and is correlated with ischemia/reperfusion injury-induced neuronal cell death. Int J Clin Exp Med 2015; 8 (10) 18115-18122
    PubMedSearch in Google Scholar
  • 48 Betel D, Koppal A, Agius P, Sander C, Leslie C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol 2010; 11 (08) R90
    CrossrefPubMedSearch in Google Scholar
  • 49 Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res 2008; 36 (Database issue): D149-D153
    PubMedSearch in Google Scholar
  • 50 Krek A, Grün D, Poy MN. , et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37 (05) 495-500
    CrossrefPubMedSearch in Google Scholar
  • 51 Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136 (02) 215-233
    CrossrefPubMedSearch in Google Scholar
  • 52 Agarwal V, Bell GW, Nam JW, Bartel DP. Predicting effective microRNA target sites in mammalian mRNAs. eLife 2015; 4: e05005
    CrossrefPubMedSearch in Google Scholar
  • 53 Miranda KC, Huynh T, Tay Y. , et al. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 2006; 126 (06) 1203-1217
    CrossrefPubMedSearch in Google Scholar
  • 54 Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA 2004; 10 (10) 1507-1517
    CrossrefPubMedSearch in Google Scholar
  • 55 Huang HY, Chien CH, Jen KH, Huang HD. RegRNA: an integrated web server for identifying regulatory RNA motifs and elements. Nucleic Acids Res 2006; 34 (Web Server issue): W429-34
    PubMedSearch in Google Scholar
  • 56 Maragkakis M, Alexiou P, Papadopoulos GL. , et al. Accurate microRNA target prediction correlates with protein repression levels. BMC Bioinformatics 2009; 10: 295
    CrossrefPubMedSearch in Google Scholar
  • 57 Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120 (01) 15-20
    CrossrefPubMedSearch in Google Scholar
  • 58 Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19 (01) 92-105
    CrossrefPubMedSearch in Google Scholar
  • 59 Hofacker IL. Vienna RNA secondary structure server. Nucleic Acids Res 2003; 31 (13) 3429-3431
    CrossrefPubMedSearch in Google Scholar
  • 60 Liu B, Li J, Cairns MJ. Identifying miRNAs, targets and functions. Brief Bioinform 2014; 15 (01) 1-19
    CrossrefPubMedSearch in Google Scholar
  • 61 Long D, Lee R, Williams P, Chan CY, Ambros V, Ding Y. Potent effect of target structure on microRNA function. Nat Struct Mol Biol 2007; 14 (04) 287-294
    CrossrefPubMedSearch in Google Scholar
  • 62 Reinhart BJ, Slack FJ, Basson M. , et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans . Nature 2000; 403 (6772): 901-906
    CrossrefPubMedSearch in Google Scholar
  • 63 Calin GA, Dumitru CD, Shimizu M. , et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 2002; 99 (24) 15524-15529
    CrossrefPubMedSearch in Google Scholar
  • 64 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
    CrossrefPubMedSearch in Google Scholar
  • 65 Freedman JE, Ercan B, Morin KM. , et al. The distribution of circulating microRNA and their relation to coronary disease. F1000 Res 2012; 1: 50
    CrossrefPubMedSearch in Google Scholar
  • 66 Chen SY, Wang Y, Telen MJ, Chi JT. The genomic analysis of erythrocyte microRNA expression in sickle cell diseases. PLoS One 2008; 3 (06) e2360
    CrossrefPubMedSearch in Google Scholar
  • 67 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 (09) 961-966
    CrossrefPubMedSearch in Google Scholar
  • 68 Mitchell PS, Parkin RK, Kroh EM. , et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A 2008; 105 (30) 10513-10518
    CrossrefPubMedSearch in Google Scholar
  • 69 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
    PubMedSearch in Google Scholar
  • 70 Yamada Y, Enokida H, Kojima S. , et al. MiR-96 and miR-183 detection in urine serve as potential tumor markers of urothelial carcinoma: correlation with stage and grade, and comparison with urinary cytology. Cancer Sci 2011; 102 (03) 522-529
    CrossrefPubMedSearch in Google Scholar
  • 71 Park NJ, Zhou H, Elashoff D. , et al. Salivary microRNA: discovery, characterization, and clinical utility for oral cancer detection. Clin Cancer Res 2009; 15 (17) 5473-5477
    CrossrefPubMedSearch in Google Scholar
  • 72 Gilad S, Meiri E, Yogev Y. , et al. Serum microRNAs are promising novel biomarkers. PLoS One 2008; 3 (09) e3148
    CrossrefPubMedSearch in Google Scholar
  • 73 Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol Med 2014; 20 (08) 460-469
    CrossrefPubMedSearch in Google Scholar
  • 74 Reddy KB. MicroRNA (miRNA) in cancer. Cancer Cell Int 2015; 15: 38
    CrossrefPubMedSearch in Google Scholar
  • 75 Iorio MV, Croce CM. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med 2017; 9 (06) 852
    CrossrefPubMedSearch in Google Scholar
  • 76 Callari M, Dugo M, Musella V. , et al. Comparison of microarray platforms for measuring differential microRNA expression in paired normal/cancer colon tissues. PLoS One 2012; 7 (09) e45105
    CrossrefPubMedSearch in Google Scholar
  • 77 Leidner RS, Li L, Thompson CL. Dampening enthusiasm for circulating microRNA in breast cancer. PLoS One 2013; 8 (03) e57841
    CrossrefPubMedSearch in Google Scholar
  • 78 Farr RJ, Januszewski AS, Joglekar MV. , et al. A comparative analysis of high-throughput platforms for validation of a circulating microRNA signature in diabetic retinopathy. Sci Rep 2015; 5: 10375
    CrossrefPubMedSearch in Google Scholar
  • 79 Mozaffarian D, Benjamin EJ, Go AS. , et al; Writing Group Members; American Heart Association Statistics Committee; Stroke Statistics Subcommittee. Heart disease and stroke statistics-2016 update: a report from the American Heart Association. Circulation 2016; 133 (04) e38-e360
    CrossrefPubMedSearch in Google Scholar
  • 80 Liu DZ, Tian Y, Ander BP. , et al. Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 2010; 30 (01) 92-101
    CrossrefPubMedSearch in Google Scholar
  • 81 Yuan Y, Wang JY, Xu LY, Cai R, Chen Z, Luo BY. MicroRNA expression changes in the hippocampi of rats subjected to global ischemia. J Clin Neurosci 2010; 17 (06) 774-778
    CrossrefPubMedSearch in Google Scholar
  • 82 Peng G, Yuan Y, Wu S, He F, Hu Y, Luo B. MicroRNA let-7e is a potential circulating biomarker of acute stage ischemic stroke. Transl Stroke Res 2015; 6 (06) 437-445
    CrossrefPubMedSearch in Google Scholar
  • 83 Tijsen AJ, Creemers EE, Moerland PD. , et al. MiR423-5p as a circulating biomarker for heart failure. Circ Res 2010; 106 (06) 1035-1039
    CrossrefPubMedSearch in Google Scholar
  • 84 Fukushima Y, Nakanishi M, Nonogi H, Goto Y, Iwai N. Assessment of plasma miRNAs in congestive heart failure. Circ J 2011; 75 (02) 336-340
    CrossrefPubMedSearch in Google Scholar
  • 85 Sondermeijer BM, Bakker A, Halliani A. , et al. Platelets in patients with premature coronary artery disease exhibit upregulation of miRNA340* and miRNA624*. PLoS One 2011; 6 (10) e25946
    CrossrefPubMedSearch in Google Scholar
  • 86 Wang X, Sundquist K, Elf JL. , et al. Diagnostic potential of plasma microRNA signatures in patients with deep-vein thrombosis. Thromb Haemost 2016; 116 (02) 328-336
    Thieme ConnectPubMedSearch in Google Scholar
  • 87 Chomczynski P, Wilfinger WW, Eghbalnia HR, Kennedy A, Rymaszewski M, Mackey K. Inter-individual differences in RNA levels in human peripheral blood. PLoS One 2016; 11 (02) e0148260
    CrossrefPubMedSearch in Google Scholar
  • 88 MacLellan SA, MacAulay C, Lam S, Garnis C. Pre-profiling factors influencing serum microRNA levels. BMC Clin Pathol 2014; 14: 27
    CrossrefPubMedSearch in Google Scholar
  • 89 Willeit P, Zampetaki A, Dudek K. , et al. Circulating microRNAs as novel biomarkers for platelet activation. Circ Res 2013; 112 (04) 595-600
    CrossrefPubMedSearch in Google Scholar
  • 90 Risitano A, Beaulieu LM, Vitseva O, Freedman JE. Platelets and platelet-like particles mediate intercellular RNA transfer. Blood 2012; 119 (26) 6288-6295
    CrossrefPubMedSearch in Google Scholar
  • 91 Laffont B, Corduan A, Plé H. , et al. Activated platelets can deliver mRNA regulatory Ago2•microRNA complexes to endothelial cells via microparticles. Blood 2013; 122 (02) 253-261
    CrossrefPubMedSearch in Google Scholar
  • 92 Mitchell AJ, Gray WD, Hayek SS. , et al. Platelets confound the measurement of extracellular miRNA in archived plasma. Sci Rep 2016; 6: 32651
    CrossrefPubMedSearch in Google Scholar
  • 93 Kroh EM, Parkin RK, Mitchell PS, Tewari M. Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods 2010; 50 (04) 298-301
    CrossrefPubMedSearch in Google Scholar
  • 94 Sourvinou IS, Markou A, Lianidou ES. Quantification of circulating miRNAs in plasma: effect of preanalytical and analytical parameters on their isolation and stability. J Mol Diagn 2013; 15 (06) 827-834
    CrossrefPubMedSearch in Google Scholar
  • 95 Wang K, Yuan Y, Cho JH, McClarty S, Baxter D, Galas DJ. Comparing the microRNA spectrum between serum and plasma. PLoS One 2012; 7 (07) e41561
    CrossrefPubMedSearch in Google Scholar
  • 96 Kirschner MB, Kao SC, Edelman JJ. , et al. Haemolysis during sample preparation alters microRNA content of plasma. PLoS One 2011; 6 (09) e24145
    CrossrefPubMedSearch in Google Scholar
  • 97 Pritchard CC, Kroh E, Wood B. , et al. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res (Phila) 2012; 5 (03) 492-497
    CrossrefPubMedSearch in Google Scholar
  • 98 Iio A, Takagi T, Miki K, Naoe T, Nakayama A, Akao Y. DDX6 post-transcriptionally down-regulates miR-143/145 expression through host gene NCR143/145 in cancer cells. Biochim Biophys Acta 2013; 1829 (10) 1102-1110
    CrossrefPubMedSearch in Google Scholar
  • 99 Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY. MicroRNA-34b and microRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res 2007; 67 (18) 8433-8438
    CrossrefPubMedSearch in Google Scholar
  • 100 Pineles BL, Romero R, Montenegro D. , et al. Distinct subsets of microRNAs are expressed differentially in the human placentas of patients with preeclampsia. Am J Obstet Gynecol 2007; 196 (03) 261.e1-261.e6
    CrossrefPubMedSearch in Google Scholar
  • 101 Benz F, Roderburg C, Vargas Cardenas D. , et al. U6 is unsuitable for normalization of serum miRNA levels in patients with sepsis or liver fibrosis. Exp Mol Med 2013; 45: e42
    CrossrefPubMedSearch in Google Scholar
  • 102 Qi R, Weiland M, Gao XH, Zhou L, Mi QS. Identification of endogenous normalizers for serum microRNAs by microarray profiling: U6 small nuclear RNA is not a reliable normalizer. Hepatology 2012; 55 (05) 1640-1642 , author reply 1642–1643
    PubMedSearch in Google Scholar
  • 103 Song J, Bai Z, Han W. , et al. Identification of suitable reference genes for qPCR analysis of serum microRNA in gastric cancer patients. Dig Dis Sci 2012; 57 (04) 897-904
    CrossrefPubMedSearch in Google Scholar
  • 104 Wang J, Chen J, Chang P. , et al. MicroRNAs in plasma of pancreatic ductal adenocarcinoma patients as novel blood-based biomarkers of disease. Cancer Prev Res (Phila) 2009; 2 (09) 807-813
    CrossrefPubMedSearch in Google Scholar
  • 105 Redova M, Poprach A, Nekvindova J. , et al. Circulating miR-378 and miR-451 in serum are potential biomarkers for renal cell carcinoma. J Transl Med 2012; 10: 55
    CrossrefPubMedSearch in Google Scholar
  • 106 Tay JW, James I, Hughes QW, Tiao JY, Baker RI. Identification of reference miRNAs in plasma useful for the study of oestrogen-responsive miRNAs associated with acquired Protein S deficiency in pregnancy. BMC Res Notes 2017; 10: 312 . Doi: 10.1186/s13104-017-2636-3.
    CrossrefPubMedSearch in Google Scholar
  • 107 Dolz S, Górriz D, Tembl JI. , et al. Circulating microRNAs as novel biomarkers of stenosis progression in asymptomatic carotid stenosis. Stroke 2017; 48 (01) 10-16
    CrossrefPubMedSearch in Google Scholar
  • 108 Ovchinnikova ES, Schmitter D, Vegter EL. , et al. Signature of circulating microRNAs in patients with acute heart failure. Eur J Heart Fail 2016; 18 (04) 414-423
    CrossrefPubMedSearch in Google Scholar
  • 109 Starikova I, Jamaly S, Sorrentino A. , et al. Differential expression of plasma miRNAs in patients with unprovoked venous thromboembolism and healthy control individuals. Thromb Res 2015; 136 (03) 566-572
    CrossrefPubMedSearch in Google Scholar
  • 110 Xiao J, Jing ZC, Ellinor PT. , et al. MicroRNA-134 as a potential plasma biomarker for the diagnosis of acute pulmonary embolism. J Transl Med 2011; 9: 159
    CrossrefPubMedSearch in Google Scholar
  • 111 Sørensen SS, Nygaard AB, Nielsen MY, Jensen K, Christensen T. miRNA expression profiles in cerebrospinal fluid and blood of patients with acute ischemic stroke. Transl Stroke Res 2014; 5 (06) 711-718
    CrossrefPubMedSearch in Google Scholar
  • 112 Wang Y, Ma Z, Kan P, Zhang B. The diagnostic value of serum miRNA-221-3p, miRNA-382-5p, and miRNA-4271 in ischemic stroke. J Stroke Cerebrovasc Dis 2017; 26 (05) 1055-1060
    CrossrefPubMedSearch in Google Scholar
  • 113 Kim BS, Jung JY, Jeon JY, Kim HA, Suh CH. Circulating hsa-miR-30e-5p, hsa-miR-92a-3p, and hsa-miR-223-3p may be novel biomarkers in systemic lupus erythematosus. HLA 2016; 88 (04) 187-193
    CrossrefPubMedSearch in Google Scholar
  • 114 Chen JQ, Papp G, Póliska S. , et al. MicroRNA expression profiles identify disease-specific alterations in systemic lupus erythematosus and primary Sjögren's syndrome. PLoS One 2017; 12 (03) e0174585
    CrossrefPubMedSearch in Google Scholar
  • 115 Pérez-Sánchez C, Aguirre MA, Ruiz-Limón P. , et al. ‘Atherothrombosis-associated microRNAs in antiphospholipid syndrome and systemic lupus erythematosus patients’. Sci Rep 2016; 6: 31375
    CrossrefPubMedSearch in Google Scholar