Download PDF
CC BY-NC-ND 4.0 · Thromb Haemost 2021; 121(04): 409-421
DOI: 10.1055/s-0040-1718730
Review Article

Methods to Investigate miRNA Function: Focus on Platelet Reactivity

Alix Garcia
1   Geneva Platelet Group, Faculty of Medicine, University of Geneva, Geneva, Switzerland
,
Sylvie Dunoyer-Geindre
1   Geneva Platelet Group, Faculty of Medicine, University of Geneva, Geneva, Switzerland
,
Richard J. Fish
2   Department of Genetic Medicine and Development, University of Geneva, Geneva, Switzerland
,
Marguerite Neerman-Arbez
2   Department of Genetic Medicine and Development, University of Geneva, Geneva, Switzerland
3   iGE3, Institute of Genetics and Genomics in Geneva, Geneva, Switzerland
,
Jean-Luc Reny
1   Geneva Platelet Group, Faculty of Medicine, University of Geneva, Geneva, Switzerland
4   Division of General Internal Medicine, Geneva University Hospitals, Geneva, Switzerland
,
Pierre Fontana
1   Geneva Platelet Group, Faculty of Medicine, University of Geneva, Geneva, Switzerland
5   Division of Angiology and Haemostasis, Geneva University Hospitals, Geneva, Switzerland
› Author Affiliations Funding This work was supported by the Private Foundation of the University Hospitals of Geneva (grant RC04–05).
› Further Information
Also available at
   Permissions and Reprints

Abstract

MicroRNAs (miRNAs) are small noncoding RNAs modulating protein production. They are key players in regulation of cell function and are considered as biomarkers in several diseases. The identification of the proteins they regulate, and their impact on cell physiology, may delineate their role as diagnostic or prognostic markers and identify new therapeutic strategies. During the last 3 decades, development of a large panel of techniques has given rise to multiple models dedicated to the study of miRNAs. Since plasma samples are easily accessible, circulating miRNAs can be studied in clinical trials. To quantify miRNAs in numerous plasma samples, the choice of extraction and purification techniques, as well as normalization procedures, are important for comparisons of miRNA levels in populations and over time. Recent advances in bioinformatics provide tools to identify putative miRNAs targets that can then be validated with dedicated assays. In vitro and in vivo approaches aim to functionally validate candidate miRNAs from correlations and to understand their impact on cellular processes. This review describes the advantages and pitfalls of the available techniques for translational research to study miRNAs with a focus on their role in regulating platelet reactivity.

Keywords

microRNAs - biomarkers - experimental studies - translational research - platelet function

Authors' Contributions

A.G. had the initial idea and conceptualized this work, A.G., S.D.-G., and P.F. wrote the first draft of the manuscript. J.-L.R., M.N.-A., and R.J.F. critically revised the manuscript. All authors approved the manuscript.




Publication History

Received: 09 July 2020

Accepted: 08 September 2020

Article published online:
29 October 2020

© 2020. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Thon JN, Italiano JE. Platelet formation. Semin Hematol 2010; 47 (03) 220-226
    CrossrefPubMedSearch in Google Scholar
  • 2 Bray PF, Mathias RA, Faraday N. et al. Heritability of platelet function in families with premature coronary artery disease. J Thromb Haemost 2007; 5 (08) 1617-1623
    CrossrefPubMedSearch in Google Scholar
  • 3 Reny JL, De Moerloose P, Dauzat M, Fontana P. Use of the PFA-100 closure time to predict cardiovascular events in aspirin-treated cardiovascular patients: a systematic review and meta-analysis. J Thromb Haemost 2008; 6 (03) 444-450
    CrossrefPubMedSearch in Google Scholar
  • 4 Combescure C, Fontana P, Mallouk N. et al. CLOpidogrel and Vascular ISchemic Events Meta-analysis Study Group. Clinical implications of clopidogrel non-response in cardiovascular patients: a systematic review and meta-analysis. J Thromb Haemost 2010; 8 (05) 923-933
    PubMedSearch in Google Scholar
  • 5 Tantry US, Gurbel PA. Antiplatelet drug resistance and variability in response: the role of antiplatelet therapy monitoring. Curr Pharm Des 2013; 19 (21) 3795-3815
    CrossrefPubMedSearch in Google Scholar
  • 6 Shuldiner AR, O'Connell JR, Bliden KP. et al. Association of cytochrome P450 2C19 genotype with the antiplatelet effect and clinical efficacy of clopidogrel therapy. JAMA 2009; 302 (08) 849-857
    CrossrefPubMedSearch in Google Scholar
  • 7 Edelstein LC, McKenzie SE, Shaw C, Holinstat MA, Kunapuli SP, Bray PF. MicroRNAs in platelet production and activation. J Thromb Haemost 2013; 11 (Suppl. 01) 340-350
    CrossrefPubMedSearch in Google Scholar
  • 8 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
  • 9 Kaudewitz D, Skroblin P, Bender LH. et al. Association of MicroRNAs and YRNAs with platelet function. Circ Res 2016; 118 (03) 420-432
    CrossrefPubMedSearch in Google Scholar
  • 10 Shi R, Zhou X, Ji WJ. et al. The emerging role of miR-223 in platelet reactivity: implications in antiplatelet therapy. BioMed Res Int 2015; 2015: 981841
    PubMedSearch in Google Scholar
  • 11 Zufferey A, Ibberson M, Reny JL. et al. New molecular insights into modulation of platelet reactivity in aspirin-treated patients using a network-based approach. Hum Genet 2016; 135 (04) 403-414
    CrossrefPubMedSearch in Google Scholar
  • 12 Zufferey A, Kapur R, Semple JW. Pathogenesis and therapeutic mechanisms in immune thrombocytopenia (ITP). J Clin Med 2017; 6 (02) E16
    CrossrefPubMedSearch in Google Scholar
  • 13 Leblanc R, Peyruchaud O. Metastasis: new functional implications of platelets and megakaryocytes. Blood 2016; 128 (01) 24-31
    CrossrefPubMedSearch in Google Scholar
  • 14 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
  • 15 Semple JW, Italiano Jr JE, Freedman J. Platelets and the immune continuum. Nat Rev Immunol 2011; 11 (04) 264-274
    CrossrefPubMedSearch in Google Scholar
  • 16 Leblanc R, Houssin A, Peyruchaud O. Platelets, autotaxin and lysophosphatidic acid signalling: win-win factors for cancer metastasis. Br J Pharmacol 2018; 175 (15) 3100-3110
    CrossrefPubMedSearch in Google Scholar
  • 17 Alles J, Fehlmann T, Fischer U. et al. An estimate of the total number of true human miRNAs. Nucleic Acids Res 2019; 47 (07) 3353-3364
    CrossrefPubMedSearch in Google Scholar
  • 18 Plé H, Landry P, Benham A, Coarfa C, Gunaratne PH, Provost P. The repertoire and features of human platelet microRNAs. PLoS One 2012; 7 (12) e50746
    CrossrefPubMedSearch in Google Scholar
  • 19 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
    Search in Google Scholar
  • 20 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 U S A 2011; 108 (12) 5003-5008
    CrossrefPubMedSearch in Google Scholar
  • 21 O'Brien K, Breyne K, Ughetto S, Laurent LC, Breakefield XO. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol 2020
    Search in Google Scholar
  • 22 Provost P. The clinical significance of platelet microparticle-associated microRNAs. Clin Chem Lab Med 2017; 55 (05) 657-666
    CrossrefPubMedSearch in Google Scholar
  • 23 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
  • 24 Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11 (03) 228-234
    CrossrefPubMedSearch in Google Scholar
  • 25 Yang JS, Lai EC. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell 2011; 43 (06) 892-903
    CrossrefPubMedSearch in Google Scholar
  • 26 Desvignes T, Batzel P, Berezikov E. et al. miRNA nomenclature: a view incorporating genetic origins, biosynthetic pathways, and sequence variants. Trends Genet 2015; 31 (11) 613-626
    CrossrefPubMedSearch in Google Scholar
  • 27 Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007; 27 (01) 91-105
    CrossrefPubMedSearch in Google Scholar
  • 28 Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136 (02) 215-233
    CrossrefPubMedSearch in Google Scholar
  • 29 Xia L, Zeng Z, Tang WH. The role of platelet microparticle associated microRNAs in cellular crosstalk. Front Cardiovasc Med 2018; 5: 29
    CrossrefPubMedSearch in Google Scholar
  • 30 Camaioni C, Gustapane M, Cialdella P, Della Bona R, Biasucci LM. Microparticles and microRNAs: new players in the complex field of coagulation. Intern Emerg Med 2013; 8 (04) 291-296
    CrossrefPubMedSearch in Google Scholar
  • 31 Anene C, Graham AM, Boyne J, Roberts W. Platelet microparticle delivered microRNA-Let-7a promotes the angiogenic switch. Biochim Biophys Acta Mol Basis Dis 2018; 1864 (08) 2633-2643
    CrossrefPubMedSearch in Google Scholar
  • 32 Sunderland N, Skroblin P, Barwari T. et al. MicroRNA biomarkers and platelet reactivity: the clot thickens. Circ Res 2017; 120 (02) 418-435
    CrossrefPubMedSearch in Google Scholar
  • 33 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 (02) 369-378
    CrossrefPubMedSearch in Google Scholar
  • 34 Shi R, Ge L, Zhou X. et al. Decreased platelet miR-223 expression is associated with high on-clopidogrel platelet reactivity. Thromb Res 2013; 131 (06) 508-513
    CrossrefPubMedSearch in Google Scholar
  • 35 Fontana P, Roffi M, Reny JL. Platelet function test use for patients with coronary artery disease in the early 2020s. J Clin Med 2020; 9 (01) E194
    CrossrefPubMedSearch in Google Scholar
  • 36 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
  • 37 Kaudewitz D, Lee R, Willeit P. et al. Impact of intravenous heparin on quantification of circulating microRNAs in patients with coronary artery disease. Thromb Haemost 2013; 110 (03) 609-615
    Thieme ConnectPubMedSearch in Google Scholar
  • 38 Fejes Z, Póliska S, Czimmerer Z. et al. Hyperglycaemia suppresses microRNA expression in platelets to increase P2RY12 and SELP levels in type 2 diabetes mellitus. Thromb Haemost 2017; 117 (03) 529-542
    Thieme ConnectPubMedSearch in Google Scholar
  • 39 Cazenave JP, Ohlmann P, Cassel D, Eckly A, Hechler B, Gachet C. Preparation of washed platelet suspensions from human and rodent blood. Methods Mol Biol 2004; 272: 13-28
    Search in Google Scholar
  • 40 Tran JQD, Pedersen OH, Larsen ML. et al. Platelet microRNA expression and association with platelet maturity and function in patients with essential thrombocythemia. Platelets 2020; 31 (03) 365-372
    CrossrefPubMedSearch in Google Scholar
  • 41 Binderup HG, Madsen JS, Heegaard NHH, Houlind K, Andersen RF, Brasen CL. Quantification of microRNA levels in plasma - impact of preanalytical and analytical conditions. PLoS One 2018; 13 (07) e0201069
    CrossrefPubMedSearch in Google Scholar
  • 42 Cheng HH, Yi HS, Kim Y. et al. Plasma processing conditions substantially influence circulating microRNA biomarker levels. PLoS One 2013; 8 (06) e64795
    CrossrefPubMedSearch in Google Scholar
  • 43 Tiberio P, Callari M, Angeloni V, Daidone MG, Appierto V. Challenges in using circulating miRNAs as cancer biomarkers. BioMed Res Int 2015; 2015: 731479
    CrossrefPubMedSearch in Google Scholar
  • 44 Jansen F, Schäfer L, Wang H. et al. Kinetics of circulating MicroRNAs in response to cardiac stress in patients with coronary artery disease. J Am Heart Assoc 2017; 6 (08) e005270
    CrossrefPubMedSearch in Google Scholar
  • 45 Zampetaki A, Willeit P, Tilling L. et al. Prospective study on circulating MicroRNAs and risk of myocardial infarction. J Am Coll Cardiol 2012; 60 (04) 290-299
    CrossrefPubMedSearch in Google Scholar
  • 46 Blondal T, Jensby Nielsen S, Baker A. et al. Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods 2013; 59 (01) S1-S6
    CrossrefPubMedSearch in Google Scholar
  • 47 Simon LM, Edelstein LC, Nagalla S. et al. Human platelet microRNA-mRNA networks associated with age and gender revealed by integrated plateletomics. Blood 2014; 123 (16) e37-e45
    CrossrefPubMedSearch in Google Scholar
  • 48 Coenen-Stass AML, Magen I, Brooks T. et al. Evaluation of methodologies for microRNA biomarker detection by next generation sequencing. RNA Biol 2018; 15 (08) 1133-1145
    PubMedSearch in Google Scholar
  • 49 Pordzik J, Jakubik D, Jarosz-Popek J. et al. Significance of circulating microRNAs in diabetes mellitus type 2 and platelet reactivity: bioinformatic analysis and review. Cardiovasc Diabetol 2019; 18 (01) 113
    CrossrefPubMedSearch in Google Scholar
  • 50 Jakob P, Kacprowski T, Briand-Schumacher S. et al. Profiling and validation of circulating microRNAs for cardiovascular events in patients presenting with ST-segment elevation myocardial infarction. Eur Heart J 2017; 38 (07) 511-515
    PubMedSearch in Google Scholar
  • 51 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
  • 52 McDonald JS, Milosevic D, Reddi HV, Grebe SK, Algeciras-Schimnich A. Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem 2011; 57 (06) 833-840
    CrossrefPubMedSearch in Google Scholar
  • 53 Tanaka M, Oikawa K, Takanashi M. et al. Down-regulation of miR-92 in human plasma is a novel marker for acute leukemia patients. PLoS One 2009; 4 (05) e5532
    CrossrefPubMedSearch in Google Scholar
  • 54 Zalewski K, Misiek M, Kowalik A. et al. Normalizers for microRNA quantification in plasma of patients with vulvar intraepithelial neoplasia lesions and vulvar carcinoma. Tumour Biol 2017; 39 (11) 1010428317717140
    Search in Google Scholar
  • 55 Mompeón A, Ortega-Paz L, Vidal-Gómez X. et al. Disparate miRNA expression in serum and plasma of patients with acute myocardial infarction: a systematic and paired comparative analysis. Sci Rep 2020; 10 (01) 5373
    CrossrefPubMedSearch in Google Scholar
  • 56 Li Y, Xiang GM, Liu LL. et al. Assessment of endogenous reference gene suitability for serum exosomal microRNA expression analysis in liver carcinoma resection studies. Mol Med Rep 2015; 12 (03) 4683-4691
    CrossrefPubMedSearch in Google Scholar
  • 57 Kok MG, Halliani A, Moerland PD, Meijers JC, Creemers EE, Pinto-Sietsma SJ. Normalization panels for the reliable quantification of circulating microRNAs by RT-qPCR. FASEB J 2015; 29 (09) 3853-3862
    CrossrefPubMedSearch in Google Scholar
  • 58 Garcia A, Dunoyer-Geindre S, Zapilko V, Nolli S, Reny JL, Fontana P. Functional validation of microRNA-126-3p as a platelet reactivity regulator using human haematopoietic stem cells. Thromb Haemost 2019; 119 (02) 254-263
    Thieme ConnectPubMedSearch in Google Scholar
  • 59 Chou CH, Lin FM, Chou MT. et al. A computational approach for identifying microRNA-target interactions using high-throughput CLIP and PAR-CLIP sequencing. BMC Genomics 2013; 14 (Suppl. 01) S2
    CrossrefPubMedSearch in Google Scholar
  • 60 Hafner M, Landthaler M, Burger L. et al. PAR-CliP–a method to identify transcriptome-wide the binding sites of RNA binding proteins. J Vis Exp 2010; (41) 2034
    PubMedSearch in Google Scholar
  • 61 Helwak A, Kudla G, Dudnakova T, Tollervey D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 2013; 153 (03) 654-665
    CrossrefPubMedSearch in Google Scholar
  • 62 Steinkraus BR, Toegel M, Fulga TA. Tiny giants of gene regulation: experimental strategies for microRNA functional studies. Wiley Interdiscip Rev Dev Biol 2016; 5 (03) 311-362
    CrossrefPubMedSearch in Google Scholar
  • 63 Hafner M, Landthaler M, Burger L. et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010; 141 (01) 129-141
    CrossrefPubMedSearch in Google Scholar
  • 64 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
  • 65 Quillet A, Saad C, Ferry G. et al. Improving bioinformatics prediction of microRNA targets by ranks aggregation. Front Genet 2020; 10: 1330
    CrossrefPubMedSearch in Google Scholar
  • 66 Chu YW, Chang KP, Chen CW, Liang YT, Soh ZT, Hsieh LC. miRgo: integrating various off-the-shelf tools for identification of microRNA-target interactions by heterogeneous features and a novel evaluation indicator. Sci Rep 2020; 10 (01) 1466
    CrossrefPubMedSearch in Google Scholar
  • 67 Moore AC, Winkjer JS, Tseng TT. Bioinformatics resources for MicroRNA discovery. Biomark Insights 2016; 10 (Suppl. 04) 53-58
    PubMedSearch in Google Scholar
  • 68 Huntley RP, Sitnikov D, Orlic-Milacic M. et al. Guidelines for the functional annotation of microRNAs using the Gene Ontology. RNA 2016; 22 (05) 667-676
    CrossrefPubMedSearch in Google Scholar
  • 69 Deng L, Wang J, Zhang J. Predicting gene ontology function of human MicroRNAs by integrating multiple networks. Front Genet 2019; 10: 3
    CrossrefPubMedSearch in Google Scholar
  • 70 Cloonan N. Re-thinking miRNA-mRNA interactions: intertwining issues confound target discovery. BioEssays 2015; 37 (04) 379-388
    CrossrefPubMedSearch in Google Scholar
  • 71 Tan SM, Lieberman J. Capture and identification of miRNA targets by biotin pulldown and RNA-seq. Methods Mol Biol 2016; 1358: 211-228
    CrossrefPubMedSearch in Google Scholar
  • 72 Jin Y, Chen Z, Liu X, Zhou X. Evaluating the microRNA targeting sites by luciferase reporter gene assay. Methods Mol Biol 2013; 936: 117-127
    CrossrefPubMedSearch in Google Scholar
  • 73 Bianchi E, Bulgarelli J, Ruberti S. et al. MYB controls erythroid versus megakaryocyte lineage fate decision through the miR-486-3p-mediated downregulation of MAF. Cell Death Differ 2015; 22 (12) 1906-1921
    CrossrefPubMedSearch in Google Scholar
  • 74 Hong W, Kondkar AA, Nagalla S. et al. Transfection of human platelets with short interfering RNA. Clin Transl Sci 2011; 4 (03) 180-182
    CrossrefPubMedSearch in Google Scholar
  • 75 Edelstein LC, Simon LM, Montoya RT. et al. Racial differences in human platelet PAR4 reactivity reflect expression of PCTP and miR-376c. Nat Med 2013; 19 (12) 1609-1616
    CrossrefPubMedSearch in Google Scholar
  • 76 Dhenge A, Kuhikar R, Kale V, Limaye L. Regulation of differentiation of MEG01 to megakaryocytes and platelet-like particles by valproic acid through Notch3 mediated actin polymerization. Platelets 2019; 30 (06) 780-795
    CrossrefPubMedSearch in Google Scholar
  • 77 Barwari T, Eminaga S, Mayr U. et al. Inhibition of profibrotic microRNA-21 affects platelets and their releasate. JCI Insight 2018; 3 (21) 123335
    CrossrefPubMedSearch in Google Scholar
  • 78 Woolthuis CM, Park CY. Hematopoietic stem/progenitor cell commitment to the megakaryocyte lineage. Blood 2016; 127 (10) 1242-1248
    CrossrefPubMedSearch in Google Scholar
  • 79 Sim X, Poncz M, Gadue P, French DL. Understanding platelet generation from megakaryocytes: implications for in vitro-derived platelets. Blood 2016; 127 (10) 1227-1233
    CrossrefPubMedSearch in Google Scholar
  • 80 Romania P, Lulli V, Pelosi E, Biffoni M, Peschle C, Marziali G. MicroRNA 155 modulates megakaryopoiesis at progenitor and precursor level by targeting Ets-1 and Meis1 transcription factors. Br J Haematol 2008; 143 (04) 570-580
    PubMedSearch in Google Scholar
  • 81 Choi ES, Nichol JL, Hokom MM, Hornkohl AC, Hunt P. Platelets generated in vitro from proplatelet-displaying human megakaryocytes are functional. Blood 1995; 85 (02) 402-413
    CrossrefPubMedSearch in Google Scholar
  • 82 Sangkuhl K, Shuldiner AR, Klein TE, Altman RB. Platelet aggregation pathway. Pharmacogenet Genomics 2011; 21 (08) 516-521
    CrossrefPubMedSearch in Google Scholar
  • 83 Kamat V, Muthard RW, Li R, Diamond SL. Microfluidic assessment of functional culture-derived platelets in human thrombi under flow. Exp Hematol 2015; 43 (10) 891.e4-900.e4
    CrossrefPubMedSearch in Google Scholar
  • 84 Auber M, Fröhlich D, Drechsel O, Karaulanov E, Krämer-Albers EM. Serum-free media supplements carry miRNAs that co-purify with extracellular vesicles. J Extracell Vesicles 2019; 8 (01) 1656042
    CrossrefPubMedSearch in Google Scholar
  • 85 Basak I, Bhatlekar S, Manne BK. et al. miR-15a-5p regulates expression of multiple proteins in the megakaryocyte GPVI signaling pathway. J Thromb Haemost 2019; 17 (03) 511-524
    CrossrefPubMedSearch in Google Scholar
  • 86 Wang T, Larcher LM, Ma L, Veedu RN. Systematic screening of commonly used commercial transfection reagents towards efficient transfection of single-stranded oligonucleotides. Molecules 2018; 23 (10) E2564
    CrossrefPubMedSearch in Google Scholar
  • 87 Spinello I, Quaranta MT, Pasquini L. et al. PLZF-mediated control on c-kit expression in CD34(+) cells and early erythropoiesis. Oncogene 2009; 28 (23) 2276-2288
    CrossrefPubMedSearch in Google Scholar
  • 88 Diener Y, Bosio A, Bissels U. Delivery of RNA-based molecules to human hematopoietic stem and progenitor cells for modulation of gene expression. Exp Hematol 2016; 44 (11) 991-1001
    CrossrefPubMedSearch in Google Scholar
  • 89 Zhou Y, Abraham S, Andre P. et al. Anti-miR-148a regulates platelet FcγRIIA signaling and decreases thrombosis in vivo in mice. Blood 2015; 126 (26) 2871-2881
    CrossrefPubMedSearch in Google Scholar
  • 90 Maurisse R, De Semir D, Emamekhoo H. et al. Comparative transfection of DNA into primary and transformed mammalian cells from different lineages. BMC Biotechnol 2010; 10: 9
    CrossrefPubMedSearch in Google Scholar
  • 91 Sharifi Tabar M, Hesaraki M, Esfandiari F, Sahraneshin Samani F, Vakilian H, Baharvand H. Evaluating electroporation and lipofectamine approaches for transient and stable transgene expressions in human fibroblasts and embryonic stem cells. Cell J 2015; 17 (03) 438-450
    PubMedSearch in Google Scholar
  • 92 Jin HY, Gonzalez-Martin A, Miletic AV. et al. Transfection of microRNA mimics should be used with caution. Front Genet 2015; 6: 340
    PubMedSearch in Google Scholar
  • 93 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
    CrossrefPubMedSearch in Google Scholar
  • 94 Kurreck J. Antisense technologies. Improvement through novel chemical modifications. Eur J Biochem 2003; 270 (08) 1628-1644
    CrossrefPubMedSearch in Google Scholar
  • 95 Soifer HS, Koch T, Lai J. et al. Silencing of gene expression by gymnotic delivery of antisense oligonucleotides. Methods Mol Biol 2012; 815: 333-346
    CrossrefPubMedSearch in Google Scholar
  • 96 Flierl U, Nero TL, Lim B. et al. Phosphorothioate backbone modifications of nucleotide-based drugs are potent platelet activators. J Exp Med 2015; 212 (02) 129-137
    CrossrefPubMedSearch in Google Scholar
  • 97 Cao F, Xie X, Gollan T. et al. Comparison of gene-transfer efficiency in human embryonic stem cells. Mol Imaging Biol 2010; 12 (01) 15-24
    CrossrefPubMedSearch in Google Scholar
  • 98 Vian L, Di Carlo M, Pelosi E. et al. Transcriptional fine-tuning of microRNA-223 levels directs lineage choice of human hematopoietic progenitors. Cell Death Differ 2014; 21 (02) 290-301
    CrossrefPubMedSearch in Google Scholar
  • 99 Nazari B, Soleimani M, Ebrahimi-Barough S. et al. Overexpression of miR-219 promotes differentiation of human induced pluripotent stem cells into pre-oligodendrocyte. J Chem Neuroanat 2018; 91: 8-16
    CrossrefPubMedSearch in Google Scholar
  • 100 van Til NP, Wagemaker G. Lentiviral gene transduction of mouse and human hematopoietic stem cells. Methods Mol Biol 2014; 1185: 311-319
    CrossrefPubMedSearch in Google Scholar
  • 101 Sebrow J, Goff SP, Griffin DO. Successfully transfected primary peripherally mobilized human CD34+ hematopoietic stem and progenitor cells (HSPCs) demonstrate increased susceptibility to retroviral infection. Virol J 2020; 17 (01) 22
    CrossrefPubMedSearch in Google Scholar
  • 102 Lataniotis L, Albrecht A, Kok FO. et al. CRISPR/Cas9 editing reveals novel mechanisms of clustered microRNA regulation and function. Sci Rep 2017; 7 (01) 8585
    CrossrefPubMedSearch in Google Scholar
  • 103 Kim YK, Wee G, Park J. et al. TALEN-based knockout library for human microRNAs. Nat Struct Mol Biol 2013; 20 (12) 1458-1464
    CrossrefPubMedSearch in Google Scholar
  • 104 Mir P, Ritter M, Welte K, Skokowa J, Klimiankou M. Gene knockout in hematopoietic stem and progenitor cells followed by granulocytic differentiation. Methods Mol Biol 2020; 2115: 455-469
    CrossrefPubMedSearch in Google Scholar
  • 105 Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75 (05) 843-854
    CrossrefPubMedSearch in Google Scholar
  • 106 Carthew RW, Agbu P, Giri R. MicroRNA function in Drosophila melanogaster. Semin Cell Dev Biol 2017; 65: 29-37
    CrossrefPubMedSearch in Google Scholar
  • 107 Schier AF, Giraldez AJ. MicroRNA function and mechanism: insights from zebra fish. Cold Spring Harb Symp Quant Biol 2006; 71: 195-203
    CrossrefPubMedSearch in Google Scholar
  • 108 Lewis MA, Steel KP. MicroRNAs in mouse development and disease. Semin Cell Dev Biol 2010; 21 (07) 774-780
    CrossrefPubMedSearch in Google Scholar
  • 109 Pal AS, Kasinski AL. Animal models to study MicroRNA function. Adv Cancer Res 2017; 135: 53-118
    CrossrefPubMedSearch in Google Scholar
  • 110 Lang MR, Gihr G, Gawaz MP, Müller II. Hemostasis in Danio rerio: is the zebrafish a useful model for platelet research?. J Thromb Haemost 2010; 8 (06) 1159-1169
    CrossrefPubMedSearch in Google Scholar
  • 111 Gregory M, Hanumanthaiah R, Jagadeeswaran P. Genetic analysis of hemostasis and thrombosis using vascular occlusion. Blood Cells Mol Dis 2002; 29 (03) 286-295
    CrossrefPubMedSearch in Google Scholar
  • 112 Lin HF, Traver D, Zhu H. et al. Analysis of thrombocyte development in CD41-GFP transgenic zebrafish. Blood 2005; 106 (12) 3803-3810
    CrossrefPubMedSearch in Google Scholar
  • 113 Roberto VP, Tiago DM, Gautvik K, Cancela ML. Evidence for the conservation of miR-223 in zebrafish (Danio rerio): Implications for function. Gene 2015; 566 (01) 54-62
    CrossrefPubMedSearch in Google Scholar
  • 114 Zapilko V, Fish RJ, Garcia A. et al. MicroRNA-126 is a regulator of platelet-supported thrombin generation. Platelets 2020; 31 (06) 746-755
    CrossrefPubMedSearch in Google Scholar
  • 115 Dong M, Fu YF, Du TT. et al. Heritable and lineage-specific gene knockdown in zebrafish embryo. PLoS One 2009; 4 (07) e6125
    CrossrefPubMedSearch in Google Scholar
  • 116 Thermes V, Grabher C, Ristoratore F. et al. I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev 2002; 118 (1–2): 91-98
    CrossrefPubMedSearch in Google Scholar
  • 117 Abe G, Suster ML, Kawakami K. Tol2-mediated transgenesis, gene trapping, enhancer trapping, and the Gal4-UAS system. Methods Cell Biol 2011; 104: 23-49
    CrossrefPubMedSearch in Google Scholar
  • 118 Suster ML, Abe G, Schouw A, Kawakami K. Transposon-mediated BAC transgenesis in zebrafish. Nat Protoc 2011; 6 (12) 1998-2021
    CrossrefPubMedSearch in Google Scholar
  • 119 Haffter P, Granato M, Brand M. et al. The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 1996; 123: 1-36
    CrossrefPubMedSearch in Google Scholar
  • 120 Housden BE, Muhar M, Gemberling M. et al. Loss-of-function genetic tools for animal models: cross-species and cross-platform differences. Nat Rev Genet 2017; 18 (01) 24-40
    CrossrefPubMedSearch in Google Scholar
  • 121 Bassett AR, Azzam G, Wheatley L. et al. Understanding functional miRNA-target interactions in vivo by site-specific genome engineering. Nat Commun 2014; 5: 4640
    CrossrefPubMedSearch in Google Scholar
  • 122 Hwang WY, Fu Y, Reyon D. et al. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 2013; 31 (03) 227-229
    CrossrefPubMedSearch in Google Scholar
  • 123 Wienholds E, van Eeden F, Kosters M, Mudde J, Plasterk RH, Cuppen E. Efficient target-selected mutagenesis in zebrafish. Genome Res 2003; 13 (12) 2700-2707
    CrossrefPubMedSearch in Google Scholar
  • 124 Fish RJ, Di Sanza C, Neerman-Arbez M. Targeted mutation of zebrafish fga models human congenital afibrinogenemia. Blood 2014; 123 (14) 2278-2281
    CrossrefPubMedSearch in Google Scholar
  • 125 Gut P, Reischauer S, Stainier DYR, Arnaout R. Little fish, big data: zebrafish as a model for cardiovascular and metabolic disease. Physiol Rev 2017; 97 (03) 889-938
    CrossrefPubMedSearch in Google Scholar
  • 126 Howe K, Clark MD, Torroja CF. et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496 (7446): 498-503
    Search in Google Scholar
  • 127 Yin VP, Lepilina A, Smith A, Poss KD. Regulation of zebrafish heart regeneration by miR-133. Dev Biol 2012; 365 (02) 319-327
    CrossrefPubMedSearch in Google Scholar
  • 128 Giacomotto J, Rinkwitz S, Becker TS. Effective heritable gene knockdown in zebrafish using synthetic microRNAs. Nat Commun 2015; 6: 7378
    CrossrefPubMedSearch in Google Scholar
  • 129 Stainier DYR, Raz E, Lawson ND. et al. Guidelines for morpholino use in zebrafish. PLoS Genet 2017; 13 (10) e1007000
    CrossrefPubMedSearch in Google Scholar
  • 130 Zou J, Li WQ, Li Q. et al. Two functional microRNA-126s repress a novel target gene p21-activated kinase 1 to regulate vascular integrity in zebrafish. Circ Res 2011; 108 (02) 201-209
    CrossrefPubMedSearch in Google Scholar
  • 131 Shestopalov IA, Chen JK. Oligonucleotide-based tools for studying zebrafish development. Zebrafish 2010; 7 (01) 31-40
    CrossrefPubMedSearch in Google Scholar
  • 132 Ebert MS, Sharp PA. MicroRNA sponges: progress and possibilities. RNA 2010; 16 (11) 2043-2050
    CrossrefPubMedSearch in Google Scholar
  • 133 Bak RO, Hollensen AK, Mikkelsen JG. Managing microRNAs with vector-encoded decoy-type inhibitors. Mol Ther 2013; 21 (08) 1478-1485
    CrossrefPubMedSearch in Google Scholar
  • 134 Lee KT, Nam JW. Post-transcriptional and translational regulation of mRNA-like long non-coding RNAs by microRNAs in early developmental stages of zebrafish embryos. BMB Rep 2017; 50 (04) 226-231
    CrossrefPubMedSearch in Google Scholar
  • 135 Bernardo BC, Gregorevic P, Ritchie RH, McMullen JR. Generation of MicroRNA-34 sponges and tough decoys for the heart: developments and challenges. Front Pharmacol 2018; 9: 1090
    CrossrefPubMedSearch in Google Scholar
  • 136 Gays D, Santoro MM. The admiR-able advances in cardiovascular biology through the zebrafish model system. Cell Mol Life Sci 2013; 70 (14) 2489-2503
    CrossrefPubMedSearch in Google Scholar
  • 137 Mohammed BM, Monroe DM, Gailani D. Mouse models of hemostasis. Platelets 2020; 31 (04) 417-422
    CrossrefPubMedSearch in Google Scholar
  • 138 Rivera J, Lozano ML, Navarro-Núñez L, Vicente V. Platelet receptors and signaling in the dynamics of thrombus formation. Haematologica 2009; 94 (05) 700-711
    CrossrefPubMedSearch in Google Scholar
  • 139 Roux J, Gonzàlez-Porta M, Robinson-Rechavi M. Comparative analysis of human and mouse expression data illuminates tissue-specific evolutionary patterns of miRNAs. Nucleic Acids Res 2012; 40 (13) 5890-5900
    CrossrefPubMedSearch in Google Scholar
  • 140 Park CY, Choi YS, McManus MT. Analysis of microRNA knockouts in mice. Hum Mol Genet 2010; 19 (R2): R169-R175
    CrossrefPubMedSearch in Google Scholar
  • 141 Prosser HM, Koike-Yusa H, Cooper JD, Law FC, Bradley A. A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat Biotechnol 2011; 29 (09) 840-845
    CrossrefPubMedSearch in Google Scholar
  • 142 Leierseder S, Petzold T, Zhang L, Loyer X, Massberg S, Engelhardt S. MiR-223 is dispensable for platelet production and function in mice. Thromb Haemost 2013; 110 (06) 1207-1214
    Thieme ConnectPubMedSearch in Google Scholar
  • 143 Kleinhammer A, Deussing J, Wurst W, Kühn R. Conditional RNAi in mice. Methods 2011; 53 (02) 142-150
    CrossrefPubMedSearch in Google Scholar
  • 144 Park CY, Jeker LT, Carver-Moore K. et al. A resource for the conditional ablation of microRNAs in the mouse. Cell Rep 2012; 1 (04) 385-391
    CrossrefPubMedSearch in Google Scholar
  • 145 Tiedt R, Schomber T, Hao-Shen H, Skoda RC. Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood 2007; 109 (04) 1503-1506
    CrossrefPubMedSearch in Google Scholar
  • 146 Rowley JW, Chappaz S, Corduan A. et al. Dicer1-mediated miRNA processing shapes the mRNA profile and function of murine platelets. Blood 2016; 127 (14) 1743-1751
    CrossrefPubMedSearch in Google Scholar
  • 147 Boilard E, Belleannée C. (Dicer)phering roles of microRNA in platelets. Blood 2016; 127 (14) 1733-1734
    CrossrefPubMedSearch in Google Scholar
  • 148 Nagy Z, Vögtle T, Geer MJ. et al. The Gp1ba-Cre transgenic mouse: a new model to delineate platelet and leukocyte functions. Blood 2019; 133 (04) 331-343
    CrossrefPubMedSearch in Google Scholar
  • 149 Takada S, Sato T, Ito Y. et al. Targeted gene deletion of miRNAs in mice by TALEN system. PLoS One 2013; 8 (10) e76004
    CrossrefPubMedSearch in Google Scholar
  • 150 Chang H, Yi B, Ma R, Zhang X, Zhao H, Xi Y. CRISPR/cas9, a novel genomic tool to knock down microRNA in vitro and in vivo. Sci Rep 2016; 6: 22312
    CrossrefPubMedSearch in Google Scholar
  • 151 Yasue A, Mitsui SN, Watanabe T. et al. Highly efficient targeted mutagenesis in one-cell mouse embryos mediated by the TALEN and CRISPR/Cas systems. Sci Rep 2014; 4: 5705
    CrossrefPubMedSearch in Google Scholar
  • 152 Zeng LL, He XS, Liu JR, Zheng CB, Wang YT, Yang GY. Lentivirus-mediated overexpression of MicroRNA-210 improves long-term outcomes after focal cerebral ischemia in mice. CNS Neurosci Ther 2016; 22 (12) 961-969
    CrossrefPubMedSearch in Google Scholar
  • 153 Tsumaru S, Masumoto H, Minakata K. et al. Therapeutic angiogenesis by local sustained release of microRNA-126 using poly lactic-co-glycolic acid nanoparticles in murine hindlimb ischemia. J Vasc Surg 2018; 68 (04) 1209-1215
    CrossrefPubMedSearch in Google Scholar
  • 154 Witkowski M, Weithauser A, Tabaraie T. et al. Micro-RNA-126 reduces the blood thrombogenicity in diabetes mellitus via targeting of tissue factor. Arterioscler Thromb Vasc Biol 2016; 36 (06) 1263-1271
    CrossrefPubMedSearch in Google Scholar
  • 155 Peng L, Liu J, Qin L. et al. Interaction between platelet-derived microRNAs and CYP2C19*2 genotype on clopidogrel antiplatelet responsiveness in patients with ACS. Thromb Res 2017; 157: 97-102
    CrossrefPubMedSearch in Google Scholar
  • 156 Ding T, Zeng X, Cheng B. et al. Platelets in acute coronary syndrome patients with high platelet reactivity after dual antiplatelet therapy exhibit upregulation of miR-204-5p. Ann Clin Lab Sci 2019; 49 (05) 619-631
    PubMedSearch in Google Scholar
  • 157 Tang QJ, Lei HP, Wu H. et al. Plasma miR-142 predicts major adverse cardiovascular events as an intermediate biomarker of dual antiplatelet therapy. Acta Pharmacol Sin 2019; 40 (02) 208-215
    CrossrefPubMedSearch in Google Scholar
  • 158 Liu J, Qin L, Wang Z. et al. Platelet-derived miRNAs as determinants of the antiplatelet response in clopidogrel-treated patients with ACS. Thromb Res 2020; 186: 71-74
    CrossrefPubMedSearch in Google Scholar