Identifying circulating microRNAs as biomarkers of cardiovascular disease: a systematic review

Rokas Navickas, Diane Gal, Aleksandras Laucevičius, Agnė Taparauskaitė, Monika Zdanytė, Paul Holvoet, Rokas Navickas, Diane Gal, Aleksandras Laucevičius, Agnė Taparauskaitė, Monika Zdanytė, Paul Holvoet

Abstract

The aim of the present study is to identify microRNAs (miRs) with high potential to be used as biomarkers in plasma and/or serum to clinically diagnose, or provide accurate prognosis for survival in, patients with atherosclerosis, coronary artery disease, and acute coronary syndrome (ACS). A systematic search of published original research yielded a total of 72 studies. After review of the risk of bias of the published studies, according to Cochrane Collaboration and the QUADUAS Group standards, 19 studies were selected. Overall 52 different miRs were reported. In particular, miR-133a/b (5 studies), miR-208a/b (6 studies), and miR-499 (7 studies) were well studied and found to be significant diagnostic and/or prognostic markers across different cardiovascular disease progression stages. miR-1 and miR-145b are potential biomarkers of ACS; miR-1 with higher sensitivity for all acute myocardial infarction (AMI), and miR-145 for STEMI and worse outcome of AMI. But when miRs were studied across different ACS study populations, patients had varying degrees of coronary stenosis, which was identified as an important confounder that limited the ability to quantitatively pool the study results. The identified miRs were found to regulate endothelial function and angiogenesis (miR-1, miR-133), vascular smooth muscle cell differentiation (miR-133, miR-145), communication between vascular smooth muscle and endothelial cell to stabilize plaques (miR-145), apoptosis (miR-1, miR-133, miR-499), cardiac myocyte differentiation (miR-1, miR-133, miR-145, miR-208, miR-499), and to repress cardiac hypertrophy (miR-133). Their role in these processes may be explained by regulation of shared RNA targets such as cyclin-dependent kinase inhibitor 1A (or p21), ETS proto-oncogene 1, fascin actin-bundling protein 1, hyperpolarization-activated cyclic nucleotide-gated potassium channel 4, insulin-like growth factor 1 receptor LIM and SH3 protein 1, purine nucleoside phosphorylase, and transgelin 2. These mechanistic data further support the clinical relevance of the identified miRs. miR-1, miR-133a/b, miR-145, miR-208a/b, and miR-499(a) in plasma and/or serum show some potential for diagnosis of cardiovascular disease. However, biased selection of miRs in most studies and unexplained contrasting results are major limitations of current miR research. Inconsistencies need to be addressed in order to definitively identify clinically useful miRs. Therefore, this paper presents important aspects to improve future miR research, including unbiased selection of miRs, standardization/normalization of reference miRs, adjustment for patient comorbidities and medication, and robust protocols of data-sharing plans that could prevent selective publication and selective reporting of miR research outcomes.

Keywords: (Disease) Progression; Acute coronary syndrome; Biomarkers; Circulating microRNA; Coronary artery disease.

© The Author 2016. Published by Oxford University Press on behalf of the European Society of Cardiology.

Figures

Figure 1
Figure 1
Flow diagram from study identification to inclusion.
Figure 2
Figure 2
Function of miRs. We identified miR-1, miR-133, miR-145, miR-208, and miR-499 as significant diagnostic and/or prognostic markers across different cardiovascular disease progression stages. They regulate endothelial function and angiogenesis (miR-1, miR-133), VSMC differentiation (miR-133, miR-145), communication between vascular smooth muscle and endothelial cell to stabilize plaques (miR-145), and regulate apoptosis in endothelial and VSMCs (miR-1, miR-133, miR-499), cardiac myocyte differentiation (miR-1, miR-133, miR-145, miR-208, miR-499), and repress cardiac hypertrophy (miR-133).

References

    1. Ling H, Fabbri M, Calin GA. MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat Rev Drug Discov 2013;12:847–865.
    1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281–297.
    1. Lytle JR, Yario TA, Steitz JA. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5’ UTR as in the 3’ UTR. Proc Natl Acad Sci U S A 2007;104:9667–9672.
    1. Ørom UA, Nielsen FC, Lund AH. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 2008;30:460–471.
    1. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008;455:1124–1128.
    1. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science 2007;318:1931–1934.
    1. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, Li Q, Li X, Wang W, Zhang Y, Wang J, Jiang X, Xiang Y, Xu C, Zheng P, Zhang J, Li R, Zhang H, Shang X, Gong T, Ning G, Wang J, Zen K, Zhang J, Zhang C-Y. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 2008;18:997–1006.
    1. Lawrie CH, Gal S, Dunlop HM, Pushkaran B, Liggins AP, Pulford K, Banham AH, Pezzella F, Boultwood J, Wainscoat JS, Hatton CSR, Harris AL. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br J Haematol England 2008;141:672–675.
    1. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A 2008;105:10513–10518.
    1. Small EM, Olson EN. Pervasive roles of microRNAs in cardiovascular biology. Nature 2011;469:336–342.
    1. Ren J, Zhang J, Xu N, Han G, Geng Q, Song J, Li S, Zhao J, Chen H. Signature of circulating microRNAs as potential biomarkers in vulnerable coronary artery disease. PloS One 2013;8:e80738.
    1. Seneviratne A, Hulsmans M, Holvoet P, Monaco C. Biomechanical factors and macrophages in plaque stability. Cardiovasc Res 2013;99:284–293.
    1. Huber HJ, Holvoet P. Exosomes: emerging roles in communication between blood cells and vascular tissues during atherosclerosis. Curr Opin Lipidol 2015;26:412–419.
    1. Hulsmans M, Holvoet P. MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease. Cardiovasc Res 2013;100:7–18.
    1. The Cochrane Collaboration. Cochrane systematic reviews of diagnostic accuracy. (26 November 2015).
    1. Whiting PF. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 2011;155:529.
    1. Macaskill P, Gatsonis C, Deeks J, Harbord R, Takwoingi Y. Chapter 10: Analysing and presenting results. In: Deeks J, Bossuyt P, Gatsonis C (eds). Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy Version 1.0. The Cochrane Collaboration; 2010. .
    1. Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097.
    1. Whiting PF, Rutjes AWS, Westwood ME, Mallett S. A systematic review classifies sources of bias and variation in diagnostic test accuracy studies. J Clin Epidemiol 2013;66:1093–1104.
    1. Bossuyt P, Leeflang M. Chapter 6: Developing criteria for including studies. In: Deeks J, Bossuyt P, Gatsonis C (eds). Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy Version 0.4. The Cochrane Collaboration; 2008. .
    1. Reitsma J, Rutes A, Whiting P, Vlassov V, Leeflang M, Deeks J. Chapter 9: Assessing methodological quality. In: Deeks J, Bossuyt P, Gatsonis C (eds). Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy Version 1.0.0. The Cochrane Collaboration; 2009. .
    1. Devaux Y, Mueller M, Haaf P, Goretti E, Twerenbold R, Zangrando J, Vausort M, Reichlin T, Wildi K, Moehring B, Wagner DR, Mueller C. Diagnostic and prognostic value of circulating microRNAs in patients with acute chest pain. J Intern Med 2015;277:260–271.
    1. Dong Y-M, Liu X-X, Wei G-Q, Da Y-N, Cha L, Ma C-S. Prediction of long-term outcome after acute myocardial infarction using circulating miR-145. Scand J Clin Lab Invest 2015;75:85–91.
    1. Gacoń J, Kabłak-Ziembicka A, Stępień E, Enguita FJ, Karch I, Derlaga B, Żmudka K, Przewłocki T. Decision making micro RNAs (miR-124, -133a/b, -34a and -134) in patients with occluded target vessel in acute coronary syndrome. Kardiol Pol 2016;74:280–288.
    1. Gao H, Guddeti RR, Matsuzawa Y, Liu L-P, Su L-X, Guo D, Nie S-P, Du J, Zhang M. Plasma levels of microRNA-145 are associated with severity of coronary artery disease. PloS One 2015;10:e0123477.
    1. Gao W, He H-W, Wang Z-M, Zhao H, Lian X-Q, Wang Y-S, Zhu J, Yan J-J, Zhang D-G, Yang Z-J, Wang L-S. Plasma levels of lipometabolism-related miR-122 and miR-370 are increased in patients with hyperlipidemia and associated with coronary artery disease. Lipids Health Dis 2012;11:55.
    1. Goretti E, Vausort M, Wagner DR, Devaux Y. Association between circulating microRNAs, cardiovascular risk factors and outcome in patients with acute myocardial infarction. Int J Cardiol 2013;168:4548–4550.
    1. He F, Lv P, Zhao X, Wang X, Ma X, Meng W, Meng X, Dong S. Predictive value of circulating miR-328 and miR-134 for acute myocardial infarction. Mol Cell Biochem 2014;394:137–144.
    1. Li X, Yang Y, Wang L, Qiao S, Lu X, Wu Y, Xu B, Li H, Gu D. Plasma miR-122 and miR-3149 potentially novel biomarkers for acute coronary syndrome. PloS One 2015;10:e0125430.
    1. Matsumoto S, Sakata Y, Nakatani D, Suna S, Mizuno H, Shimizu M, Usami M, Sasaki T, Sato H, Kawahara Y, Hamasaki T, Nanto S, Hori M, Komuro I. A subset of circulating microRNAs are predictive for cardiac death after discharge for acute myocardial infarction. Biochem Biophys Res Commun 2012;427:280–284.
    1. Oerlemans MIFJ, Mosterd A, Dekker MS, de Vrey EA, van Mil A, Pasterkamp G, Doevendans PA, Hoes AW, Sluijter JPG. Early assessment of acute coronary syndromes in the emergency department: the potential diagnostic value of circulating microRNAs. EMBO Mol Med 2012;4:1176–1185.
    1. Sun X, Zhang M, Sanagawa A, Mori C, Ito S, Iwaki S, Satoh H, Fujii S. Circulating microRNA-126 in patients with coronary artery disease: correlation with LDL cholesterol. Thromb J 2012;10:16.
    1. Wang F, Long G, Zhao C, Li H, Chaugai S, Wang Y, Chen C, Wang DW. Plasma microRNA-133a is a new marker for both acute myocardial infarction and underlying coronary artery stenosis. J Transl Med 2013;11:222.
    1. Wang G-K, Zhu J-Q, Zhang J-T, Li Q, Li Y, He J, Qin Y-W, Jing Q. Circulating microRNA: a novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J 2010;31:659–666.
    1. Widera C, Gupta SK, Lorenzen JM, Bang C, Bauersachs J, Bethmann K, Kempf T, Wollert KC, Thum T. Diagnostic and prognostic impact of six circulating microRNAs in acute coronary syndrome. J Mol Cell Cardiol 2011;51:872–875.
    1. Zampetaki A, Willeit P, Tilling L, Drozdov I, Prokopi M, Renard J-M, Mayr A, Weger S, Schett G, Shah A, Boulanger CM, Willeit J, Chowienczyk PJ, Kiechl S, Mayr M. Prospective study on circulating microRNAs and risk of myocardial infarction. J Am Coll Cardiol 2012;60:290–299.
    1. Zeller T, Keller T, Ojeda F, Reichlin T, Twerenbold R, Tzikas S, Wild PS, Reiter M, Czyz E, Lackner KJ, Munzel T, Mueller C, Blankenberg S. Assessment of microRNAs in patients with unstable angina pectoris. Eur Heart J 2014;35:2106–2114.
    1. Zhang L, Chen X, Su T, Li H, Huang Q, Wu D, Yang C, Han Z. Circulating miR-499 are novel and sensitive biomarker of acute myocardial infarction. J Thorac Dis 2015;7:303–308.
    1. Zhang R, Lan C, Pei H, Duan G, Huang L, Li L. Expression of circulating miR-486 and miR-150 in patients with acute myocardial infarction. BMC Cardiovasc Disord 2015;15:51.
    1. Zhu G-F, Yang L-X, Guo R-W, Liu H, Shi Y-K, Ye J-S, Yang Z-H. MicroRNA-155 is inversely associated with severity of coronary stenotic lesions calculated by the Gensini score. Coron Artery Dis 2014;25:304–310.
    1. Ji Q, Jiang Q, Yan W, Li X, Zhang Y, Meng P, Shao M, Chen L, Zhu H, Tian N. Expression of circulating microRNAs in patients with ST segment elevation acute myocardial infarction. Minerva Cardioangiol 2015;63:397–402.
    1. Liang J, Bai S, Su L, Li C, Wu J, Xia Z, Xu D. A subset of circulating microRNAs is expressed differently in patients with myocardial infarction. Mol Med Rep 2015;12:243–247.
    1. Nabiałek E, Wańha W, Kula D, Jadczyk T, Krajewska M, Kowalówka A, Dworowy S, Hrycek E, Włudarczyk W, Parma Z, Michalewska-Włudarczyk A, Pawłowski T, Ochała B, Jarząb B, Tendera M, Wojakowski W. Circulating microRNAs (miR-423-5p, miR-208a and miR-1) in acute myocardial infarction and stable coronary heart disease. Minerva Cardioangiol 2013;61:627–637.
    1. Ali Sheikh MS, Xia K, Li F, Deng X, Salma U, Deng H, Wei Wei L, Yang T-L, Peng J. Circulating miR-765 and miR-149: potential noninvasive diagnostic biomarkers for geriatric coronary artery disease patients. BioMed Res Int 2015;2015:740301.
    1. Chen X, Zhang L, Su T, Li H, Huang Q, Wu D, Yang C, Han Z. Kinetics of plasma microRNA-499 expression in acute myocardial infarction. J Thorac Dis 2015;7:890–896.
    1. Devaux Y, Vausort M, Goretti E, Nazarov PV, Azuaje F, Gilson G, Corsten MF, Schroen B, Lair M-L, Heymans S, Wagner DR. Use of circulating microRNAs to diagnose acute myocardial infarction. Clin Chem 2012;58:559–567.
    1. Eitel I, Adams V, Dieterich P, Fuernau G, de Waha S, Desch S, Schuler G, Thiele H. Relation of circulating microRNA-133a concentrations with myocardial damage and clinical prognosis in ST-elevation myocardial infarction. Am Heart J 2012;164:706–714.
    1. Fan X, Wang E, Wang X, Cong X, Chen X. MicroRNA-21 is a unique signature associated with coronary plaque instability in humans by regulating matrix metalloproteinase-9 via reversion-inducing cysteine-rich protein with Kazal motifs. Exp Mol Pathol 2014;96:242–249.
    1. Freedman JE, Ercan B, Morin KM, Liu C-T, Tamer L, Ayaz L, Kanadasi M, Cicek D, Seyhan AI, Akilli RE, Camci C, Cengiz B, Oztuzcu S, Tanriverdi K. The distribution of circulating microRNA and their relation to coronary disease. F1000Research 2012;1:50.
    1. Gidlöf O, Smith JG, Miyazu K, Gilje P, Spencer A, Blomquist S, Erlinge D. Circulating cardio-enriched microRNAs are associated with long-term prognosis following myocardial infarction. BMC Cardiovasc Disord 2013;13:12.
    1. Jansen F, Yang X, Proebsting S, Hoelscher M, Przybilla D, Baumann K, Schmitz T, Dolf A, Endl E, Franklin BS, Sinning J-M, Vasa-Nicotera M, Nickenig G, Werner N. MicroRNA expression in circulating microvesicles predicts cardiovascular events in patients with coronary artery disease. J Am Heart Assoc 2014;3:e001249.
    1. Jiang Y, Wang H, Li Y, Guo S, Zhang L, Cai J, Cao H, Wang C, Wang H, Liu L. Peripheral blood miRNAs as a biomarker for chronic cardiovascular diseases. Sci Rep 2014;4:5026.
    1. Jin Y, Yang C-J, Xu X, Cao J-N, Feng Q-T, Yang J. MiR-214 regulates the pathogenesis of patients with coronary artery disease by targeting VEGF. Mol Cell Biochem 2015;402:111–122.
    1. Kuwabara Y, Ono K, Horie T, Nishi H, Nagao K, Kinoshita M, Watanabe S, Baba O, Kojima Y, Shizuta S, Imai M, Tamura T, Kita T, Kimura T. Increased microRNA-1 and microRNA-133a levels in serum of patients with cardiovascular disease indicate myocardial damage. Circ Cardiovasc Genet 2011;4:446–454.
    1. Li C, Fang Z, Jiang T, Zhang Q, Liu C, Zhang C, Xiang Y. Serum microRNAs profile from genome-wide serves as a fingerprint for diagnosis of acute myocardial infarction and angina pectoris. BMC Med Genomics 2013;6:16.
    1. Li Y-Q, Zhang M-F, Wen H-Y, Hu C-L, Liu R, Wei H-Y, Ai C-M, Wang G, Liao X-X, Li X. Comparing the diagnostic values of circulating microRNAs and cardiac troponin T in patients with acute myocardial infarction. Clin São Paulo Braz 2013;68:75–80.
    1. Li S, Ren J, Xu N, Zhang J, Geng Q, Cao C, Lee C, Song J, Li J, Chen H. 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.
    1. Olivieri F, Antonicelli R, Lorenzi M, D'Alessandra Y, Lazzarini R, Santini G, Spazzafumo L, Lisa R, La Sala L, Galeazzi R, Recchioni R, Testa R, Pompilio G, Capogrossi MC, Procopio AD. Diagnostic potential of circulating miR-499-5p in elderly patients with acute non ST-elevation myocardial infarction. Int J Cardiol 2013;167:531–536.
    1. Olivieri F, Antonicelli R, Spazzafumo L, Santini G, Rippo MR, Galeazzi R, Giovagnetti S, D'Alessandra Y, Marcheselli F, Capogrossi MC, Procopio AD. Admission levels of circulating miR-499-5p and risk of death in elderly patients after acute non-ST elevation myocardial infarction. Int J Cardiol 2014;172:e276–e278.
    1. Peng L, Chun-guang Q, Bei-fang L, Xue-zhi D, Zi-hao W, Yun-fu L, Yan-ping D, Yang-gui L, Wei-guo L, Tian-yong H, Zhen-wen H. Clinical impact of circulating miR-133, miR-1291 and miR-663b in plasma of patients with acute myocardial infarction. Diagn Pathol 2014;9:89.
    1. Pilbrow AP, Cordeddu L, Cameron VA, Frampton CM, Troughton RW, Doughty RN, Whalley GA, Ellis CJ, Yandle TG, Richards AM, Foo RS-Y. Circulating miR-323-3p and miR-652: candidate markers for the presence and progression of acute coronary syndromes. Int J Cardiol 2014;176:375–385.
    1. Sun Q, Jia X, Gao J, Zhang P, Mou W, Yang C, Tong H, Wen X, Tian Y. Identification and characterization of novel serum microRNAs in unstable angina pectoris and subclinical atherosclerotic patients. Exp Cell Res 2015;333:220–227.
    1. Vogel B, Keller A, Frese KS, Kloos W, Kayvanpour E, Sedaghat-Hamedani F, Hassel S, Marquart S, Beier M, Giannitis E, Hardt S, Katus HA, Meder B. Refining diagnostic microRNA signatures by whole-miRNome kinetic analysis in acute myocardial infarction. Clin Chem 2013;59:410–418.
    1. Wang F, Long G, Zhao C, Li H, Chaugai S, Wang Y, Chen C, Wang DW. Atherosclerosis-related circulating miRNAs as novel and sensitive predictors for acute myocardial infarction. PloS One 2014;9:e105734.
    1. Ward JA, Esa N, Pidikiti R, Freedman JE, Keaney JF, Tanriverdi K, Vitseva O, Ambros V, Lee R, McManus DD. Circulating cell and plasma microRNA profiles differ between non-ST-segment and ST-segment-elevation myocardial infarction. Fam Med Med Sci Res 2013;2:108.
    1. Adachi T, Nakanishi M, Otsuka Y, Nishimura K, Hirokawa G, Goto Y, Nonogi H, Iwai N. Plasma microRNA 499 as a biomarker of acute myocardial infarction. Clin Chem 2010;56:1183–1185.
    1. Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, Li K, Yu B, Li Z, Wang R, Wang L, Li Q, Wang N, Shan H, Li Z, Yang B. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun 2010;391:73–77.
    1. Cheng Y, Tan N, Yang J, Liu X, Cao X, He P, Dong X, Qin S, Zhang C. A translational study of circulating cell-free microRNA-1 in acute myocardial infarction. Clin Sci 2010;119:87–95.
    1. Corsten MF, Dennert R, Jochems S, Kuznetsova T, Devaux Y, Hofstra L, Wagner DR, Staessen JA, Heymans S, Schroen B. Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet 2010;3:499–506.
    1. D'Alessandra Y, Devanna P, Limana F, Straino S, Di Carlo A, Brambilla PG, Rubino M, Carena MC, Spazzafumo L, De Simone M, Micheli B, Biglioli P, Achilli F, Martelli F, Maggiolini S, Marenzi G, Pompilio G, Capogrossi MC. Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur Heart J 2010;31:2765–2773.
    1. D'Alessandra Y, Carena MC, Spazzafumo L, Martinelli F, Bassetti B, Devanna P, Rubino M, Marenzi G, Colombo GI, Achilli F, Maggiolini S, Capogrossi MC, Pompilio G. Diagnostic potential of plasmatic MicroRNA signatures in stable and unstable angina. PloS One 2013;8:e80345.
    1. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, Weber M, Hamm CW, Röxe T, Müller-Ardogan M, Bonauer A, Zeiher AM, Dimmeler S. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010;107:677–684.
    1. Han H, Qu G, Han C, Wang Y, Sun T, Li F, Wang J, Luo S. MiR-34a, miR-21 and miR-23a as potential biomarkers for coronary artery disease: a pilot microarray study and confirmation in a 32 patient cohort. Exp Mol Med 2015;47:e138.
    1. Hsu A, Chen S-J, Chang Y-S, Chen H-C, Chu P-H. Systemic approach to identify serum microRNAs as potential biomarkers for acute myocardial infarction. BioMed Res Int 2014;2014:418628.
    1. Huang S, Chen M, Li L, He M, Hu D, Zhang X, Li J, Tanguay RM, Feng J, Cheng L, Zeng H, Dai X, Deng Q, Hu FB, Wu T. Circulating MicroRNAs and the occurrence of acute myocardial infarction in Chinese populations. Circ Cardiovasc Genet 2014;7:189–198.
    1. Li T, Cao H, Zhuang J, Wan J, Guan M, Yu B, Li X, Zhang W. Identification of miR-130a, miR-27b and miR-210 as serum biomarkers for atherosclerosis obliterans. Clin Chim Acta Int J Clin Chem 2011;412:66–70.
    1. Li L-M, Cai W-B, Ye Q, Liu J-M, Li X, Liao X-X. Comparison of plasma microRNA-1 and cardiac troponin T in early diagnosis of patients with acute myocardial infarction. World J Emerg Med 2014;5:182–186.
    1. Li Z, Lu J, Luo Y, Li S, Chen M. High association between human circulating microRNA-497 and acute myocardial infarction. Sci World J 2014;2014:931845.
    1. Li C, Chen X, Huang J, Sun Q, Wang L. Clinical impact of circulating miR-26a, miR-191, and miR-208b in plasma of patients with acute myocardial infarction. Eur J Med Res 2015;20:58.
    1. Liu F, Li R, Zhang Y, Qiu J, Ling W. Association of plasma MiR-17-92 with dyslipidemia in patients with coronary artery disease. Medicine (Baltimore) 2014;93:e98.
    1. Liu J, Liu Y, Sun Y-N, Li S, Liu X-Q, Li J, Li C-M, Tian W, Zhou Y-T, Shang X-M. MiR-28-5p involved in LXR-ABCA1 pathway is increased in the plasma of unstable angina patients. Heart Lung Circ 2015;24:724–730.
    1. Long G, Wang F, Duan Q, Chen F, Yang S, Gong W, Wang Y, Chen C, Wang DW. Human circulating microRNA-1 and microRNA-126 as potential novel indicators for acute myocardial infarction. Int J Biol Sci 2012;8:811–818.
    1. Long G, Wang F, Duan Q, Yang S, Chen F, Gong W, Yang X, Wang Y, Chen C, Wang DW. Circulating miR-30a, miR-195 and let-7b associated with acute myocardial infarction. PloS One 2012;7:e50926.
    1. Lu H-Q, Liang C, He Z-Q, Fan M, Wu Z-G. Circulating miR-214 is associated with the severity of coronary artery disease. J Geriatr Cardiol JGC 2013;10:34–38.
    1. Meder B, Keller A, Vogel B, Haas J, Sedaghat-Hamedani F, Kayvanpour E, Just S, Borries A, Rudloff J, Leidinger P, Meese E, Katus HA, Rottbauer W. MicroRNA signatures in total peripheral blood as novel biomarkers for acute myocardial infarction. Basic Res Cardiol 2011;106:13–23.
    1. Sayed ASM, Xia K, Li F, Deng X, Salma U, Li T, Deng H, Yang D, Haoyang Z, Yang T, Peng J. The diagnostic value of circulating microRNAs for middle-aged (40-60-year-old) coronary artery disease patients. Clin São Paulo Braz 2015;70:257–263.
    1. Stather PW, Sylvius N, Wild JB, Choke E, Sayers RD, Bown MJ. Differential microRNA expression profiles in peripheral arterial disease. Circ Cardiovasc Genet 2013;6:490–497.
    1. Wang R, Li N, Zhang Y, Ran Y, Pu J. Circulating microRNAs are promising novel biomarkers of acute myocardial infarction. Intern Med Tokyo Jpn 2011;50:1789–1795.
    1. Wang J, Pei Y, Zhong Y, Jiang S, Shao J, Gong J. Altered serum microRNAs as novel diagnostic biomarkers for atypical coronary artery disease. PloS One 2014;9:e107012.
    1. Weber M, Baker MB, Patel RS, Quyyumi AA, Bao G, Searles CD. MicroRNA expression profile in CAD patients and the impact of ACEI/ARB. Cardiol Res Pract 2011;2011:1–5.
    1. Zhao CH, Cheng G-C, He RL, Hong Y, Wan QL, Wang Z-Z, Pan Z-Y. Analysis and clinical significance of microRNA-499 expression levels in serum of patients with acute myocardial infarction. Genet Mol Res GMR 2015;14:4027–4034.
    1. Zhong J, He Y, Chen W, Shui X, Chen C, Lei W. Circulating microRNA-19a as a potential novel biomarker for diagnosis of acute myocardial infarction. Int J Mol Sci 2014;15:20355–20364.
    1. Welten SMJ, Goossens EAC, Quax PHA, Nossent AY. The multifactorial nature of microRNAs in vascular remodelling. Cardiovasc Res 2016;110:6–22.
    1. Rotllan N, Price N, Pati P, Goedeke L, Fernández-Hernando C. microRNAs in lipoprotein metabolism and cardiometabolic disorders. Atherosclerosis 2016;246:352–360.
    1. Dai Y, Condorelli G, Mehta JL. Scavenger receptors and non-coding RNAs: relevance in atherogenesis. Cardiovasc Res 2016;109:24–33.
    1. Economou EK, Oikonomou E, Siasos G, Papageorgiou N, Tsalamandris S, Mourouzis K, Papaioanou S, Tousoulis D. The role of microRNAs in coronary artery disease: from pathophysiology to diagnosis and treatment. Atherosclerosis 2015;241:624–633.
    1. Schober A, Nazari-Jahantigh M, Weber C. MicroRNA-mediated mechanisms of the cellular stress response in atherosclerosis. Nat Rev Cardiol 2015;12:361–374.
    1. Romaine SPR, Tomaszewski M, Condorelli G, Samani NJ. MicroRNAs in cardiovascular disease: an introduction for clinicians. Heart 2015;101:921–928.
    1. Hulsmans M, De Keyzer D, Holvoet P. MicroRNAs regulating oxidative stress and inflammation in relation to obesity and atherosclerosis. FASEB J Off Publ Fed Am Soc Exp Biol 2011;25:2515–2527.
    1. Wang H, Zhu H-Q, Wang F, Zhou Q, Gui S-Y, Wang Y. MicroRNA-1 prevents high-fat diet-induced endothelial permeability in apoE knock-out mice. Mol Cell Biochem 2013;378:153–159.
    1. Lin C-Y, Lee H-C, Fu C-Y, Ding Y-Y, Chen J-S, Lee M-H, Huang W-J, Tsai H-J. MiR-1 and miR-206 target different genes to have opposing roles during angiogenesis in zebrafish embryos. Nat Commun 2013;4:2829.
    1. Stahlhut C, Suarez Y, Lu J, Mishima Y, Giraldez AJ. MiR-1 and miR-206 regulate angiogenesis by modulating VegfA expression in zebrafish. Development 2012;139:4356–4365.
    1. Glass C, Singla DK. MicroRNA-1 transfected embryonic stem cells enhance cardiac myocyte differentiation and inhibit apoptosis by modulating the PTEN/Akt pathway in the infarcted heart. AJP Heart Circ Physiol 2011;301:H2038–H2049.
    1. Kumarswamy R, Lyon AR, Volkmann I, Mills AM, Bretthauer J, Pahuja A, Geers-Knorr C, Kraft T, Hajjar RJ, Macleod KT, Harding SE, Thum T. SERCA2a gene therapy restores microRNA-1 expression in heart failure via an Akt/FoxO3A-dependent pathway. Eur Heart J 2012;33:1067–1075.
    1. Soufi-Zomorrod M, Hajifathali A, Kouhkan F, Mehdizadeh M, Rad SMAH, Soleimani M. MicroRNAs modulating angiogenesis: miR-129-1 and miR-133 act as angio-miR in HUVECs. Tumour Biol J Int Soc Oncodevelopmental Biol Med 2016; .
    1. Torella D, Iaconetti C, Catalucci D, Ellison GM, Leone A, Waring CD, Bochicchio A, Vicinanza C, Aquila I, Curcio A, Condorelli G, Indolfi C. MicroRNA-133 controls vascular smooth muscle cell phenotypic switch in vitro and vascular remodeling in vivo. Circ Res 2011;109:880–893.
    1. Carè A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, Bang M-L, Segnalini P, Gu Y, Dalton ND, Elia L, Latronico MVG, Høydal M, Autore C, Russo MA, Dorn GW, Ellingsen O, Ruiz-Lozano P, Peterson KL, Croce CM, Peschle C, Condorelli G. MicroRNA-133 controls cardiac hypertrophy. Nat Med 2007;13:613–618.
    1. Wang Y-S, Li S-H, Guo J, Mihic A, Wu J, Sun L, Davis K, Weisel RD, Li R-K. Role of miR-145 in cardiac myofibroblast differentiation. J Mol Cell Cardiol 2014;66:94–105.
    1. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee T-H, Miano JM, Ivey KN, Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009;460:705–710.
    1. Climent M, Quintavalle M, Miragoli M, Chen J, Condorelli G, Elia L. TGF-beta triggers miR-143/145 transfer from smooth muscle cells to endothelial cells, thereby modulating vessel stabilization. Circ Res 2015;116:1753–1764.
    1. Cheng Y, Liu X, Yang J, Lin Y, Xu D-Z, Lu Q, Deitch EA, Huo Y, Delphin ES, Zhang C. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ Res 2009;105:158–166.
    1. Shyu K-G, Cheng W-P, Wang B-W. Angiotensin II downregulates microRNA-145 to regulate Kruppel-like factor 4 and myocardin expression in human coronary arterial smooth muscle cells under high glucose conditions. Mol Med Camb Mass 2015;21:616–625.
    1. Leistner DM, Boeckel J-N, Reis SM, Thome CE, De Rosa R, Keller T, Palapies L, Fichtlscherer S, Dimmeler S, Zeiher AM. Transcoronary gradients of vascular miRNAs and coronary atherosclerotic plaque characteristics. Eur Heart J 2016;37:1738–1749.
    1. Sala F, Aranda JF, Rotllan N, Ramírez CM, Aryal B, Elia L, Condorelli G, Catapano AL, Fernández-Hernando C, Norata GD. MiR-143/145 deficiency attenuates the progression of atherosclerosis in Ldlr-/-mice. Thromb Haemost 2014;112:796–802.
    1. Caruso P, Dempsie Y, Stevens HC, McDonald RA, Long L, Lu R, White K, Mair KM, McClure JD, Southwood M, Upton P, Xin M, van Rooij E, Olson EN, Morrell NW, MacLean MR, Baker AH. A role for miR-145 in pulmonary arterial hypertension: evidence from mouse models and patient samples. Circ Res 2012;111:290–300.
    1. Paulin R, Sutendra G, Gurtu V, Dromparis P, Haromy A, Provencher S, Bonnet S, Michelakis ED. A miR-208-Mef2 axis drives the decompensation of right ventricular function in pulmonary hypertension. Circ Res 2015;116:56–69.
    1. Callis TE, Pandya K, Seok HY, Tang R-H, Tatsuguchi M, Huang Z-P, Chen J-F, Deng Z, Gunn B, Shumate J, Willis MS, Selzman CH, Wang D-Z. MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Invest 2009;119:2772–2786.
    1. Xin M, Olson EN, Bassel-Duby R. Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat Rev Mol Cell Biol 2013;14:529–541.
    1. Wang J, Jia Z, Zhang C, Sun M, Wang W, Chen P, Ma K, Zhang Y, Li X, Zhou C. miR-499 protects cardiomyocytes from H2O2-induced apoptosis via its effects on Pdcd4 and Pacs2. RNA Biol 2014;11:339–350.
    1. Bonello MR, Bobryshev YV, Khachigian LM. Peroxide-inducible Ets-1 mediates platelet-derived growth factor receptor-α gene transcription in vascular smooth muscle cells. Am J Pathol 2005;167:1149–1159.
    1. Baruscotti M, Bucchi A, Milanesi R, Paina M, Barbuti A, Gnecchi-Ruscone T, Bianco E, Vitali-Serdoz L, Cappato R, DiFrancesco D. A gain-of-function mutation in the cardiac pacemaker HCN4 channel increasing cAMP sensitivity is associated with familial inappropriate sinus tachycardia. Eur Heart J 2015; .
    1. Yamamoto M, Dobrzynski H, Tellez J, Niwa R, Billeter R, Honjo H, Kodama I, Boyett M. Extended atrial conduction system characterised by the expression of the HCN4 channel and connexin45. Cardiovasc Res 2006;72:271–281.
    1. Hofmann F, Fabritz L, Stieber J, Schmitt J, Kirchhof P, Ludwig A, Herrmann S. Ventricular HCN channels decrease the repolarization reserve in the hypertrophic heart. Cardiovasc Res 2012;95:317–326.
    1. Raman D, Sai J, Neel NF, Chew CS, Richmond A. LIM and SH3 Protein -1 Modulates CXCR2-Mediated Cell Migration. Unutmaz D, ed PLoS One 2010;5:e10050.
    1. Ho M-C, Shi W, Rinaldo-Matthis A, Tyler PC, Evans GB, Clinch K, Almo SC, Schramm VL. Four generations of transition-state analogues for human purine nucleoside phosphorylase. Proc Natl Acad Sci 2010;107:4805–4812.
    1. Li A, Yang Q, Yang K. miR-133a mediates the hypoxia-induced apoptosis by inhibiting TAGLN2 expression in cardiac myocytes. Mol Cell Biochem 2015;400:173–181.
    1. Zhang Y, Lin Q. MicroRNA-145 inhibits migration and invasion by down-regulating FSCN1 in lung cancer. Int J Clin Exp Med 2015;8:8794–8802.
    1. Wang G, Zhu S, Gu Y, Chen Q, Liu X, Fu H. MicroRNA-145 and microRNA-133a inhibited proliferation, migration, and invasion, while promoted apoptosis in hepatocellular carcinoma cells via targeting FSCN1. Dig Dis Sci 2015;60:3044–3052.
    1. Xue M, Zhao L, Yang F, Li Z, Li G. MicroRNA-145 inhibits the malignant phenotypes of gastric carcinoma cells via downregulation of fascin 1 expression. Mol Med Rep 2016;13:1033–1039.
    1. Gao S, Wassler M, Zhang L, Li Y, Wang J, Zhang Y, Shelat H, Williams J, Geng Y-J. MicroRNA-133a regulates insulin-like growth factor-1 receptor expression and vascular smooth muscle cell proliferation in murine atherosclerosis. Atherosclerosis 2014;232:171–179.
    1. Li M, Chiu J-F, Gagne J, Fukagawa NK. Age-related differences in insulin-like growth factor-1 receptor signaling regulates Akt/FOXO3a and ERK/Fos pathways in vascular smooth muscle cells. J Cell Physiol 2008;217:377–387.
    1. Qa'aty N, Wang Y, Wang A, Mao S, Vincent M, Husain M, Hinek A. The antidiabetic hormone glucagon-like peptide-1 induces formation of new elastic fibers in human cardiac fibroblasts after cross-activation of IGF-IR. Endocrinology 2015;156:90–102.
    1. Warboys CM, de Luca A, Amini N, Luong L, Duckles H, Hsiao S, White A, Biswas S, Khamis R, Chong CK, Cheung W-M, Sherwin SJ, Bennett MR, Gil J, Mason JC, Haskard DO, Evans PC. Disturbed flow promotes endothelial senescence via a p53-dependent pathway. Arterioscler Thromb Vasc Biol 2014;34:985–995.
    1. Spinetti G, Cordella D, Fortunato O, Sangalli E, Losa S, Gotti A, Carnelli F, Rosa F, Riboldi S, Sessa F, Avolio E, Beltrami AP, Emanueli C, Madeddu P. Global remodeling of the vascular stem cell niche in bone marrow of diabetic patients: implication of the microRNA-155/FOXO3a signaling pathway. Circ Res 2013;112:510–522.
    1. Kaudewitz D, Zampetaki A, Mayr M. MicroRNA biomarkers for coronary artery disease? Curr Atheroscler Rep 2015;17:70.
    1. Rukov JL, Wilentzik R, Jaffe I, Vinther J, Shomron N. Pharmaco-miR: linking microRNAs and drug effects. Brief Bioinform 2014;15:648–659.
    1. Li J, Chen H, Ren J, Song J, Zhang F, Zhang J, Lee C, Li S, Geng Q, Cao C, Xu N. Effects of statin on circulating microRNAome and predicted function regulatory network in patients with unstable angina. BMC Med Genomics 2015;8:12.
    1. Willeit P, Zampetaki A, Dudek K, Kaudewitz D, King A, Kirkby NS, Crosby-Nwaobi R, Prokopi M, Drozdov I, Langley SR, Sivaprasad S, Markus HS, Mitchell JA, Warner TD, Kiechl S, Mayr M. Circulating microRNAs as novel biomarkers for platelet activation. Circ Res 2013;112:595–600.
    1. Kaudewitz D, Lee R, Willeit P, McGregor R, Markus HS, Kiechl S, Zampetaki A, Storey RF, Channon KM, Mayr M. Impact of intravenous heparin on quantification of circulating microRNAs in patients with coronary artery disease. Thromb Haemost 2013;110:609–615.
    1. Tuck MK, Chan DW, Chia D, Godwin AK, Grizzle WE, Krueger KE, Rom W, Sanda M, Sorbara L, Stass S, Wang W, Brenner DE. Standard operating procedures for serum and plasma collection: early detection research network consensus statement Standard Operating Procedure Integration Working Group. J Proteome Res 2009;8:113–117.
    1. Garcia ME, Blanco JL, Caballero J, Gargallo-Viola D. Anticoagulants interfere with PCR used to diagnose invasive aspergillosis. J Clin Microbiol 2002;40:1567–1568.
    1. Blondal T, Jensby Nielsen S, Baker A, Andreasen D, Mouritzen P, Wrang Teilum M, Dahlsveen IK. Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods 2013;59:S1–S6.
    1. Calza S, Valentini D, Pawitan Y. Normalization of oligonucleotide arrays based on the least-variant set of genes. BMC Bioinformatics 2008;9:140.
    1. Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, Speleman F, Vandesompele J. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol 2009;10:R64.
    1. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 2007;8:R19.
    1. D'haene B, Mestdagh P, Hellemans J, Vandesompele J. MiRNA expression profiling: from reference genes to global mean normalization. In: Fan J-B, ed. Next-Generation MicroRNA Expression Profiling Technology. Totowa, NJ: Humana Press; 2012. 261–272.
    1. Schlosser K, McIntyre LA, White RJ, Stewart DJ. Customized internal reference controls for improved assessment of circulating micrornas in disease. Jeyaseelan K, ed. PLoS One 2015;10:e0127443.
    1. Creemers EE, Tijsen AJ, Pinto YM. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res 2012;110:483–495.
    1. Xiang M, Zeng Y, Yang R, Xu H, Chen Z, Zhong J, Xie H, Xu Y, Zeng X. U6 is not a suitable endogenous control for the quantification of circulating microRNAs. Biochem Biophys Res Commun 2014;454:210–214.
    1. Roberts TC, Coenen-Stass AML, Wood MJA. Assessment of RT-qPCR normalization strategies for accurate quantification of extracellular microRNAs in murine serum. Mukhopadhyay P, ed. PLoS One 2014;9:e89237.
    1. Lekchnov EA, Zaporozhchenko IA, Morozkin ES, Bryzgunova OE, Vlassov VV, Laktionov PP. Protocol for miRNA isolation from biofluids. Anal Biochem 2016;499:78–84.
    1. Taichman DB, Backus J, Baethge C, Bauchner H, de Leeuw PW, Drazen JM, Fletcher J, Frizelle FA, Groves T, Haileamlak A, James A, Laine C, Peiperl L, Pinborg A, Sahni P, Wu S. Sharing clinical trial data: a proposal from the international committee of medical journal editors. JAMA 2016;315:467–468.
    1. Zhao Y, Samal E, Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 2005;436:214–220.
    1. Bostjancic E, Zidar N, Stajner D, Glavac D. MicroRNA miR-1 is up-regulated in remote myocardium in patients with myocardial infarction. Folia Biol (Praha) 2010;56:27–31.
    1. Chen J-F, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang D-Z. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006;38:228–233.
    1. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, Olson EN. Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 2007;316:575–579.
    1. Ye Y, Perez-Polo JR, Qian J, Birnbaum Y. The role of microRNA in modulating myocardial ischemia-reperfusion injury. Physiol Genomics 2011;43:534–542.
    1. Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X, Wang D, Krall TJ, Delphin ES, Zhang C. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem 2009;284:29514–29525.
    1. Tang Y, Zheng J, Sun Y, Wu Z, Liu Z, Huang G. MicroRNA-1 regulates cardiomyocyte apoptosis by targeting Bcl-2. Int Heart J 2009;50:377–387.
    1. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 2008;105:13027–13032.
    1. 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;13:423–433.
    1. Jansen F, Yang X, Hoelscher M, Cattelan A, Schmitz T, Proebsting S, Wenzel D, Vosen S, Franklin BS, Fleischmann BK, Nickenig G, Werner N. Endothelial microparticle-mediated transfer of microRNA-126 promotes vascular endothelial cell repair via SPRED1 and is abrogated in glucose-damaged endothelial microparticles. Circulation 2013;128:2026–2038.
    1. Canfrán-Duque A, Ramírez CM, Goedeke L, Lin C-S, Fernández-Hernando C. MicroRNAs and HDL life cycle. Cardiovasc Res 2014;103:414–422.
    1. Jiang H, Huang S, Li X, Li X, Zhang Y, Chen Z-Y. Tyrosine kinase receptor B protects against coronary artery disease and promotes adult vasculature integrity by regulating Ets1-mediated VE-cadherin expression significance. Arterioscler Thromb Vasc Biol 2015;35:580–588.

Source: PubMed

3
Subskrybuj