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Erschienen in: Cardiovascular Drugs and Therapy 4/2019

22.07.2019 | ORIGINAL ARTICLE

The Role of Non-coding RNAs in Ischemic Myocardial Reperfusion Injury

verfasst von: Vince Siebert, Joseph Allencherril, Yumei Ye, Xander H. T. Wehrens, Yochai Birnbaum

Erschienen in: Cardiovascular Drugs and Therapy | Ausgabe 4/2019

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Abstract

MicroRNAs (miRNA) are non-coding RNAs that regulate gene expression in up to 90% of the human genome through interactions with messenger RNA (mRNA). The expression of miRNAs varies and changes in diseased and healthy states, including all stages of myocardial ischemia-reperfusion and subsequent ischemia-reperfusion injury (IRI). These changes in expression make miRNAs an attractive potential therapeutic target. Herein, we review the differences in miRNA expression prior to ischemia (including remote ischemic conditioning and ischemic pre-conditioning), the changes during ischemia-reperfusion, and the changes in miRNA expression after IRI, with an emphasis on inflammatory and fibrotic pathways. Additionally, we review the effects of manipulating the levels of certain miRNAs on changes in infarct size, inflammation, remodeling, angiogenesis, and cardiac function after either ischemia-reperfusion or permanent coronary ligation. Levels of target miRNA can be increased using molecular mimics (“agomirs”), or can be decreased by using “antagomirs” which are antisense molecules that act to bind and thus inactivate the target miRNA sequence. Other non-coding RNAs, including long non-coding RNAs and circular RNAs, also regulate gene expression and have a role in the regulation of IRI pathways. We review the mechanisms and downstream effects of the miRNAs that have been studied as therapy in both permanent coronary ligation and ischemia-reperfusion models.
Literatur
1.
Zurück zum Zitat Altesha M-A, Ni T, Khan A, Liu K, Zheng X. Circular RNA in cardiovascular disease. J Cell Physiol. 2019;234:5588–600.CrossRefPubMed Altesha M-A, Ni T, Khan A, Liu K, Zheng X. Circular RNA in cardiovascular disease. J Cell Physiol. 2019;234:5588–600.CrossRefPubMed
2.
Zurück zum Zitat Bayoumi AS, Teoh J-P, Aonuma T, Yuan Z, Ruan X, Tang Y, et al. MicroRNA-532 protects the heart in acute myocardial infarction, and represses prss23, a positive regulator of endothelial-to-mesenchymal transition. Cardiovasc Res. 2017;113:1603–14.CrossRefPubMedPubMedCentral Bayoumi AS, Teoh J-P, Aonuma T, Yuan Z, Ruan X, Tang Y, et al. MicroRNA-532 protects the heart in acute myocardial infarction, and represses prss23, a positive regulator of endothelial-to-mesenchymal transition. Cardiovasc Res. 2017;113:1603–14.CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Bellera N, Barba I, Rodriguez-Sinovas A, Ferret E, Asín MA, Gonzalez-Alujas M, et al. Single intracoronary injection of encapsulated Antagomir-92a promotes angiogenesis and prevents adverse infarct remodeling. J Am Heart Assoc. 2014;3:e000946.CrossRefPubMedPubMedCentral Bellera N, Barba I, Rodriguez-Sinovas A, Ferret E, Asín MA, Gonzalez-Alujas M, et al. Single intracoronary injection of encapsulated Antagomir-92a promotes angiogenesis and prevents adverse infarct remodeling. J Am Heart Assoc. 2014;3:e000946.CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science (80- ). 2009;324:1710–3.CrossRef Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science (80- ). 2009;324:1710–3.CrossRef
5.
Zurück zum Zitat Boon RA, Jaé N, Holdt L, Dimmeler S. Long noncoding RNAs. J Am Coll Cardiol. 2016;67:1214–26.CrossRefPubMed Boon RA, Jaé N, Holdt L, Dimmeler S. Long noncoding RNAs. J Am Coll Cardiol. 2016;67:1214–26.CrossRefPubMed
6.
Zurück zum Zitat Briceno N, Schuster A, Lumley M, Perera D. Ischaemic cardiomyopathy: pathophysiology, assessment and the role of revascularisation. Heart. 2016;102:397–406.CrossRefPubMed Briceno N, Schuster A, Lumley M, Perera D. Ischaemic cardiomyopathy: pathophysiology, assessment and the role of revascularisation. Heart. 2016;102:397–406.CrossRefPubMed
7.
Zurück zum Zitat Bromage DI, Pickard JMJ, Rossello X, Ziff OJ, Burke N, Yellon DM, et al. Remote ischaemic conditioning reduces infarct size in animal in vivo models of ischaemia-reperfusion injury: a systematic review and meta-analysis. Cardiovasc Res. 2016;113:cvw219.CrossRef Bromage DI, Pickard JMJ, Rossello X, Ziff OJ, Burke N, Yellon DM, et al. Remote ischaemic conditioning reduces infarct size in animal in vivo models of ischaemia-reperfusion injury: a systematic review and meta-analysis. Cardiovasc Res. 2016;113:cvw219.CrossRef
8.
Zurück zum Zitat Campani V, De Rosa G, Misso G, Zarone MR, Grimaldi A. Lipid nanoparticles to deliver miRNA in cancer. Curr Pharm Biotechnol. 2016;17:741–9.CrossRefPubMed Campani V, De Rosa G, Misso G, Zarone MR, Grimaldi A. Lipid nanoparticles to deliver miRNA in cancer. Curr Pharm Biotechnol. 2016;17:741–9.CrossRefPubMed
9.
Zurück zum Zitat Chen Z, Qi Y, Gao C. Cardiac myocyte-protective effect of microRNA-22 during ischemia and reperfusion through disrupting the caveolin-3/eNOS signaling. Int J Clin Exp Pathol. 2015;8:4614–26.PubMedPubMedCentral Chen Z, Qi Y, Gao C. Cardiac myocyte-protective effect of microRNA-22 during ischemia and reperfusion through disrupting the caveolin-3/eNOS signaling. Int J Clin Exp Pathol. 2015;8:4614–26.PubMedPubMedCentral
10.
Zurück zum Zitat Chen C, Ponnusamy M, Liu C, Gao J, Wang K, Li P. MicroRNA as a therapeutic target in cardiac remodeling. Biomed Res Int. 2017;2017:1–25. Chen C, Ponnusamy M, Liu C, Gao J, Wang K, Li P. MicroRNA as a therapeutic target in cardiac remodeling. Biomed Res Int. 2017;2017:1–25.
11.
Zurück zum Zitat Cheng Y, Zhu P, Yang J, Liu X, Dong S, Wang X, et al. Ischaemic preconditioning-regulated miR-21 protects heart against ischaemia/reperfusion injury via anti-apoptosis through its target PDCD4. Cardiovasc Res. 2010;87:431–9.CrossRefPubMedPubMedCentral Cheng Y, Zhu P, Yang J, Liu X, Dong S, Wang X, et al. Ischaemic preconditioning-regulated miR-21 protects heart against ischaemia/reperfusion injury via anti-apoptosis through its target PDCD4. Cardiovasc Res. 2010;87:431–9.CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Cong B-H, Zhu X-Y, Ni X. The roles of microRNA-22 in myocardial infarction. Sheng Li Xue Bao. 2017;69:571–8.PubMed Cong B-H, Zhu X-Y, Ni X. The roles of microRNA-22 in myocardial infarction. Sheng Li Xue Bao. 2017;69:571–8.PubMed
14.
Zurück zum Zitat Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X, et al. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem. 2009;284:29514–25.CrossRefPubMedPubMedCentral Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X, et al. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem. 2009;284:29514–25.CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Dutka M, Bobiński R, Korbecki J. The relevance of microRNA in post-infarction left ventricular remodelling and heart failure. Heart Fail Rev. 2019;24:575–86.CrossRefPubMedPubMedCentral Dutka M, Bobiński R, Korbecki J. The relevance of microRNA in post-infarction left ventricular remodelling and heart failure. Heart Fail Rev. 2019;24:575–86.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Fan X, Weng X, Zhao Y, Chen W, Gan T, Xu D. Circular RNAs in cardiovascular disease: An overview. Biomed Res Int. 2017;2017:1–9. Fan X, Weng X, Zhao Y, Chen W, Gan T, Xu D. Circular RNAs in cardiovascular disease: An overview. Biomed Res Int. 2017;2017:1–9.
18.
Zurück zum Zitat Feng Y, Huang W, Wani M, Yu X, Ashraf M. Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22. PLoS One. 2014;9:e88685.CrossRefPubMedPubMedCentral Feng Y, Huang W, Wani M, Yu X, Ashraf M. Ischemic preconditioning potentiates the protective effect of stem cells through secretion of exosomes by targeting Mecp2 via miR-22. PLoS One. 2014;9:e88685.CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Fiedler J, Jazbutyte V, Kirchmaier BC, Gupta SK, Lorenzen J, Hartmann D, et al. MicroRNA-24 regulates vascularity after myocardial infarction. Circulation. 2011;124:720–30.CrossRefPubMed Fiedler J, Jazbutyte V, Kirchmaier BC, Gupta SK, Lorenzen J, Hartmann D, et al. MicroRNA-24 regulates vascularity after myocardial infarction. Circulation. 2011;124:720–30.CrossRefPubMed
21.
Zurück zum Zitat Garikipati VNS, Verma SK, Jolardarashi D, Cheng Z, Ibetti J, Cimini M, et al. Therapeutic inhibition of miR-375 attenuates post-myocardial infarction inflammatory response and left ventricular dysfunction via PDK-1-AKT signalling axis. Cardiovasc Res. 2017;113:938–49.CrossRefPubMed Garikipati VNS, Verma SK, Jolardarashi D, Cheng Z, Ibetti J, Cimini M, et al. Therapeutic inhibition of miR-375 attenuates post-myocardial infarction inflammatory response and left ventricular dysfunction via PDK-1-AKT signalling axis. Cardiovasc Res. 2017;113:938–49.CrossRefPubMed
22.
Zurück zum Zitat Ge Z-W, Zhu X-L, Wang B-C, Hu J-L, Sun J-J, Wang S, et al. MicroRNA-26b relieves inflammatory response and myocardial remodeling of mice with myocardial infarction by suppression of MAPK pathway through binding to PTGS2. Int J Cardiol. 2019;280:152–9.CrossRefPubMed Ge Z-W, Zhu X-L, Wang B-C, Hu J-L, Sun J-J, Wang S, et al. MicroRNA-26b relieves inflammatory response and myocardial remodeling of mice with myocardial infarction by suppression of MAPK pathway through binding to PTGS2. Int J Cardiol. 2019;280:152–9.CrossRefPubMed
23.
Zurück zum Zitat Geng H-H, Li R, Su Y-M, Xiao J, Pan M, Cai X-X, et al. The circular RNA Cdr1as promotes myocardial infarction by mediating the regulation of miR-7a on its target genes expression. PLoS One. 2016;11:e0151753.CrossRefPubMedPubMedCentral Geng H-H, Li R, Su Y-M, Xiao J, Pan M, Cai X-X, et al. The circular RNA Cdr1as promotes myocardial infarction by mediating the regulation of miR-7a on its target genes expression. PLoS One. 2016;11:e0151753.CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Gottlieb RA, Pourpirali S. Lost in translation: miRNAs and mRNAs in ischemic preconditioning and ischemia/reperfusion injury. J Mol Cell Cardiol. 2016;95:70–7.CrossRefPubMed Gottlieb RA, Pourpirali S. Lost in translation: miRNAs and mRNAs in ischemic preconditioning and ischemia/reperfusion injury. J Mol Cell Cardiol. 2016;95:70–7.CrossRefPubMed
25.
Zurück zum Zitat Guo Y, Luo F, Liu Q, Xu D. Regulatory non-coding RNAs in acute myocardial infarction. J Cell Mol Med. 2017;21:1013–23.CrossRefPubMed Guo Y, Luo F, Liu Q, Xu D. Regulatory non-coding RNAs in acute myocardial infarction. J Cell Mol Med. 2017;21:1013–23.CrossRefPubMed
27.
Zurück zum Zitat He B, Xiao J, Ren A, Zhang Y, Zhang H, Chen M, et al. Role of miR-1 and miR-133a in myocardial ischemic postconditioning. J Biomed Sci. 2011;18:1–10.CrossRef He B, Xiao J, Ren A, Zhang Y, Zhang H, Chen M, et al. Role of miR-1 and miR-133a in myocardial ischemic postconditioning. J Biomed Sci. 2011;18:1–10.CrossRef
28.
Zurück zum Zitat He Q, Wang F, Honda T, James J, Li J, Redington A. Loss of miR-144 signaling interrupts extracellular matrix remodeling after myocardial infarction leading to worsened cardiac function. Sci Rep. 2018;8:16886.CrossRefPubMedPubMedCentral He Q, Wang F, Honda T, James J, Li J, Redington A. Loss of miR-144 signaling interrupts extracellular matrix remodeling after myocardial infarction leading to worsened cardiac function. Sci Rep. 2018;8:16886.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Hinkel R, Penzkofer D, Zühlke S, Fischer A, Husada W, Xu Q-F, et al. Inhibition of MicroRNA-92a protects against ischemia/reperfusion injury in a large-animal model. Circulation. 2013;128:1066–75.CrossRefPubMed Hinkel R, Penzkofer D, Zühlke S, Fischer A, Husada W, Xu Q-F, et al. Inhibition of MicroRNA-92a protects against ischemia/reperfusion injury in a large-animal model. Circulation. 2013;128:1066–75.CrossRefPubMed
30.
Zurück zum Zitat Hu S, Huang M, Li Z, Jia F, Ghosh Z, Lijkwan MA, et al. MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation. 2010;122:S124–31.CrossRefPubMedPubMedCentral Hu S, Huang M, Li Z, Jia F, Ghosh Z, Lijkwan MA, et al. MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation. 2010;122:S124–31.CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Hu J, Huang C-X, Rao P-P, Zhou J-P, Wang X, Tang L, et al. Inhibition of microRNA-155 attenuates sympathetic neural remodeling following myocardial infarction via reducing M1 macrophage polarization and inflammatory responses in mice. Eur J Pharmacol. 2019;851:122–32.CrossRefPubMed Hu J, Huang C-X, Rao P-P, Zhou J-P, Wang X, Tang L, et al. Inhibition of microRNA-155 attenuates sympathetic neural remodeling following myocardial infarction via reducing M1 macrophage polarization and inflammatory responses in mice. Eur J Pharmacol. 2019;851:122–32.CrossRefPubMed
32.
Zurück zum Zitat Huang Y, Qi Y, Du J-Q, Zhang D. MicroRNA-34a regulates cardiac fibrosis after myocardial infarction by targeting Smad4. Expert Opin Ther Targets. 2014;12:1355–65. Huang Y, Qi Y, Du J-Q, Zhang D. MicroRNA-34a regulates cardiac fibrosis after myocardial infarction by targeting Smad4. Expert Opin Ther Targets. 2014;12:1355–65.
33.
Zurück zum Zitat Hullinger TG, Montgomery RL, Seto AG, Dickinson BA, Semus HM, Lynch JM, et al. Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res. 2012;110:71–81.CrossRefPubMed Hullinger TG, Montgomery RL, Seto AG, Dickinson BA, Semus HM, Lynch JM, et al. Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res. 2012;110:71–81.CrossRefPubMed
34.
Zurück zum Zitat Icli B, Wara AKM, Moslehi J, Sun X, Plovie E, Cahill M, et al. MicroRNA-26a regulates pathological and physiological angiogenesis by targeting BMP/SMAD1 signaling. Circ Res. 2013;113:1231–41.CrossRefPubMedPubMedCentral Icli B, Wara AKM, Moslehi J, Sun X, Plovie E, Cahill M, et al. MicroRNA-26a regulates pathological and physiological angiogenesis by targeting BMP/SMAD1 signaling. Circ Res. 2013;113:1231–41.CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Kamps JA, Krenning G. Micromanaging cardiac regeneration: targeted delivery of microRNAs for cardiac repair and regeneration. World J Cardiol. 2016;8:163.CrossRefPubMedPubMedCentral Kamps JA, Krenning G. Micromanaging cardiac regeneration: targeted delivery of microRNAs for cardiac repair and regeneration. World J Cardiol. 2016;8:163.CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Li J, Rohailla S, Gelber N, Rutka J, Sabah N, Gladstone RA, et al. MicroRNA-144 is a circulating effector of remote ischemic preconditioning. Basic Res Cardiol. 2014;109:423.CrossRefPubMed Li J, Rohailla S, Gelber N, Rutka J, Sabah N, Gladstone RA, et al. MicroRNA-144 is a circulating effector of remote ischemic preconditioning. Basic Res Cardiol. 2014;109:423.CrossRefPubMed
37.
Zurück zum Zitat Li K, Lin T, Chen L, Wang N. MicroRNA-93 elevation after myocardial infarction is cardiac protective. Med Hypotheses. 2017;106:23–5.CrossRefPubMed Li K, Lin T, Chen L, Wang N. MicroRNA-93 elevation after myocardial infarction is cardiac protective. Med Hypotheses. 2017;106:23–5.CrossRefPubMed
38.
Zurück zum Zitat Li X, Dai Y, Yan S, Shi Y, Han B, Li J, et al. Down-regulation of lncRNA KCNQ1OT1 protects against myocardial ischemia/reperfusion injury following acute myocardial infarction. Biochem Biophys Res Commun. 2017;491:1026–33.CrossRefPubMed Li X, Dai Y, Yan S, Shi Y, Han B, Li J, et al. Down-regulation of lncRNA KCNQ1OT1 protects against myocardial ischemia/reperfusion injury following acute myocardial infarction. Biochem Biophys Res Commun. 2017;491:1026–33.CrossRefPubMed
39.
Zurück zum Zitat Li J, Cai SX, He Q, Zhang H, Friedberg D, Wang F, et al. Intravenous miR-144 reduces left ventricular remodeling after myocardial infarction. Basic Res Cardiol. 2018;113:36.CrossRefPubMed Li J, Cai SX, He Q, Zhang H, Friedberg D, Wang F, et al. Intravenous miR-144 reduces left ventricular remodeling after myocardial infarction. Basic Res Cardiol. 2018;113:36.CrossRefPubMed
40.
Zurück zum Zitat Liu X, Dong Y, Chen S, Zhang G, Zhang M, Gong Y, et al. Circulating MicroRNA-146a and MicroRNA-21 predict left ventricular remodeling after ST-elevation myocardial infarction. Cardiology. 2015;132:233–41.CrossRefPubMed Liu X, Dong Y, Chen S, Zhang G, Zhang M, Gong Y, et al. Circulating MicroRNA-146a and MicroRNA-21 predict left ventricular remodeling after ST-elevation myocardial infarction. Cardiology. 2015;132:233–41.CrossRefPubMed
41.
Zurück zum Zitat Lorenzen JM, Batkai S, Thum T. Regulation of cardiac and renal ischemia–reperfusion injury by microRNAs. Free Radic Biol Med. 2013;64:78–84.CrossRefPubMed Lorenzen JM, Batkai S, Thum T. Regulation of cardiac and renal ischemia–reperfusion injury by microRNAs. Free Radic Biol Med. 2013;64:78–84.CrossRefPubMed
42.
Zurück zum Zitat Lu C, Wang X, Ha T, Hu Y, Liu L, Zhang X, et al. Attenuation of cardiac dysfunction and remodeling of myocardial infarction by microRNA-130a are mediated by suppression of PTEN and activation of PI3K dependent signaling. J Mol Cell Cardiol. 2015;89:87–97.CrossRefPubMedPubMedCentral Lu C, Wang X, Ha T, Hu Y, Liu L, Zhang X, et al. Attenuation of cardiac dysfunction and remodeling of myocardial infarction by microRNA-130a are mediated by suppression of PTEN and activation of PI3K dependent signaling. J Mol Cell Cardiol. 2015;89:87–97.CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Martinez EC, Lilyanna S, Wang P, Vardy LA, Jiang X, Armugam A, et al. MicroRNA-31 promotes adverse cardiac remodeling and dysfunction in ischemic heart disease. J Mol Cell Cardiol. 2017;112:27–39.CrossRefPubMed Martinez EC, Lilyanna S, Wang P, Vardy LA, Jiang X, Armugam A, et al. MicroRNA-31 promotes adverse cardiac remodeling and dysfunction in ischemic heart disease. J Mol Cell Cardiol. 2017;112:27–39.CrossRefPubMed
44.
Zurück zum Zitat Mathiyalagan P, Sahoo S. Exosomes-based gene therapy for MicroRNA delivery. In: Ishikawa K, editor. Cardiac gene therapy: methods and protocols. New York: Springer; 2017. p. 139–52.CrossRef Mathiyalagan P, Sahoo S. Exosomes-based gene therapy for MicroRNA delivery. In: Ishikawa K, editor. Cardiac gene therapy: methods and protocols. New York: Springer; 2017. p. 139–52.CrossRef
45.
Zurück zum Zitat Meloni M, Marchetti M, Garner K, Littlejohns B, Sala-Newby G, Xenophontos N, et al. Local inhibition of MicroRNA-24 improves reparative angiogenesis and left ventricle remodeling and function in mice with myocardial infarction. Mol Ther. 2013;21:1390–402.CrossRefPubMedPubMedCentral Meloni M, Marchetti M, Garner K, Littlejohns B, Sala-Newby G, Xenophontos N, et al. Local inhibition of MicroRNA-24 improves reparative angiogenesis and left ventricle remodeling and function in mice with myocardial infarction. Mol Ther. 2013;21:1390–402.CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat Menees DS, Peterson ED, Wang Y, Curtis JP, Messenger JC, Rumsfeld JS, et al. Door-to-balloon time and mortality among patients undergoing primary PCI. N Engl J Med. 2013;369:901–9.CrossRefPubMed Menees DS, Peterson ED, Wang Y, Curtis JP, Messenger JC, Rumsfeld JS, et al. Door-to-balloon time and mortality among patients undergoing primary PCI. N Engl J Med. 2013;369:901–9.CrossRefPubMed
47.
Zurück zum Zitat Ong S-B, Katwadi K, Kwek X-Y, Ismail NI, Chinda K, Ong S-G, et al. Non-coding RNAs as therapeutic targets for preventing myocardial ischemia-reperfusion injury. Expert Opin Ther Targets. 2018;22:247–61.CrossRefPubMed Ong S-B, Katwadi K, Kwek X-Y, Ismail NI, Chinda K, Ong S-G, et al. Non-coding RNAs as therapeutic targets for preventing myocardial ischemia-reperfusion injury. Expert Opin Ther Targets. 2018;22:247–61.CrossRefPubMed
48.
Zurück zum Zitat Pan Z, Sun X, Shan H, Wang N, Wang J, Ren J, et al. MicroRNA-101 inhibited postinfarct cardiac fibrosis and improved left ventricular compliance via the FBJ osteosarcoma oncogene/transforming growth factor-β1 pathway. Circulation. 2012;126:840–50.CrossRefPubMed Pan Z, Sun X, Shan H, Wang N, Wang J, Ren J, et al. MicroRNA-101 inhibited postinfarct cardiac fibrosis and improved left ventricular compliance via the FBJ osteosarcoma oncogene/transforming growth factor-β1 pathway. Circulation. 2012;126:840–50.CrossRefPubMed
50.
Zurück zum Zitat Qiu G, Zheng G, Ge M, Wang J, Huang R, Shu Q, et al. Mesenchymal stem cell-derived extracellular vesicles affect disease outcomes via transfer of microRNAs. Stem Cell Res Ther. 2018;9:320.CrossRefPubMedPubMedCentral Qiu G, Zheng G, Ge M, Wang J, Huang R, Shu Q, et al. Mesenchymal stem cell-derived extracellular vesicles affect disease outcomes via transfer of microRNAs. Stem Cell Res Ther. 2018;9:320.CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Salgado-Somoza A, Zhang L, Vausort M, Devaux Y. The circular RNA MICRA for risk stratification after myocardial infarction. IJC Heart Vasc. 2017;17:33–6.CrossRef Salgado-Somoza A, Zhang L, Vausort M, Devaux Y. The circular RNA MICRA for risk stratification after myocardial infarction. IJC Heart Vasc. 2017;17:33–6.CrossRef
52.
Zurück zum Zitat Shi J, Bei Y, Kong X, Liu X, Lei Z, Xu T, et al. miR-17-3p contributes to exercise-induced cardiac growth and protects against myocardial ischemia-reperfusion injury. Theranostics. 2017;7:664–76.CrossRefPubMedPubMedCentral Shi J, Bei Y, Kong X, Liu X, Lei Z, Xu T, et al. miR-17-3p contributes to exercise-induced cardiac growth and protects against myocardial ischemia-reperfusion injury. Theranostics. 2017;7:664–76.CrossRefPubMedPubMedCentral
55.
Zurück zum Zitat Stokfisz K, Ledakowicz-Polak A, Zagorski M, Zielinska M. Ischaemic preconditioning – current knowledge and potential future applications after 30 years of experience. Adv Med Sci. 2017;62:307–16.CrossRefPubMed Stokfisz K, Ledakowicz-Polak A, Zagorski M, Zielinska M. Ischaemic preconditioning – current knowledge and potential future applications after 30 years of experience. Adv Med Sci. 2017;62:307–16.CrossRefPubMed
58.
Zurück zum Zitat van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci. 2008;105:13027–32.CrossRefPubMedPubMedCentral van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci. 2008;105:13027–32.CrossRefPubMedPubMedCentral
59.
Zurück zum Zitat van Rooij E, Purcell AL, Levin AA. Developing microRNA therapeutics. Circ Res. 2012;110:496–507.CrossRefPubMed van Rooij E, Purcell AL, Levin AA. Developing microRNA therapeutics. Circ Res. 2012;110:496–507.CrossRefPubMed
60.
Zurück zum Zitat Vausort M, Wagner DR, Devaux Y. Long noncoding RNAs in patients with acute myocardial infarction. Circ Res. 2014;115:668–77.CrossRefPubMed Vausort M, Wagner DR, Devaux Y. Long noncoding RNAs in patients with acute myocardial infarction. Circ Res. 2014;115:668–77.CrossRefPubMed
61.
Zurück zum Zitat Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15:261–71.CrossRefPubMedPubMedCentral Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15:261–71.CrossRefPubMedPubMedCentral
62.
Zurück zum Zitat Wang X, Zhang X, Ren X-P, Chen J, Liu H, Yang J, et al. MicroRNA-494 targeting both proapoptotic and antiapoptotic proteins protects against ischemia/reperfusion-induced cardiac injury. Circulation. 2010;122:1308–18.CrossRefPubMedPubMedCentral Wang X, Zhang X, Ren X-P, Chen J, Liu H, Yang J, et al. MicroRNA-494 targeting both proapoptotic and antiapoptotic proteins protects against ischemia/reperfusion-induced cardiac injury. Circulation. 2010;122:1308–18.CrossRefPubMedPubMedCentral
63.
Zurück zum Zitat Wang J, Huang W, Xu R, Nie Y, Cao X, Meng J, et al. MicroRNA-24 regulates cardiac fibrosis after myocardial infarction. J Cell Mol Med. 2012;16:2150–60.CrossRefPubMedPubMedCentral Wang J, Huang W, Xu R, Nie Y, Cao X, Meng J, et al. MicroRNA-24 regulates cardiac fibrosis after myocardial infarction. J Cell Mol Med. 2012;16:2150–60.CrossRefPubMedPubMedCentral
64.
Zurück zum Zitat Wang X, Zhu H, Zhang X, Liu Y, Chen J, Medvedovic M, et al. Loss of the miR-144/451 cluster impairs ischaemic preconditioning-mediated cardioprotection by targeting Rac-1. Cardiovasc Res. 2012;94:379–90.CrossRefPubMedPubMedCentral Wang X, Zhu H, Zhang X, Liu Y, Chen J, Medvedovic M, et al. Loss of the miR-144/451 cluster impairs ischaemic preconditioning-mediated cardioprotection by targeting Rac-1. Cardiovasc Res. 2012;94:379–90.CrossRefPubMedPubMedCentral
65.
Zurück zum Zitat Wang K, Long B, Zhou L-Y, Liu F, Zhou Q-Y, Liu C-Y, et al. CARL lncRNA inhibits anoxia-induced mitochondrial fission and apoptosis in cardiomyocytes by impairing miR-539-dependent PHB2 downregulation. Nat Commun. 2014;5:3596.CrossRefPubMed Wang K, Long B, Zhou L-Y, Liu F, Zhou Q-Y, Liu C-Y, et al. CARL lncRNA inhibits anoxia-induced mitochondrial fission and apoptosis in cardiomyocytes by impairing miR-539-dependent PHB2 downregulation. Nat Commun. 2014;5:3596.CrossRefPubMed
66.
Zurück zum Zitat Wang K, Sun T, Li N, Wang Y, Wang J-X, Zhou L-Y, et al. MDRL lncRNA regulates the processing of miR-484 primary transcript by targeting miR-361. PLoS Genet. 2014;10:e1004467.CrossRefPubMedPubMedCentral Wang K, Sun T, Li N, Wang Y, Wang J-X, Zhou L-Y, et al. MDRL lncRNA regulates the processing of miR-484 primary transcript by targeting miR-361. PLoS Genet. 2014;10:e1004467.CrossRefPubMedPubMedCentral
67.
Zurück zum Zitat Wang JX, Zhang XJ, Li Q, Wang K, Wang Y, Jiao JQ, et al. MicroRNA-103/107 regulate programmed necrosis and myocardial ischemia/reperfusion injury through targeting FADD. Circ Res. 2015;117:352–63.CrossRefPubMed Wang JX, Zhang XJ, Li Q, Wang K, Wang Y, Jiao JQ, et al. MicroRNA-103/107 regulate programmed necrosis and myocardial ischemia/reperfusion injury through targeting FADD. Circ Res. 2015;117:352–63.CrossRefPubMed
68.
Zurück zum Zitat Wang K, Liu C-Y, Zhou L-Y, Wang J-X, Wang M, Zhao B, et al. APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p. Nat Commun. 2015;6:6779.CrossRefPubMed Wang K, Liu C-Y, Zhou L-Y, Wang J-X, Wang M, Zhao B, et al. APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p. Nat Commun. 2015;6:6779.CrossRefPubMed
69.
Zurück zum Zitat Wang K, Liu F, Liu C-Y, An T, Zhang J, Zhou L-Y, et al. The long noncoding RNA NRF regulates programmed necrosis and myocardial injury during ischemia and reperfusion by targeting miR-873. Cell Death Differ. 2016;23:1394–405.CrossRefPubMedPubMedCentral Wang K, Liu F, Liu C-Y, An T, Zhang J, Zhou L-Y, et al. The long noncoding RNA NRF regulates programmed necrosis and myocardial injury during ischemia and reperfusion by targeting miR-873. Cell Death Differ. 2016;23:1394–405.CrossRefPubMedPubMedCentral
70.
Zurück zum Zitat Wang K, Gan T-Y, Li N, Liu C-Y, Zhou L-Y, Gao J-N, et al. Circular RNA mediates cardiomyocyte death via miRNA-dependent upregulation of MTP18 expression. Cell Death Differ. 2017;24:1111–20.CrossRefPubMedPubMedCentral Wang K, Gan T-Y, Li N, Liu C-Y, Zhou L-Y, Gao J-N, et al. Circular RNA mediates cardiomyocyte death via miRNA-dependent upregulation of MTP18 expression. Cell Death Differ. 2017;24:1111–20.CrossRefPubMedPubMedCentral
71.
Zurück zum Zitat Wu H-Y, Wu J-L, Ni Z-L. Overexpression of microRNA-202-3p protects against myocardial ischemia-reperfusion injury through activation of TGF-β1/Smads signaling pathway by targeting TRPM6. Cell Cycle. 2019;18:621–37.CrossRefPubMedPubMedCentral Wu H-Y, Wu J-L, Ni Z-L. Overexpression of microRNA-202-3p protects against myocardial ischemia-reperfusion injury through activation of TGF-β1/Smads signaling pathway by targeting TRPM6. Cell Cycle. 2019;18:621–37.CrossRefPubMedPubMedCentral
72.
Zurück zum Zitat Xiao Y, Zhang Y, Chen Y, Li J, Zhang Z, Sun Y, et al. Inhibition of microRNA-9-5p protects against cardiac remodeling following myocardial infarction in mice. Hum Gene Ther. 2018;30:286–301.CrossRefPubMed Xiao Y, Zhang Y, Chen Y, Li J, Zhang Z, Sun Y, et al. Inhibition of microRNA-9-5p protects against cardiac remodeling following myocardial infarction in mice. Hum Gene Ther. 2018;30:286–301.CrossRefPubMed
73.
Zurück zum Zitat Xu H, Cao H, Zhu G, Liu S, Li H. Overexpression of microRNA-145 protects against rat myocardial infarction through targeting PDCD4. Am J Transl Res. 2017;9:5003–11.PubMedPubMedCentral Xu H, Cao H, Zhu G, Liu S, Li H. Overexpression of microRNA-145 protects against rat myocardial infarction through targeting PDCD4. Am J Transl Res. 2017;9:5003–11.PubMedPubMedCentral
74.
Zurück zum Zitat Yamamura S, Sumida MI, Tanaka Y. Interaction and cross-talk between non-coding RNAs. Cell Mol Life Sci. 2018;75:467–84.CrossRefPubMed Yamamura S, Sumida MI, Tanaka Y. Interaction and cross-talk between non-coding RNAs. Cell Mol Life Sci. 2018;75:467–84.CrossRefPubMed
75.
Zurück zum Zitat Yan Y, Zhang B, Liu N, Qi C, Xiao Y, Tian X, et al. Circulating long noncoding RNA UCA1 as a novel biomarker of acute myocardial infarction. Biomed Res Int. 2016;2016:1–7. Yan Y, Zhang B, Liu N, Qi C, Xiao Y, Tian X, et al. Circulating long noncoding RNA UCA1 as a novel biomarker of acute myocardial infarction. Biomed Res Int. 2016;2016:1–7.
76.
Zurück zum Zitat Yang L, Wang B, Zhou Q, Wang Y, Liu X, Liu Z, et al. MicroRNA-21 prevents excessive inflammation and cardiac dysfunction after myocardial infarction through targeting KBTBD7. Cell Death Dis. 2018;9:769.CrossRefPubMedPubMedCentral Yang L, Wang B, Zhou Q, Wang Y, Liu X, Liu Z, et al. MicroRNA-21 prevents excessive inflammation and cardiac dysfunction after myocardial infarction through targeting KBTBD7. Cell Death Dis. 2018;9:769.CrossRefPubMedPubMedCentral
77.
Zurück zum Zitat Ye Y, Hu Z, Lin Y, Zhang C, Perez-Polo JR. Downregulation of microRNA-29 by antisense inhibitors and a PPAR-γ agonist protects against myocardial ischaemia–reperfusion injury. Cardiovasc Res. 2010;87:535–44.CrossRefPubMed Ye Y, Hu Z, Lin Y, Zhang C, Perez-Polo JR. Downregulation of microRNA-29 by antisense inhibitors and a PPAR-γ agonist protects against myocardial ischaemia–reperfusion injury. Cardiovasc Res. 2010;87:535–44.CrossRefPubMed
78.
Zurück zum Zitat Ye Y, Perez-Polo JR, Qian J, Birnbaum Y. The role of microRNA in modulating myocardial ischemia-reperfusion injury. Physiol Genomics. 2011;43:534–42.CrossRefPubMed Ye Y, Perez-Polo JR, Qian J, Birnbaum Y. The role of microRNA in modulating myocardial ischemia-reperfusion injury. Physiol Genomics. 2011;43:534–42.CrossRefPubMed
80.
Zurück zum Zitat Zhou L-Y, Zhai M, Huang Y, Xu S, An T, Wang Y-H, et al. The circular RNA ACR attenuates myocardial ischemia/reperfusion injury by suppressing autophagy via modulation of the Pink1/FAM65B pathway. Cell Death Differ. 2018;26:1299–315.CrossRefPubMedPubMedCentral Zhou L-Y, Zhai M, Huang Y, Xu S, An T, Wang Y-H, et al. The circular RNA ACR attenuates myocardial ischemia/reperfusion injury by suppressing autophagy via modulation of the Pink1/FAM65B pathway. Cell Death Differ. 2018;26:1299–315.CrossRefPubMedPubMedCentral
81.
Zurück zum Zitat Zhu H, Fan G-C. Role of microRNAs in the reperfused myocardium towards post-infarct remodelling. Cardiovasc Res. 2012;94:284–92.CrossRefPubMed Zhu H, Fan G-C. Role of microRNAs in the reperfused myocardium towards post-infarct remodelling. Cardiovasc Res. 2012;94:284–92.CrossRefPubMed
Metadaten
Titel
The Role of Non-coding RNAs in Ischemic Myocardial Reperfusion Injury
verfasst von
Vince Siebert
Joseph Allencherril
Yumei Ye
Xander H. T. Wehrens
Yochai Birnbaum
Publikationsdatum
22.07.2019
Verlag
Springer US
Erschienen in
Cardiovascular Drugs and Therapy / Ausgabe 4/2019
Print ISSN: 0920-3206
Elektronische ISSN: 1573-7241
DOI
https://doi.org/10.1007/s10557-019-06893-x

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