Differential Cardiac MicroRNA Expression Predicts the Clinical Course in Human Enterovirus Cardiomyopathy

Circulation: Heart Failure

Volumn 8, Issue 3, 2015, Pages 605-618

  Kuehl, Uwe ^a   Lassner, Dirk ^b   Gast, Martina ^a   Stroux, Andrea ^a   Rohde, Maria ^b   Siegismund, Christine ^a   Wang, Xiaomin ^a   Escher, Felicitas ^a   Gross, Michael ^a   Skurk, Carsten ^a   Tschoepe, Carsten ^a   Loebel, Madlen ^a   Scheibenbogen, Carmen ^a   Schultheiss, Heinz Peter ^a   Poller, Wolfgang ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Institute for Cardiac Diagnostic and Therapy (IKDT)   (Germany)

Author keywords

cardiomyopathies; immune system; microRNAs; viruses

Indexed keywords

MICRORNA; TRANSCRIPTOME; ANTISENSE OLIGONUCLEOTIDE; GENETIC MARKER; MESSENGER RNA;

AREA UNDER THE CURVE; ARTICLE; CARDIOMYOPATHY; COHORT ANALYSIS; CONFIDENCE INTERVAL; CONTROLLED STUDY; DETERIORATION; DISEASE COURSE; ENTEROVIRUS; FOLLOW UP; HEART MUSCLE BIOPSY; HUMAN; HUMAN CELL; HUMAN ENTEROVIRUS CARDIOMYOPATHY; IMMUNE RESPONSE GENE; MONONUCLEAR CELL; NONHUMAN; PERSISTENT VIRUS INFECTION; PREDICTION; PRIORITY JOURNAL; RECEIVER OPERATING CHARACTERISTIC; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCREENING; VIRAL CLEARANCE; ADULT; CARDIOMYOPATHIES; COXSACKIEVIRUS INFECTIONS; DNA MICROARRAY; ENTEROVIRUS B; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC MARKER; GENETIC TRANSFECTION; GENETICS; HEART MUSCLE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; PATHOGENICITY; PREDICTIVE VALUE; PROCEDURES; REPRODUCIBILITY; TUMOR CELL LINE; VIROLOGY;

ADULT; AREA UNDER CURVE; CARDIOMYOPATHIES; CELL LINE, TUMOR; COXSACKIEVIRUS INFECTIONS; DISEASE PROGRESSION; ENTEROVIRUS B, HUMAN; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENETIC MARKERS; HOST-PATHOGEN INTERACTIONS; HUMANS; MALE; MICRORNAS; MIDDLE AGED; MULTIVARIATE ANALYSIS; MYOCARDIUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OLIGONUCLEOTIDES, ANTISENSE; PREDICTIVE VALUE OF TESTS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; ROC CURVE; TRANSCRIPTOME; TRANSFECTION;

EID: 84938507800     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.114.001475     Document Type: Article

References (51)

1. Mattick JS, Taft RJ, Faulkner GJ. A global view of genomic information-moving beyond the gene and the master regulator. Trends Genet. 2010;26:21-28. doi: 10.1016/j.tig.2009.11.002.
2. Poller W, Tank J, Skurk C, Gast M. Cardiovascular RNA interference therapy: the broadening tool and target spectrum. Circ Res. 2013;113:588-602. doi: 10.1161/CIRCRESAHA.113.301056.
3. Suckau L, Fechner H, Chemaly E, Krohn S, Hadri L, Kockskämper J, Westermann D, Bisping E, Ly H, Wang X, Kawase Y, Chen J, Liang L, Sipo I, Vetter R, Weger S, Kurreck J, Erdmann V, Tschope C, Pieske B, Lebeche D, Schultheiss HP, Hajjar RJ, Poller WC. Long-term cardiac-targeted RNA interference for the treatment of heart failure restores cardiac function and reduces pathological hypertrophy. Circulation. 2009;119:1241-1252. doi: 10.1161/CIRCULATIONAHA.108.783852.
4. Majmudar MD, Keliher EJ, Heidt T, Leuschner F, Truelove J, Sena BF, Gorbatov R, Iwamoto Y, Dutta P, Wojtkiewicz G, Courties G, Sebas M, Borodovsky A, Fitzgerald K, Nolte MW, Dickneite G, Chen JW, Anderson DG, Swirski FK, Weissleder R, Nahrendorf M. Monocytedirected RNAi targeting CCR2 improves infarct healing in atherosclerosis-prone mice. Circulation. 2013;127:2038-2046. doi: 10.1161/CIRCULATIONAHA.112.000116.
5. Tank J, Lindner D, Wang X, Stroux A, Gilke L, Gast M, Zietsch C, Skurk C, Scheibenbogen C, Klingel K, Lassner D, Kühl U, Schultheiss HP, Westermann D, Poller W. Single-target RNA interference for the blockade of multiple interacting proinflammatory and profibrotic pathways in cardiac fibroblasts. J Mol Cell Cardiol. 2014;66:141-156. doi: 10.1016/j. yjmcc.2013.11.004.
6. van Rooij E, Purcell AL, Levin AA. Developing microRNA therapeutics. Circ Res. 2012;110:496-507. doi: 10.1161/CIRCRESAHA.111.247916.
7. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, Burchfield J, Fox H, Doebele C, Ohtani K, Chavakis E, Potente M, Tjwa M, Urbich C, Zeiher AM, Dimmeler S. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science. 2009;324:1710-1713. doi: 10.1126/science.1174381.
8. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Galuppo P, Just S, Rottbauer W, Frantz S, Castoldi M, Soutschek J, Koteliansky V, Rosenwald A, Basson MA, Licht JD, Pena JT, Rouhanifard SH, Muckenthaler MU, Tuschl T, Martin GR, Bauersachs J, Engelhardt S. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature. 2008;456:980-984. doi: 10.1038/nature07511.
9. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, Epstein CB, Frietze S, Harrow J, Kaul R, Khatun J, Lajoie BR, Landt SG, Lee BK, Pauli F, Rosenbloom KR, Sabo P, Safi A, Sanyal A, Shoresh N, Simon JM, Song L, Trinklein ND, Altshuler RC, Birney E, Brown JB, Cheng C, Djebali S, Dong X, Dunham I, Ernst J, Furey TS, Gerstein M, Giardine B, Greven M, Hardison RC, Harris RS, Herrero J, Hoffman MM, Iyer S, Kelllis M, Khatun J, Kheradpour P, Kundaje A, Lassmann T, Li Q, Lin X, Marinov GK, Merkel A, Mortazavi A, Parker SC, Reddy TE, Rozowsky J, Schlesinger F, Thurman RE, Wang J, Ward LD, Whitfield TW, Wilder SP, Wu W, Xi HS, Yip KY, Zhuang J, Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M, Pazin MJ, Lowdon RF, Dillon LA, Adams LB, Kelly CJ, Zhang J, Wexler JR, Green ED, Good PJ, Feingold EA, Bernstein BE, Birney E, Crawford GE, Dekker J, Elinitski L, Farnham PJ, Gerstein M, Giddings MC, Gingeras TR, Green ED, Guigo R, Hardison RC, Hubbard TJ, Kellis M, Kent WJ, Lieb JD, Margulies EH, Myers RM, Snyder M, Starnatoyannopoulos JA,An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
10. Bernstein BE, Birney E, Dunham I, Green ED, Gunter C and Snyder M. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
11. Volders PJ, Helsens K, Wang X, Menten B, Martens L, Gevaert K, Vandesompele J, Mestdagh P. LNCipedia: a database for annotated human lncRNA transcript sequences and structures. Nucleic Acids Res. 2013;41(Database issue):D246-D251. doi: 10.1093/nar/gks915.
12. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigó R. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012;22:1775-1789. doi: 10.1101/gr.132159.111.
13. Marfella R, Di Filippo C, Potenza N, Sardu C, Rizzo MR, Siniscalchi M, Musacchio E, Barbieri M, Mauro C, Mosca N, Solimene F, Mottola MT, Russo A, Rossi F, Paolisso G, D'Amico M. Circulating microRNA changes in heart failure patients treated with cardiac resynchronization therapy: responders vs. non-responders. Eur J Heart Fail. 2013;15:1277-1288. doi: 10.1093/eurjhf/hft088.
14. Matsumoto S, Sakata Y, Suna S, Nakatani D, Usami M, Hara M, Kitamura T, Hamasaki T, Nanto S, Kawahara Y, Komuro I. Circulating p53-responsive microRNAs are predictive indicators of heart failure after acute myocardial infarction. Circ Res. 2013;113:322-326. doi: 10.1161/CIRCRESAHA.113.301209.
15. Jaguszewski M, Osipova J, Ghadri JR, Napp LC, Widera C, Franke J, Fijalkowski M, Nowak R, Fijalkowska M, Volkmann I, Katus HA, Wollert KC, Bauersachs J, Erne P, Lüscher TF, Thum T, Templin C. A signature of circulating microRNAs differentiates takotsubo cardiomyopathy from acute myocardial infarction. Eur Heart J. 2014;35:999-1006. doi: 10.1093/eurheartj/eht392.
16. Vogel B, Keller A, Frese KS, Leidinger P, Sedaghat-Hamedani F, Kayvanpour E, Kloos W, Backe C, Thanaraj A, Brefort T, Beier M, Hardt S, Meese E, Katus HA, Meder B. Multivariate miRNA signatures as biomarkers for non-ischaemic systolic heart failure. Eur Heart J. 2013;34:2812-2822. doi: 10.1093/eurheartj/eht256.
17. Kühl U, Pauschinger M, Schwimmbeck PL, Seeberg B, Lober C, Noutsias M, Poller W, Schultheiss HP. Interferon-beta treatment eliminates cardiotropic viruses and improves left ventricular function in patients with myocardial persistence of viral genomes and left ventricular dysfunction. Circulation. 2003;107:2793-2798. doi: 10.1161/01. CIR.0000072766.67150.51.
18. Kühl U, Pauschinger M, Noutsias M, Seeberg B, Bock T, Lassner D, Poller W, Kandolf R, Schultheiss HP. High prevalence of viral genomes and multiple viral infections in the myocardium of adults with "idiopathic" left ventricular dysfunction. Circulation. 2005;111:887-893. doi: 10.1161/01.CIR.0000155616.07901.35.
19. Kühl U, Lassner D, von Schlippenbach J, Poller W, Schultheiss HP. Interferon-Beta improves survival in enterovirus-associated cardiomyopathy. J Am Coll Cardiol. 2012;60:1295-1296. doi: 10.1016/j. jacc.2012.06.026.
20. Corsten MF, Papageorgiou A, Verhesen W, Carai P, Lindow M, Obad S, Summer G, Coort SL, Hazebroek M, van Leeuwen R, Gijbels MJ, Wijnands E, Biessen EA, De Winther MP, Stassen FR, Carmeliet P, Kauppinen S, Schroen B, Heymans S. MicroRNA profiling identifies microRNA-155 as an adverse mediator of cardiac injury and dysfunction during acute viral myocarditis. Circ Res. 2012;111:415-425. doi: 10.1161/CIRCRESAHA.112.267443.
21. Seko Y, Kayagaki N, Seino K, Yagita H, Okumura K, Nagai R. Role of Fas/FasL pathway in the activation of infiltrating cells in murine acute myocarditis caused by Coxsackievirus B3. J Am Coll Cardiol. 2002;39:1399-1403.
22. Huber S, Shi C, Budd RC. Gammadelta T cells promote a Th1 response during coxsackievirus B3 infection in vivo: role of Fas and Fas ligand. J Virol. 2002;76:6487-6494.
23. Junt T, Scandella E, Förster R, Krebs P, Krautwald S, Lipp M, Hengartner H, Ludewig B. Impact of CCR7 on priming and distribution of antiviral effector and memory CTL. J Immunol. 2004;173:6684-6693.
24. Nickel T, Pfeiler S, Summo C, Kopp R, Meimarakis G, Sicic Z, Lambert M, Lackermair K, David R, Beiras-Fernandez A, Kaczmarek I, Weis M. oxLDL downregulates the dendritic cell homing factors CCR7 and CCL21. Mediators Inflamm. 2012;2012:320953. doi: 10.1155/2012/320953.
25. Leptidis S, El Azzouzi H, Lok SI, de Weger R, Olieslagers S, Olieslagers S, Kisters N, Silva GJ, Heymans S, Cuppen E, Berezikov E, De Windt LJ, da Costa Martins P. A deep sequencing approach to uncover the miRNOME in the human heart. PLoS One. 2013;8:e57800. doi: 10.1371/journal.pone.0057800.
26. Condorelli G, Latronico MV, Dorn GW 2nd. microRNAs in heart disease: putative novel therapeutic targets Eur Heart J. 2010;31:649-658. doi: 10.1093/eurheartj/ehp573.
27. Naga Prasad SV, Duan ZH, Gupta MK, Surampudi VS, Volinia S, Calin GA, Liu CG, Kotwal A, Moravec CS, Starling RC, Perez DM, Sen S, Wu Q, Plow EF, Croce CM, Karnik S. Unique microRNA profile in endstage heart failure indicates alterations in specific cardiovascular signaling networks. J Biol Chem. 2009;284:27487-27499. doi: 10.1074/jbc. M109.036541.
28. Heymans S, Corsten MF, Verhesen W, Carai P, van Leeuwen RE, Custers K, Peters T, Hazebroek M, Stöger L, Wijnands E, Janssen BJ, Creemers EE, Pinto YM, Grimm D, Schürmann N, Vigorito E, Thum T, Stassen F, Yin X, Mayr M, de Windt LJ, Lutgens E, Wouters K, de Winther MP, Zacchigna S, Giacca M, van Bilsen M, Papageorgiou AP, Schroen B. Macrophage microRNA-155 promotes cardiac hypertrophy and failure. Circulation. 2013;128:1420-1432. doi: 10.1161/CIRCULATIONAHA.112.001357.
29. Papait R, Greco C, Kunderfranco P, Latronico MV, Condorelli G. Epigenetics: a new mechanism of regulation of heart failure Basic Res Cardiol. 2013;108:361. doi: 10.1007/s00395-013-0361-1.
30. Schonrock N, Harvey RP, Mattick JS. Long noncoding RNAs in cardiac development and pathophysiology. Circ Res. 2012;111:1349-1362. doi: 10.1161/CIRCRESAHA.112.268953.
31. Sati S, Ghosh S, Jain V, Scaria V, Sengupta S. Genome-wide analysis reveals distinct patterns of epigenetic features in long non-coding RNA loci. Nucleic Acids Res. 2012;40:10018-10031. doi: 10.1093/nar/gks776.
32. Walsh D, Mohr I. Viral subversion of the host protein synthesis machinery. Nat Rev Microbiol. 2011;9:860-875. doi: 10.1038/nrmicro2655.
33. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature. 2007;449:919-922. doi: 10.1038/nature06205.
34. Liang D, Gao Y, Lin X, He Z, Zhao Q, Deng Q, Lan K. A human herpesvirus miRNA attenuates interferon signaling and contributes to maintenance of viral latency by targeting IKK. Cell Res. 2011;21:793-806. doi: 10.1038/cr.2011.5.
35. David M. Interferons and microRNAs. J Interferon Cytokine Res. 2010;30:825-828. doi: 10.1089/jir.2010.0080.
36. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros WH, Chi JT, Braich R, Manoharan M, Soutschek J, Ohler U, Cullen BR. A viral microRNA functions as an orthologue of cellular miR-155. Nature. 2007;450:1096-1099. doi: 10.1038/nature05992.
37. Wen BP, Dai HJ, Yang YH, Zhuang Y, Sheng R. MicroRNA-23b inhibits enterovirus 71 replication through downregulation of EV71 VPl protein. Intervirology. 2013;56:195-200. doi: 10.1159/000348504.
38. Zheng Z, Ke X, Wang M, He S, Li Q, Zheng C, Zhang Z, Liu Y, Wang H. Human microRNA hsa-miR-296-5p suppresses enterovirus 71 replication by targeting the viral genome. J Virol. 2013;87:5645-5656. doi: 10.1128/JVI.02655-12.
39. Ye X, Hemida MG, Qiu Y, Hanson PJ, Zhang HM, Yang D. MiR-126 promotes coxsackievirus replication by mediating cross-talk of ERK1/2 and Wnt/-catenin signal pathways. Cell Mol Life Sci. 2013;70:4631-4644. doi: 10.1007/s00018-013-1411-4.
40. Tong L, Lin L, Wu S, Guo Z, Wang T, Qin Y, Wang R, Zhong X, Wu X, Wang Y, Luan T, Wang Q, Li Y, Chen X, Zhang F, Zhao W, Zhong Z. MiR-10a, up-regulates coxsackievirus B3 biosynthesis by targeting the 3D-coding sequence. Nucleic Acids Res. 2013;41:3760-3771. doi: 10.1093/nar/gkt058.
41. Hemida MG, Ye X, Zhang HM, Hanson PJ, Liu Z, McManus BM, Yang D. MicroRNA-203 enhances coxsackievirus B3 replication through targeting zinc finger protein-148. Cell Mol Life Sci. 2013;70:277-291. doi: 10.1007/s00018-012-1104-4.
42. Wang L, Qin Y, Tong L, Wu S, Wang Q, Jiao Q, Guo Z, Lin L, Wang R, Zhao W, Zhong Z. MiR-342-5p suppresses coxsackievirus B3 biosynthesis by targeting the 2C-coding region. Antiviral Res. 2012;93:270-279. doi: 10.1016/j.antiviral.2011.12.004.
43. Ho BC, Yu SL, Chen JJ, Chang SY, Yan BS, Hong QS, Singh S, Kao CL, Chen HY, Su KY, Li KC, Cheng CL, Cheng HW, Lee JY, Lee CN, Yang PC. Enterovirus-induced miR-141 contributes to shutoff of host protein translation by targeting the translation initiation factor eIF4E. Cell Host Microbe. 2011;9:58-69. doi: 10.1016/j.chom.2010.12.001.
44. He J, Yue Y, Dong C, Xiong S. MiR-21 confers resistance against CVB3-induced myocarditis by inhibiting PDCD4-mediated apoptosis. Clin Invest Med. 2013;36:E103-E111.
45. Liu YL, Wu W, Xue Y, Gao M, Yan Y, Kong Q, Pang Y, Yang F. MicroRNA-21 and-146b are involved in the pathogenesis of murine viral myocarditis by regulating TH-17 differentiation. Arch Virol. 2013;158:1953-1963. doi: 10.1007/s00705-013-1695-6.
46. Wang X, Ha T, Liu L, Zou J, Zhang X, Kalbfleisch J, Gao X, Williams D, Li C. Increased expression of microRNA-146a decreases myocardial ischaemia/reperfusion injury. Cardiovasc Res. 2013;97:432-442. doi: 10.1093/cvr/cvs356.
47. Klattenhoff CA, Scheuermann JC, Surface LE, Bradley RK, Fields PA, Steinhauser ML, Ding H, Butty VL, Torrey L, Haas S, Abo R, Tabebordbar M, Lee RT, Burge CB, Boyer LA. Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell. 2013;152:570-583. doi: 10.1016/j.cell.2013.01.003.
48. Bidzhekov K, Gan L, Denecke B, Rostalsky A, Hristov M, Koeppel TA, Zernecke A, Weber C. microRNA expression signatures and parallels between monocyte subsets and atherosclerotic plaque in humans. Thromb Haemost. 2012;107:619-625. doi: 10.1160/TH11-09-0607.
49. Siegel SR, Mackenzie J, Chaplin G, Jablonski NG, Griffiths L. Circulating microRNAs involved in multiple sclerosis. Mol Biol Rep. 2012;39:6219-6225. doi: 10.1007/s11033-011-1441-7.
50. Keller A, Leidinger P, Lange J, Borries A, Schroers H, Scheffler M, Lenhof HP, Ruprecht K, Meese E. Multiple sclerosis: microRNA expression profiles accurately differentiate patients with relapsingremitting disease from healthy controls. PLoS One. 2009;4:e7440. doi: 10.1371/journal.pone.0007440.
51. Kühl U, Pauschinger M, Seeberg B, Lassner D, Noutsias M, Poller W, Schultheiss HP. Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation. 2005;112:1965-1970. doi: 10.1161/CIRCULATIONAHA.105.548156.