By targeting Stat3 microRNA-17-5p promotes cardiomyocyte apoptosis in response to ischemia followed by reperfusion

Cellular Physiology and Biochemistry

Volumn 34, Issue 3, 2014, Pages 955-965

  Du, Weijie ^a   Pan, Zhenwei ^a   Chen, Xu ^a   Wang, Leimin ^a   Zhang, Ying ^a   Li, Shuang ^a   Liang, Haihai ^a   Xu, Chaoqian ^a   Zhang, Yong ^a   Wu, Yanping ^a   Shan, Hongli ^a   Lu, Yanjie ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Ischemia reperfusion injury; miR 17 5p; Stat3

Indexed keywords

EVANS BLUE; HYDROGEN PEROXIDE; MICRORNA; MICRORNA 17 5P; STAT3 PROTEIN; TRIPHENYLTETRAZOLIUM; UNCLASSIFIED DRUG; MIRN17 MICRORNA, MOUSE; STAT3 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; GENE TARGETING; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE REPERFUSION; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MALE; MOUSE; MTT ASSAY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPERFUSION INJURY; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; PATHOLOGY; RAT; SPRAGUE DAWLEY RAT; TUNEL ASSAY;

MUS; RATTUS;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HYDROGEN PEROXIDE; IN SITU NICK-END LABELING; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MYOCYTES, CARDIAC; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; STAT3 TRANSCRIPTION FACTOR;

EID: 84927124774     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000366312     Document Type: Article

References (38)

1. Zornoff LA, Paiva SA, Duarte DR, Spadaro J: Ventricular remodeling after myocardial infarction: Concepts and clinical implications. Arq Bras Cardiol 2009;92:150-164.
2. Katircioglu SF, Iscan HZ, Ulus T, Saritas Z: Myocardial preservation in acute coronary artery occlusion with coronary sinus retroperfusion and carnitine. J Cardiovasc Surg (Torino) 2000;41:45-50.
3. Zweier JL: Measurement of superoxide-derived free radicals in the reperfused heart. Evidence for a free radical mechanism of reperfusion injury. J Biol Chem 1988;263:1353-1357.
4. Garlick PB, Davies MJ, Hearse DJ, Slater TF: Direct detection of free radicals in the reperfused rat heart using electron spin resonance spectroscopy. Circ Res 1987;61:757-760.
5. Arroyo CM, Kramer JH, Dickens BF, Weglicki WB: Identification of free radicals in myocardial ischemia/ reperfusion by spin trapping with nitrone dmpo. FEBS Letters 1987;221:101-104.
6. McCully JD, Wakiyama H, Hsieh YJ, Jones M, Levitsky S: Differential contribution of necrosis and apoptosis in myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 2004;286:H1923-1935.
7. Abe T, Zhou P, Jackman K, Capone C, Casolla B, Hochrainer K, Kahles T, Ross ME, Anrather J, Iadecola C: Lipoprotein receptor-related protein-6 protects the brain from ischemic injury. Stroke 2013;44:2284-2291.
8. Krol J, Loedige I, Filipowicz W: The widespread regulation of microrna biogenesis, function and decay. Nat Rev Genet 2010;11:597-610.
9. Norbury CJ: 3' Uridylation and the regulation of RNA function in the cytoplasm. Biochem Soc Trans. 2010;38:1150-1153.
10. Ren XP, Wu J, Wang X, Sartor MA, Qian J, Jones K, Nicolaou P, Pritchard TJ, Fan GC: MicroRNA-320 is involved in the regulation of cardiac ischemia/reperfusion injury by targeting heat-shock protein 20. Circulation 2009;119:2357-2366.
11. Wang X, Zhang X, Ren XP, Chen J, Liu H, Yang J, Medvedovic M, Hu Z, Fan GC: MicroRNA-494 targeting both proapoptotic and antiapoptotic proteins protects against ischemia/reperfusion-induced cardiac injury. Circulation 2010;122:1308-1318.
12. Pan Z, Sun X, Ren J, Li X, Gao X, Lu C, Zhang Y, Sun H, Wang Y, Wang H, Wang J, Xie L, Lu Y, Yang B: MiR-1 exacerbates cardiac ischemia-reperfusion injury in mouse models. PLoS One 2012;7:e50515.
13. Mogilyansky E, Rigoutsos I: The miR-17/92 cluster: A comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ 2013;20:1603-1614.
14. Zhou L, Qi RQ, Liu M, Xu YP, Li G, Weiland M, Kaplan DH, Mi QS: MicroRNA miR-17-92 cluster is highly expressed in epidermal langerhans cells but not required for its development. Genes Immun 2014;15:57-61.
15. Chen J, Huang ZP, Seok HY, Ding J, Kataoka M, Zhang Z, Hu X, Wang G, Lin Z, Wang S, Pu WT, Liao R, Wang DZ: MiR-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ Res 2013;112:1557-1566.
16. Yu J, Ohuchida K, Mizumoto K, Fujita H, Nakata K, Tanaka M: MicroRNA miR-17-5p is overexpressed in pancreatic cancer, associated with a poor prognosis, and involved in cancer cell proliferation and invasion. Cancer Biol Ther 2010;10:748-757.
17. Takakura S, Mitsutake N, Nakashima M, Namba H, Saenko VA, Rogounovitch TI, Nakazawa Y, Hayashi T, Ohtsuru A, Yamashita S: Oncogenic role of miR-17-92 cluster in anaplastic thyroid cancer cells. Cancer Sci 2008;99:1147-1154.
18. Zhang B, Pan X, Cobb GP, Anderson TA: MicroRNAs as oncogenes and tumor suppressors. Dev Biol 2007;302:1-12.
19. Danielson LS, Park DS, Rotllan N, Chamorro-Jorganes A, Guijarro MV, Fernandez-Hernando C, Fishman GI, Phoon CK, Hernando E: Cardiovascular dysregulation of miR-17-92 causes a lethal hypertrophic cardiomyopathy and arrhythmogenesis. FASEB J 2013;27:1460-1467.
20. Kaucsar T, Revesz C, Godo M, Krenacs T, Albert M, Szalay CI, Rosivall L, Benyo Z, Batkai S, Thum T, Szenasi G, Hamar P: Activation of the miR-17 family and miR-21 during murine kidney ischemia-reperfusion injury. Nucleic Acid Ther 2013;23:344-354.
21. Yeh CT, Huang WC, Rao YK, Ye M, Lee WH, Wang LS, Tzeng DT, Wu CH, Shieh YS, Huang CY, Chen YJ, Hsiao M, Wu AT, Yang Z, Tzeng YM: A sesquiterpene lactone antrocin from antrodia camphorata negatively modulates Jak2/Stat3 signaling via microRNA let-7c and induces apoptosis in lung cancer cells. Carcinogenesis 2013;34:2918-2928.
22. Yang Y, Duan W, Jin Z, Yi W, Yan J, Zhang S, Wang N, Liang Z, Li Y, Chen W, Yi D, Yu S: Jak2/Stat3 activation by melatonin attenuates the mitochondrial oxidative damage induced by myocardial ischemia/reperfusion injury. J Pineal Res 2013;55:275-286.
23. Vandeput F, Krall J, Ockaili R, Salloum FN, Florio V, Corbin JD, Francis SH, Kukreja RC, Movsesian MA: Cgmphydrolytic activity and its inhibition by sildenafil in normal and failing human and mouse myocardium. J Pharmacol Exp Ther 2009;330:884-891.
24. Li YS, Gao BR: Transplantation of neonatal cardiomyocytes plus fibrin sealant restores myocardial function in a rat model of myocardial infarction. Chin Med J (Engl) 2007;120:2022-2027.
25. Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B, Zhang Y, Xu C, Bai Y, Wang H, Chen G, Wang Z: The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med 2007;13:486-491.
26. Jiang J, Lee EJ, Gusev Y, Schmittgen TD: Real-time expression profiling of microRNA precursors in human cancer cell lines. Nucleic Acids Res 2005;33:5394-5403.
27. Cebotari S, Mertsching H, Kallenbach K, Kostin S, Repin O, Batrinac A, Kleczka C, Ciubotaru A, Haverich A: Construction of autologous human heart valves based on an acellular allograft matrix. Circulation 2002;106:I63-I68.
28. Ng IH, Yeap YY, Ong LS, Jans DA, Bogoyevitch MA: Oxidative stress impairs multiple regulatory events to drive persistent cytokine-stimulated Stat3 phosphorylation. Biochim Biophys Acta 2014;1843:483-94.
29. Lu Y, Zhou J, Xu C, Lin H, Xiao J, Wang Z, Yang B: Jak/Stat and PI3K/Akt pathways form a mutual transactivation loop and afford resistance to oxidative stress-induced apoptosis in cardiomyocytes. Cell Physiol Biochem 2008;21:305-314.
30. Chien CT, Chen CF, Hsu SM, Lee PH, Lai MK: Protective mechanism of preconditioning hypoxia attenuates apoptosis formation during renal ischemia/reperfusion phase. Transplant Proc 1999;31:2012-2013.
31. Vanlangenakker N, Vanden Berghe T, Krysko DV, Festjens N, Vandenabeele P: Molecular mechanisms and pathophysiology of necrotic cell death. Curr Mol Med 2008;8:207-220.
32. Halestrap AP: Calcium, mitochondria and reperfusion injury: A pore way to die. Biochem Soc Trans 2006;34:232-237.
33. Spaccarotella E, Pellegrino E, Ferracin M, Ferreri C, Cuccuru G, Liu C, Iqbal J, Cantarella D, Taulli R, Provero P, Di Cunto F, Medico E, Negrini M, Chan WC, Inghirami G, Piva R: Stat3-mediated activation of microRNA cluster 17~92 promotes proliferation and survival of ALK-positive anaplastic large cell lymphoma. Haematologica 2014;99:116-24.
34. Novotny GW, Sonne SB, Nielsen JE, Jonstrup SP, Hansen MA, Skakkebaek NE, Rajpert-De Meyts E, Kjems J, Leffers H: Translational repression of E2F1 mRNA in carcinoma in situ and normal testis correlates with expression of the miR-17-92 cluster. Cell Death Differ 2007;14:879-882.
35. Cloonan N, Brown MK, Steptoe AL, Wani S, Chan WL, Forrest AR, Kolle G, Gabrielli B, Grimmond SM: The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol 2008;9:R127.
36. Bhattacharya S, Ray RM, Johnson LR: Stat3-mediated transcription of Bcl-2, Mcl-1 and c-IAP2 prevents apoptosis in polyamine-depleted cells. Biochem J 2005;392:335-344.
37. Dziennis S, Jia T, Ronnekleiv OK, Hurn PD, Alkayed NJ: Role of signal transducer and activator of transcription-3 in estradiol-mediated neuroprotection. J Neurosci 2007;27:7268-7274.
38. Arribas SM, Hermida C, Gonzalez MC, Wang Y, Hinek A: Enhanced survival of vascular smooth muscle cells accounts for heightened elastin deposition in arteries of neonatal spontaneously hypertensive rats. Exp Physiol 2010;95:550-560.