MicroRNA-21 mediates isoflurane-induced cardioprotection against ischemia-reperfusion injury via Akt/Nitric oxide synthase/mitochondrial permeability transition pore pathway

Anesthesiology

Volumn 123, Issue 4, 2015, Pages 786-798

  Qiao, Shigang ^a   Olson, Jessica M ^a,b   Paterson, Mark ^a   Yan, Yasheng ^a   Zaja, Ivan ^a   Liu, Yanan ^a   Riess, Matthias L ^b,c   Kersten, Judy R ^a   Liang, Mingyu ^b   Warltier, David C ^a   Bosnjak, Zeljko J ^a   Ge, Zhi Dong ^a,b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Department of Physiology ^*  (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TROPOMYOSIN; BETA ACTIN; COMPLEMENTARY DNA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INITIATION FACTOR 4A; ISOFLURANE; MARCKS PROTEIN; MESSENGER RNA; MICRORNA 21; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN KINASE B; PROTEIN S7; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CARDIOTONIC AGENT; CARRIER PROTEIN; MICRORNA; MIRN21 MICRORNA, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EX VIVO STUDY; FLUORESCENCE; HEART FUNCTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART MUSCLE CELL; HEART PERFORMANCE; HEART PROTECTION; IN VIVO STUDY; KNOCKOUT MOUSE; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSTHORACIC ECHOCARDIOGRAPHY; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; MALE; METABOLISM; MYOCARDIAL REPERFUSION INJURY; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOTONIC AGENTS; CELLS, CULTURED; ISOFLURANE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; NITRIC OXIDE SYNTHASE; ORGAN CULTURE TECHNIQUES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84942056683     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0000000000000807     Document Type: Article

References (40)

1. Kersten JR, Schmeling TJ, Pagel PS, Gross GJ, Warltier DC: Isoflurane mimics ischemic preconditioning via activation of K(ATP) channels: Reduction of myocardial infarct size with an acute memory phase. Anesthesiolog y 1997; 87:361-70
2. Raphael J, Rivo J, Gozal Y: Isoflurane-induced myocardial preconditioning is dependent on phosphatidylinositol-3-kinase/Akt signalling. Br J Anaesth 2005; 95:756-63
3. Raphael J, Abedat S, Rivo J, Meir K, Beeri R, Pugatsch T, Zuo Z, Gozal Y: Volatile anesthetic preconditioning attenuates myocardial apoptosis in rabbits after regional ischemia and reperfusion via Akt signaling and modulation of Bcl-2 family proteins. J Pharmacol Exp Ther 2006; 318:186-94
4. Lang XE, Wang X, Zhang KR, Lv JY, Jin JH, Li QS: Isoflurane preconditioning confers cardioprotection by activation of ALDH2. PLoS One 2013; 8:e52469
5. De Hert SG, ten Broecke PW, Mertens E, Van Sommeren EW, De Blier IG, Stockman BA, Rodrigus IE: Sevoflurane but not propofol preserves myocardial function in coronary surgery patients. Anesthesiolog y 2002; 97:42-9
6. Frssdorf J, Borowski A, Ebel D, Feindt P, Hermes M, Meemann T, Weber R, Mllenheim J, Weber NC, Preckel B, Schlack W: Impact of preconditioning protocol on anesthetic-induced cardioprotection in patients having coronary artery bypass surgery. J Thorac Cardiovasc Surg 2009; 137:1436-42, 1442.e1-2
7. Pagel PS: Myocardial protection by volatile anesthetics in patients undergoing cardiac surgery: A critical review of the laboratory and clinical evidence. J Cardiothorac Vasc Anesth 2013; 27:972-82
8. Sayed D, He M, Hong C, Gao S, Rane S, Yang Z, Abdellatif M: MicroRNA-21 is a downstream effector of AKT that mediates its antiapoptotic effects via suppression of Fas ligand. J Biol Chem 2010; 285:20281-90
9. Chen J, Wang DZ: microRNAs in cardiovascular development. J Mol Cell Cardiol 2012; 52:949-57
10. Cheng Y, Ji R, Yue J, Yang J, Liu X, Chen H, Dean DB, Zhang C: MicroRNAs are aberrantly expressed in hypertrophic heart: Do they play a role in cardiac hypertrophy? Am J Pathol 2007; 170:1831-40
11. Surez Y, Fernndez-Hernando C, Pober JS, Sessa WC: Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 2007; 100:1164-73
12. Cheng Y, Zhang C: MicroRNA-21 in cardiovascular disease. J Cardiovasc Transl Res 2010; 3:251-5
13. Li J, Zhao L, He X, Yang T, Yang K: MiR-21 inhibits c-Ski signaling to promote the proliferation of rat vascular smooth muscle cells. Cell Signal 2014; 26:724-9
14. Bang C, Batkai S, Dangwal S, Gupta SK, Foinquinos A, Holzmann A, Just A, Remke J, Zimmer K, Zeug A, Ponimaskin E, Schmiedl A, Yin X, Mayr M, Halder R, Fischer A, Engelhardt S, Wei Y, Schober A, Fiedler J, Thum T: Cardiac fibroblastderived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Invest 2014; 124:2136-46
15. Dong S, Ma W, Hao B, Hu F, Yan L, Yan X, Wang Y, Chen Z, Wang Z: microRNA-21 promotes cardiac fibrosis and development of heart failure with preserved left ventricular ejection fraction by up-regulating Bcl-2. Int J Clin Exp Pathol 2014; 7:565-74
16. 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; 456:980-4
17. 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; 284:29514-25
18. Duygu B, Da Costa Martins PA: miR-21: A star player in cardiac hypertrophy. Cardiovasc Res 2015; 105:235-7
19. Toldo S, Das A, Mezzaroma E, Chau VQ, Marchetti C, Durrant D, Samidurai A, Van Tassell BW, Yin C, Ockaili RA, Vigneshwar N, Mukhopadhyay ND, Kukreja RC, Abbate A, Salloum FN: Induction of microRNA-21 with exogenous hydrogen sulfide attenuates myocardial ischemic and inflammatory injury in mice. Circ Cardiovasc Genet 2014; 7:311-20
20. Olson JM, Yan Y, Bai X, Ge ZD, Liang M, Kriegel AJ, Twaroski DM, Bosnjak ZJ: Up-regulation of microRNA-21 mediates isoflurane-induced protection of cardiomyocytes. Anesthesiolog y 2015; 122:795-805
21. Ge ZD, Peart JN, Kreckler LM, Wan TC, Jacobson MA, Gross GJ, Auchampach JA: Cl-IB-MECA [2-chloro-N6-(3-iodobenzyl) adenosine-5-N-methylcarboxamide] reduces ischemia/reperfusion injury in mice by activating the A3 adenosine receptor. J Pharmacol Exp Ther 2006; 319:1200-10
22. Saegusa N, Sato T, Saito T, Tamagawa M, Komuro I, Nakaya H: Kir6.2-deficient mice are susceptible to stimulated ANP secretion: K(ATP) channel acts as a negative feedback mechanism? Cardiovasc Res 2005; 67:60-8
23. Small EM, Frost RJ, Olson EN: MicroRNAs add a new dimension to cardiovascular disease. Circulation 2010; 121:1022-32
24. Ge ZD, Ionova IA, Vladic N, Pravdic D, Hirata N, Vsquez-Vivar J, Pratt PF Jr, Warltier DC, Pieper GM, Kersten JR: Cardiac-specific overexpression of GTP cyclohydrolase 1 restores ischaemic preconditioning during hyperglycaemia. Cardiovasc Res 2011; 91:340-9
25. Ramanujam N: Fluorescence spectroscopy of neoplastic and non-neoplastic tissues. Neoplasia 2000; 2:89-117
26. Riess ML, Camara AK, Kevin LG, An J, Stowe DF: Reduced reactive O2 species formation and preserved mitochondrial NADH and Ca2+ levels during short-term 17C ischemia in intact hearts. Cardiovasc Res 2004; 61:580-90
27. Chen CH, Chuang JH, Liu K, Chan JY: Nitric oxide triggers delayed anesthetic preconditioning-induced cardiac protection via activation of nuclear factor-κB and upregulation of inducible nitric oxide synthase. Shock 2008; 30:241-9
28. Sedlic F, Pravdic D, Hirata N, Mio Y, Sepac A, Camara AK, Wakatsuki T, Bosnjak ZJ, Bienengraeber M: Monitoring mitochondrial electron fluxes using NAD(P)H-flavoprotein fluorometry reveals complex action of isoflurane on cardiomyocytes. Biochim Biophys Acta 2010; 1797:1749-58
29. Canfield SG, Sepac A, Sedlic F, Muravyeva MY, Bai X, Bosnjak ZJ: Marked hyperglycemia attenuates anesthetic preconditioning in human-induced pluripotent stem cell-derived cardiomyocytes. Anesthesiolog y 2012; 117:735-44
30. Ge ZD, van der Hoeven D, Maas JE, Wan TC, Auchampach JA: A(3) adenosine receptor activation during reperfusion reduces infarct size through actions on bone marrow-derived cells. J Mol Cell Cardiol 2010; 49:280-6
31. Papagiannakopoulos T, Shapiro A, Kosik KS: MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 2008; 68:8164-72
32. Roy S, Khanna S, Hussain SR, Biswas S, Azad A, Rink C, Gnyawali S, Shilo S, Nuovo GJ, Sen CK: MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc Res 2009; 82:21-9
33. Moens AL, Champion HC, Claeys MJ, Tavazzi B, Kaminski PM, Wolin MS, Borgonjon DJ, Van Nassauw L, Haile A, Zviman M, Bedja D, Wuyts FL, Elsaesser RS, Cos P, Gabrielson KL, Lazzarino G, Paolocci N, Timmermans JP, Vrints CJ, Kass DA: High-dose folic acid pretreatment blunts cardiac dysfunction during ischemia coupled to maintenance of high-energy phosphates and reduces postreperfusion injury. Circulation 2008; 117:1810-9
34. Sack MN, Murphy E, Schulz R: The regulation and control of mitochondrial homeostasis in changing cardiac tolerance to ischemia-reperfusion injury: A focused issue. Basic Res Cardiol 2009; 104:111-2
35. Jamnicki-Abegg M, Weihrauch D, Pagel PS, Kersten JR, Bosnjak ZJ, Warltier DC, Bienengraeber MW: Isoflurane inhibits cardiac myocyte apoptosis during oxidative and inflammatory stress by activating Akt and enhancing Bcl-2 expression. Anesthesiolog y 2005; 103:1006-14
36. Vigneron F, Dos Santos P, Lemoine S, Bonnet M, Tariosse L, Couffinhal T, Duplau C, Jaspard-Vinassa B: GSK-3β at the crossroads in the signalling of heart preconditioning: Implication of mTOR and Wnt pathways. Cardiovasc Res 2011; 90:49-56
37. Sussman MA, Vlkers M, Fischer K, Bailey B, Cottage CT, Din S, Gude N, Avitabile D, Alvarez R, Sundararaman B, Quijada P, Mason M, Konstandin MH, Malhowski A, Cheng Z, Khan M, McGregor M: Myocardial AKT: The omnipresent nexus. Physiol Rev 2011; 91:1023-70
38. H alestrap AP, Clarke SJ, Javadov SA: Mitochondrial permeability transition pore opening during myocardial reperfusion-A target for cardioprotection. Cardiovasc Res 2004; 61:372-85
39. Ge ZD, Pravdic D, Bienengraeber M, Pratt PF Jr, Auchampach JA, Gross GJ, Kersten JR, Warltier DC: Isoflurane postconditioning protects against reperfusion injury by preventing mitochondrial permeability transition by an endothelial nitric oxide synthase-dependent mechanism. Anesthesiolog y 2010; 112:73-85
40. Heusch G, Boengler K, Schulz R: Cardioprotection: Nitric oxide, protein kinases, and mitochondria. Circulation 2008; 118:1915-9