MicroRNA-451 exacerbates lipotoxicity in cardiac myocytes and high-fat diet-induced cardiac hypertrophy in mice through suppression of the LKB1/AMPK pathway

Circulation Research

Volumn 116, Issue 2, 2015, Pages 279-288

  Kuwabara, Yasuhide ^a   Horie, Takahiro ^a   Baba, Osamu ^a   Watanabe, Shin ^a   Nishiga, Masataka ^a   Usami, Shunsuke ^a   Izuhara, Masayasu ^a   Nakao, Tetsushi ^a   Nishino, Tomohiro ^a   Otsu, Kinya ^b   Kita, Toru ^c   Kimura, Takeshi ^a   Ono, Koh ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c KOBE CITY MEDICAL CENTER GENERAL HOSPITAL   (Japan)

Author keywords

AMP activated protein kinase; cardiomegaly; microRNAs; type 2 diabetes mellitus

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM BINDING PROTEIN 39; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MICRORNA 451; PALMITIC ACID; PROTEIN KINASE LKB1; REACTIVE OXYGEN METABOLITE; SATURATED FATTY ACID; UNCLASSIFIED DRUG; MIRN451 MICRORNA, MOUSE; PROTEIN SERINE THREONINE KINASE; STK11 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; GENE EXPRESSION; GENE INACTIVATION; HEART CONTRACTION; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; IN VIVO STUDY; LIPID DIET; LIPOTOXICITY; MICROARRAY ANALYSIS; MOLECULAR BIOLOGY; MOUSE; NEWBORN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CARDIOMEGALY; CELL CULTURE; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TRANSGENIC MOUSE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, NEWBORN; CARDIOMEGALY; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICRORNAS; MYOCYTES, CARDIAC; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84922104763     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.304707     Document Type: Article

References (40)

1. Sharma S, Adrogue JV, Golfman L, Uray I, Lemm J, Youker K, Noon GP, Frazier OH, Taegtmeyer H. Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. FASEB J. 2004;18:1692-1700.
2. Szczepaniak LS, Dobbins RL, Metzger GJ, Sartoni-D'Ambrosia G, Arbique D, Vongpatanasin W, Unger R, Victor RG. Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magn Reson Med. 2003;49:417-423.
3. Ghosh S, Rodrigues B. Cardiac cell death in early diabetes and its modulation by dietary fatty acids. Biochim Biophys Acta. 2006;1761:1148-1162.
4. Wende AR, Abel ED. Lipotoxicity in the heart. Biochim Biophys Acta. 2010;1801:311-319.
5. Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 2011;25:1895-1908.
6. Boudeau J, Baas AF, Deak M, Morrice NA, Kieloch A, Schutkowski M, Prescott AR, Clevers HC, Alessi DR. MO25alpha/beta interact with STRADalpha/beta enhancing their ability to bind, activate and localize LKB1 in the cytoplasm. EMBO J. 2003;22:5102-5114.
7. Ko HJ, Zhang Z, Jung DY, Jun JY, Ma Z, Jones KE, Chan SY, Kim JK. Nutrient stress activates inflammation and reduces glucose metabolism by suppressing AMP-activated protein kinase in the heart. Diabetes. 2009;58:2536-2546.
8. Noyan-Ashraf MH, Shikatani EA, Schuiki I, Mukovozov I, Wu J, Li RK, Volchuk A, Robinson LA, Billia F, Drucker DJ, Husain M. A glucagonlike peptide-1 analog reverses the molecular pathology and cardiac dysfunction of a mouse model of obesity. Circulation. 2013;127:74-85.
9. Katare R, Caporali A, Zentilin L, Avolio E, Sala-Newby G, Oikawa A, Cesselli D, Beltrami AP, Giacca M, Emanueli C, Madeddu P. Intravenous gene therapy with PIM-1 via a cardiotropic viral vector halts the progression of diabetic cardiomyopathy through promotion of prosurvival signaling. Circ Res. 2011;108:1238-1251.
10. Shen E, Diao X, Wang X, Chen R, Hu B. MicroRNAs involved in the mitogen-activated protein kinase cascades pathway during glucose-induced cardiomyocyte hypertrophy. Am J Pathol. 2011;179:639-650.
11. Wang N, Yang C, Xie F, Sun L, Su X, Wang Y, Wei R, Zhang R, Li X, Yang B, Ai J. Gadd45?: a novel diabetes-associated gene potentially linking diabetic cardiomyopathy and baroreflex dysfunction. PLoS One. 2012;7:e49077.
12. Takanabe R, Ono K, Abe Y, Takaya T, Horie T, Wada H, Kita T, Satoh N, Shimatsu A, Hasegawa K. Up-regulated expression of microRNA-143 in association with obesity in adipose tissue of mice fed high-fat diet. Biochem Biophys Res Commun. 2008;376:728-732.
13. Calligaris SD, Lecanda M, Solis F, Ezquer M, Gutiérrez J, Brandan E, Leiva A, Sobrevia L, Conget P. Mice long-term high-fat diet feeding recapitulates human cardiovascular alterations: an animal model to study the early phases of diabetic cardiomyopathy. PLoS One. 2013;8:e60931.
14. Rasmussen KD, Simmini S, Abreu-Goodger C, Bartonicek N, Di Giacomo M, Bilbao-Cortes D, Horos R, Von Lindern M, Enright AJ, O'Carroll D. The miR-144/451 locus is required for erythroid homeostasis. J Exp Med. 2010;207:1351-1358.
15. Patrick DM, Zhang CC, Tao Y, Yao H, Qi X, Schwartz RJ, Jun-Shen Huang L, Olson EN. Defective erythroid differentiation in miR-451 mutant mice mediated by 14-3-3zeta. Genes Dev. 2010;24:1614-1619.
16. Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, Wolfe SA, Giraldez AJ. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science. 2010;328:1694-1698.
17. Hattori F, Chen H, Yamashita H, et al. Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods. 2010;7:61-66.
18. Chen H, Untiveros GM, McKee LA, Perez J, Li J, Antin PB, Konhilas JP. Micro-RNA-195 and-451 regulate the LKB1/AMPK signaling axis by targeting MO25. PLoS One. 2012;7:e41574.
19. Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, Kako Y, Seo T, Hu Y, Lutz EP, Merkel M, Bensadoun A, Homma S, Goldberg IJ. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest. 2003;111:419-426.
20. Duncan JG, Bharadwaj KG, Fong JL, Mitra R, Sambandam N, Courtois MR, Lavine KJ, Goldberg IJ, Kelly DP. Rescue of cardiomyopathy in peroxisome proliferator-activated receptor-alpha transgenic mice by deletion of lipoprotein lipase identifies sources of cardiac lipids and peroxisome proliferator-activated receptor-alpha activators. Circulation. 2010;121:426-435.
21. Bandres E, Bitarte N, Arias F, Agorreta J, Fortes P, Agirre X, Zarate R, Diaz-Gonzalez JA, Ramirez N, Sola JJ, Jimenez P, Rodriguez J, Garcia-Foncillas J. microRNA-451 regulates macrophage migration inhibitory factor production and proliferation of gastrointestinal cancer cells. Clin Cancer Res. 2009;15:2281-2290.
22. Godlewski J, Nowicki MO, Bronisz A, Nuovo G, Palatini J, De Lay M, Van Brocklyn J, Ostrowski MC, Chiocca EA, Lawler SE. MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells. Mol Cell. 2010;37:620-632.
23. Wang X, Zhu H, Zhang X, Liu Y, Chen J, Medvedovic M, Li H, Weiss MJ, Ren X, Fan GC. Loss of the miR-144/451 cluster impairs ischaemic preconditioning-mediated cardioprotection by targeting Rac-1. Cardiovasc Res. 2012;94:379-390.
24. Miller EJ, Li J, Leng L, McDonald C, Atsumi T, Bucala R, Young LH. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature. 2008;451:578-582.
25. Zhang X, Wang X, Zhu H, Zhu C, Wang Y, Pu WT, Jegga AG, Fan GC. Synergistic effects of the GATA-4-mediated miR-144/451 cluster in protection against simulated ischemia/reperfusion-induced cardiomyocyte death. J Mol Cell Cardiol. 2010;49:841-850.
26. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008;30:214-226.
27. Goldberg IJ, Trent CM, Schulze PC. Lipid metabolism and toxicity in the heart. Cell Metab. 2012;15:805-812.
28. Toyokuni S, Miyake N, Hiai H, Hagiwara M, Kawakishi S, Osawa T, Uchida K. The monoclonal antibody specific for the 4-hydroxy-2-nonenal histidine adduct. FEBS Lett. 1995;359:189-191.
29. Lu H, Buchan RJ, Cook SA. MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc Res. 2010;86:410-420.
30. Hickson-Bick DL, Sparagna GC, Buja LM, McMillin JB. Palmitateinduced apoptosis in neonatal cardiomyocytes is not dependent on the generation of ROS. Am J Physiol Heart Circ Physiol. 2002;282:H656-H664.
31. de Aguiar Vallim TQ, Tarling EJ, Kim T, Civelek M, Baldán Á, Esau C, Edwards PA. MicroRNA-144 regulates hepatic ATP binding cassette transporter A1 and plasma high-density lipoprotein after activation of the nuclear receptor farnesoid X receptor. Circ Res. 2013;112:1602-1612.
32. Rafter JJ, Child P, Anderson AM, Alder R, Eng V, Bruce WR. Cellular toxicity of fecal water depends on diet. Am J Clin Nutr. 1987;45:559-563.
33. Yoshimoto S, Loo TM, Atarashi K, Kanda H, Sato S, Oyadomari S, Iwakura Y, Oshima K, Morita H, Hattori M, Hattori M, Honda K, Ishikawa Y, Hara E, Ohtani N. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature. 2013;499:97-101.
34. Eguchi K, Boden-Albala B, Jin Z, Rundek T, Sacco RL, Homma S, Di Tullio MR. Association between diabetes mellitus and left ventricular hypertrophy in a multiethnic population. Am J Cardiol. 2008;101:1787-1791.
35. Turdi S, Kandadi MR, Zhao J, Huff AF, Du M, Ren J. Deficiency in AMPactivated protein kinase exaggerates high fat diet-induced cardiac hypertrophy and contractile dysfunction. J Mol Cell Cardiol. 2011;50:712-722.
36. Ikeda Y, Sato K, Pimentel DR, Sam F, Shaw RJ, Dyck JR, Walsh K. Cardiac-specific deletion of LKB1 leads to hypertrophy and dysfunction. J Biol Chem. 2009;284:35839-35849.
37. Lizcano JM, Göransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Mäkelä TP, Hardie DG, Alessi DR. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 2004;23:833-843.
38. Dugan LL, You YH, Ali SS, et al. AMPK dysregulation promotes diabetesrelated reduction of superoxide and mitochondrial function. J Clin Invest. 2013;123:4888-4899.
39. Hultqvist M, Olsson LM, Gelderman KA, Holmdahl R. The protective role of ROS in autoimmune disease. Trends Immunol. 2009;30:201-208.
40. Kim Y, Roh S, Lawler S, Friedman A. miR451 and AMPK mutual antagonism in glioma cell migration and proliferation: a mathematical model. PLoS One. 2011;6:e28293.