Upregulation of MG53 induces diabetic cardiomyopathy through transcriptional activation of peroxisome proliferation-activated receptor α

Circulation

Volumn 131, Issue 9, 2015, Pages 795-804

  Liu, Fenghua ^a,b   Song, Ruisheng ^a,b,c   Feng, Yuanqing ^a,b   Guo, Jiaojiao ^a,b   Chen, Yanmin ^a,b   Zhang, Yong ^a,b   Chen, Tao ^a   Wang, Yanru ^a,b   Huang, Yanyi ^a   Li, Chuan Yun ^a   Cao, Chunmei ^a,b   Zhang, Yan ^a,b   Hu, Xinli ^a,b   Xiao, Rui Ping ^a,b  

^a PEKING UNIVERSITY   (China)

^b Peking University   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Diabetic cardiomyopathies; Insulin resistance; MG53 protein, mouse; Peroxisome proliferation activated receptors

Indexed keywords

INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; LIGASE; MITSUGUMIN 53; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; UNCLASSIFIED DRUG; CARRIER PROTEIN; HYBRID PROTEIN; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, MOUSE; MESSENGER RNA; MG53 PROTEIN, MOUSE; MYOSIN HEAVY CHAIN; SMALL INTERFERING RNA; SYNTHETIC DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; DYSLIPIDEMIA; GLUCOSE TRANSPORT; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HYPERGLYCEMIA; IN VIVO STUDY; INSULIN RESISTANCE; LIPID METABOLISM; LIPID STORAGE; MALE; METABOLIC DISORDER; METABOLIC SYNDROME X; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; GENETIC TRANSCRIPTION; GENETICS; HEART MUSCLE CELL; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; DIABETIC CARDIOMYOPATHIES; GENES, SYNTHETIC; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYOCYTES, CARDIAC; MYOSIN HEAVY CHAINS; PPAR ALPHA; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84928754600     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.114.012285     Document Type: Article

References (47)

1. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27:1047-1053.
2. Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Branwood AW, Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol. 1972;30:595-602.
3. Kannel WB, Hjortland M, Castelli WP. Role of diabetes in congestive heart failure: the Framingham study. Am J Cardiol. 1974;34:29-34.
4. Kannel WB, McGee DL. Diabetes and cardiovascular risk factors: the Framingham study. Circulation. 1979;59:8-13.
5. Kannel WB, McGee DL. Diabetes and glucose tolerance as risk factors for cardiovascular disease: the Framingham study. Diabetes Care. 1979;2:120-126.
6. Devereux RB, Roman MJ, Paranicas M, O'Grady MJ, Lee ET, Welty TK, Fabsitz RR, Robbins D, Rhoades ER, Howard BV. Impact of diabetes on cardiac structure and function: the strong heart study. Circulation. 2000;101:2271-2276.
7. Kannel WB, McGee DL. Diabetes and cardiovascular disease: the Framingham study. JAMA. 1979;241:2035-2038.
8. Semeniuk LM, Kryski AJ, Severson DL. Echocardiographic assessment of cardiac function in diabetic db/db and transgenic db/db-hGLUT4 mice. Am J Physiol Heart Circ Physiol. 2002;283:H976-H982. doi: 10.1152/ajpheart.00088.2002.
9. Battiprolu PK, Hojayev B, Jiang N, Wang ZV, Luo X, Iglewski M, Shelton JM, Gerard RD, Rothermel BA, Gillette TG, Lavandero S, Hill JA. Metabolic stress-induced activation of FoxO1 triggers diabetic cardiomyopathy in mice. J Clin Invest. 2012;122:1109-1118. doi: 10.1172/JCI60329.
10. Carley AN, Semeniuk LM, Shimoni Y, Aasum E, Larsen TS, Berger JP, Severson DL. Treatment of type 2 diabetic db/db mice with a novel PPARgamma agonist improves cardiac metabolism but not contractile function. Am J Physiol Endocrinol Metab. 2004;286:E449-E455. doi: 10.1152/ajpendo.00329.2003.
11. Ouwens DM, Boer C, Fodor M, de Galan P, Heine RJ, Maassen JA, Diamant M. Cardiac dysfunction induced by high-fat diet is associated with altered myocardial insulin signalling in rats. Diabetologia. 2005;48:1229-1237. doi: 10.1007/s00125-005-1755-x.
12. Song R, Peng W, Zhang Y, Lv F, Wu HK, Guo J, Cao Y, Pi Y, Zhang X, Jin L, Zhang M, Jiang P, Liu F, Meng S, Zhang X, Jiang P, Cao CM, Xiao RP. Central role of E3 ubiquitin ligase MG53 in insulin resistance and metabolic disorders. Nature. 2013;494:375-379. doi: 10.1038/nature11834.
13. Yi JS, Park JS, Ham YM, Nguyen N, Lee NR, Hong J, Kim BW, Lee H, Lee CS, Jeong BC, Song HK, Cho H, Kim YK, Lee JS, Park KS, Shin H, Choi I, Lee SH, Park WJ, Park SY, Choi CS, Lin P, Karunasiri M, Tan T, Duann P, Zhu H, Ma J, Ko YG. MG53-induced IRS-1 ubiquitination negatively regulates skeletal myogenesis and insulin signalling. Nat Commun. 2013;4:2354. doi: 10.1038/ncomms3354.
14. Cai C, Masumiya H, Weisleder N, Matsuda N, Nishi M, Hwang M, Ko JK, Lin P, Thornton A, Zhao X, Pan Z, Komazaki S, Brotto M, Takeshima H, Ma J. MG53 nucleates assembly of cell membrane repair machinery. Nat Cell Biol. 2009;11:56-64. doi: 10.1038/ncb1812.
15. Wang X, Xie W, Zhang Y, Lin P, Han L, Han P, Wang Y, Chen Z, Ji G, Zheng M, Weisleder N, Xiao RP, Takeshima H, Ma J, Cheng H. Cardioprotection of ischemia/reperfusion injury by cholesterol-dependent MG53-mediated membrane repair. Circ Res. 2010;107:76-83. doi: 10.1161/CIRCRESAHA.109.215822.
16. Cao CM, Zhang Y, Weisleder N, Ferrante C, Wang X, Lv F, Zhang Y, Song R, Hwang M, Jin L, Guo J, Peng W, Li G, Nishi M, Takeshima H, Ma J, Xiao RP. MG53 constitutes a primary determinant of cardiac ischemic preconditioning. Circulation. 2010;121:2565-2574. doi: 10.1161/CIRCULATIONAHA.110.954628.
17. Zhang Y, Lv F, Jin L, Peng W, Song R, Ma J, Cao CM, Xiao RP. MG53 participates in ischaemic postconditioning through the RISK signalling pathway. Cardiovasc Res. 2011;91:108-115. doi: 10.1093/cvr/cvr029.
18. Freudiger CW, Min W, Saar BG, Lu S, Holtom GR, He C, Tsai JC, Kang JX, Xie XS. Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy. Science. 2008;322:1857-1861. doi: 10.1126/science.1165758.
19. Yu Z, Chen T, Zhang X, Fu D, Liao X, Shen J, Liu X, Zhang B, Xie XS, Su X-D, Chen J, Huang Y. Label-free chemical imaging in vivo: three-dimensional non-invasive microscopic observation of amphioxus notochord through stimulated Raman scattering (SRS). Chemical Science. 2012;3:2646-2654.
20. Moyers JS, Bilan PJ, Reynet C, Kahn CR. Overexpression of Rad inhibits glucose uptake in cultured muscle and fat cells. J Biol Chem. 1996;271:23111-23116.
21. Zhang SJ, Liu CJ, Yu P, Zhong X, Chen JY, Yang X, Peng J, Yan S, Wang C, Zhu X, Xiong J, Zhang YE, Tan BC, Li CY. Evolutionary interrogation of human biology in well-annotated genomic framework of rhesus macaque. Mol Biol Evol. 2014;31:1309-1324. doi: 10.1093/molbev/msu084.
22. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57. doi: 10.1038/nprot.2008.211.
23. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1-13.
24. Lee CS, Yi JS, Jung SY, Kim BW, Lee NR, Choo HJ, Jang SY, Han J, Chi SG, Park M, Lee JH, Ko YG. TRIM72 negatively regulates myogenesis via targeting insulin receptor substrate-1. Cell Death Differ. 2010;17:1254-1265. doi: 10.1038/cdd.2010.1.
25. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature. 1995;378:785-789. doi: 10.1038/378785a0.
26. Kohn AD, Kovacina KS, Roth RA. Insulin stimulates the kinase activity of RAC-PK, a pleckstrin homology domain containing ser/thr kinase. EMBO J. 1995;14:4288-4295.
27. Gertz EW, Wisneski JA, Stanley WC, Neese RA. Myocardial substrate utilization during exercise in humans: dual carbon-labeled carbohydrate isotope experiments. J Clin Invest. 1988;82:2017-2025. doi: 10.1172/JCI113822.
28. Saddik M, Lopaschuk GD. Myocardial triglyceride turnover and contribution to energy substrate utilization in isolated working rat hearts. J Biol Chem. 1991;266:8162-8170.
29. Razeghi P, Young ME, Cockrill TC, Frazier OH, Taegtmeyer H. Downregulation of myocardial myocyte enhancer factor 2C and myocyte enhancer factor 2C-regulated gene expression in diabetic patients with nonischemic heart failure. Circulation. 2002;106:407-411.
30. Young ME, Guthrie PH, Razeghi P, Leighton B, Abbasi S, Patil S, Youker KA, Taegtmeyer H. Impaired long-chain fatty acid oxidation and contractile dysfunction in the obese Zucker rat heart. Diabetes. 2002;51:2587-2595.
31. Buchanan J, Mazumder PK, Hu P, Chakrabarti G, Roberts MW, Yun UJ, Cooksey RC, Litwin SE, Abel ED. Reduced cardiac efficiency and altered substrate metabolism precedes the onset of hyperglycemia and contractile dysfunction in two mouse models of insulin resistance and obesity. Endocrinology. 2005;146:5341-5349. doi: 10.1210/en.2005-0938.
32. How OJ, Aasum E, Severson DL, Chan WY, Essop MF, Larsen TS. Increased myocardial oxygen consumption reduces cardiac efficiency in diabetic mice. Diabetes. 2006;55:466-473.
33. Djouadi F, Weinheimer CJ, Saffitz JE, Pitchford C, Bastin J, Gonzalez FJ, Kelly DP. A gender-related defect in lipid metabolism and glucose homeostasis in peroxisome proliferator-activated receptor alpha-deficient mice. J Clin Invest. 1998;102:1083-1091. doi: 10.1172/JCI3949.
34. Finck BN, Lehman JJ, Leone TC, Welch MJ, Bennett MJ, Kovacs A, Han X, Gross RW, Kozak R, Lopaschuk GD, Kelly DP. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J Clin Invest. 2002;109:121-130. doi: 10.1172/JCI14080.
35. Zhang X, Zhang R, Raab S, Zheng W, Wang J, Liu N, Zhu T, Xue L, Song Z, Mao J, Li K, Zhang H, Zhang Y, Han C, Ding Y, Wang H, Hou N, Liu Y, Shang S, Li C, Sebokova E, Cheng H, Huang PL. Rhesus macaques develop metabolic syndrome with reversible vascular dysfunction responsive to pioglitazone. Circulation. 2011;124:77-86. doi: 10.1161/CIRCULATIONAHA.110.990333.
36. Shi Y, Downes M, Xie W, Kao HY, Ordentlich P, Tsai CC, Hon M, Evans RM. Sharp, an inducible cofactor that integrates nuclear receptor repression and activation. Genes Dev. 2001;15:1140-1151. doi: 10.1101/gad.871201.
37. Sorrentino D, Robinson RB, Kiang CL, Berk PD. At physiologic albumin/oleate concentrations oleate uptake by isolated hepatocytes, cardiac myocytes, and adipocytes is a saturable function of the unbound oleate concentration: uptake kinetics are consistent with the conventional theory. J Clin Invest. 1989;84:1325-1333. doi: 10.1172/JCI114301.
38. Coburn CT, Knapp FF Jr, Febbraio M, Beets AL, Silverstein RL, Abumrad NA. Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J Biol Chem. 2000;275:32523-32529. doi: 10.1074/jbc.M003826200.
39. Bugger H, Abel ED. Molecular mechanisms of diabetic cardiomyopathy. Diabetologia. 2014;57:660-671. doi: 10.1007/s00125-014-3171-6.
40. Nunoda S, Genda A, Sugihara N, Nakayama A, Mizuno S, Takeda R. Quantitative approach to the histopathology of the biopsied right ventricular myocardium in patients with diabetes mellitus. Heart Vessels. 1985;1:43-47.
41. Syrový I, Hodný Z. Non-enzymatic glycosylation of myosin: effects of diabetes and ageing. Gen Physiol Biophys. 1992;11:301-307.
42. Tsai WW, Wang Z, Yiu TT, Akdemir KC, Xia W, Winter S, Tsai CY, Shi X, Schwarzer D, Plunkett W, Aronow B, Gozani O, Fischle W, Hung MC, Patel DJ, Barton MC. TRIM24 links a non-canonical histone signature to breast cancer. Nature. 2010;468:927-932. doi: 10.1038/nature09542.
43. Zoumpoulidou G, Broceño C, Li H, Bird D, Thomas G, Mittnacht S. Role of the tripartite motif protein 27 in cancer development. J Natl Cancer Inst. 2012;104:941-952. doi: 10.1093/jnci/djs224.
44. Abrink M, Ortiz JA, Mark C, Sanchez C, Looman C, Hellman L, Chambon P, Losson R. Conserved interaction between distinct Krüppel-associated box domains and the transcriptional intermediary factor 1 beta. Proc Natl Acad Sci U S A. 2001;98:1422-1426. doi: 10.1073/pnas.041616998.
45. Ito K, Carracedo A, Weiss D, Arai F, Ala U, Avigan DE, Schafer ZT, Evans RM, Suda T, Lee CH, Pandolfi PP. A PML-PPAR-δ pathway for fatty acid oxidation regulates hematopoietic stem cell maintenance. Nat Med. 2012;18:1350-1358. doi: 10.1038/nm.2882.
46. Bell JL, Malyukova A, Kavallaris M, Marshall GM, Cheung BB. TRIM16 inhibits neuroblastoma cell proliferation through cell cycle regulation and dynamic nuclear localization. Cell Cycle. 2013;12:889-898. doi: 10.4161/cc.23825.
47. Yuan Z, Villagra A, Peng L, Coppola D, Glozak M, Sotomayor EM, Chen J, Lane WS, Seto E. The ATDC (TRIM29) protein binds p53 and antagonizes p53-mediated functions. Mol Cell Biol. 2010;30:3004-3015. doi: 10.1128/MCB.01023-09.