Exercise prevents cardiac injury and improves mitochondrial biogenesis in advanced diabetic cardiomyopathy with PGC-1α and Akt activation

Cellular Physiology and Biochemistry

Volumn 35, Issue 6, 2015, Pages 2159-2168

  Wang, Hui ^a   Bei, Yihua ^b   Lu, Yan ^a   Sun, Wei ^a   Liu, Qi ^c   Wang, Yalong ^b   Cao, Yujie ^b   Chen, Ping ^b   Xiao, Junjie ^b   Kong, Xiangqing ^a  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b SHANGHAI UNIVERSITY   (China)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Akt; Diabetic cardiomyopathy; Exercise; Mitochondria; PGC 1

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 3; MESSENGER RNA; MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; SINGLE STRANDED DNA BINDING PROTEIN; PPARGC1A PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ADVANCED DIABETIC CARDIOMYOPATHY; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOGENESIS; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; DNA TRANSCRIPTION; DOWN REGULATION; EVALUATION STUDY; EXERCISE; HEART CONTRACTION; HEART EJECTION FRACTION; HEART FUNCTION; HEART INJURY; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART PROTECTION; MALE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SEDENTARY LIFESTYLE; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL EXPERIMENT; C57BL MOUSE; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; GENETICS; HEART; METABOLISM; MITOCHONDRION; ORGANELLE BIOGENESIS; PATHOPHYSIOLOGY; PHYSIOLOGY;

MUS;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; COLLAGEN TYPE I; COLLAGEN TYPE III; DIABETIC CARDIOMYOPATHIES; DNA, MITOCHONDRIAL; HEART; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MYOCARDIUM; MYOCYTES, CARDIAC; ORGANELLE BIOGENESIS; PHYSICAL CONDITIONING, ANIMAL; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84928151786     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000374021     Document Type: Article

References (45)

1. Chavali V, Tyagi SC, Mishra PK: Predictors and prevention of diabetic cardiomyopathy. Diabetes Metab Syndr Obes Targets Ther 2013;6:151-160.
2. Huynh K, Bernardo BC, McMullen JR, Ritchie RH: Diabetic cardiomyopathy: Mechanisms and new treatment strategies targeting antioxidant signaling pathways. Pharmacol Ther 2014;142:375-415.
3. Boudina S, Sena S, O'Neill BT, Tathireddy P, Young ME, Abel ED: Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 2005;112:2686-2695.
4. Iliadis F, Kadoglou N, Didangelos T: Insulin and the heart. Diabetes Res Clin Pract 2011;93 Suppl 1:S86-91.
5. Finck BN, Kelly DP: Peroxisome proliferator-activated receptor gamma coactivator-1 (PGC-1) regulatory cascade in cardiac physiology and disease. Circulation 2007;115:2540-2548.
6. Rowe GC, Jiang A, Arany Z: PGC-1 coactivators in cardiac development and disease. Circ Res 2010;107:825-838.
7. Aksnes TA, Kjeldsen SE, Rostrup M, Omvik P, Hua TA, Julius S: Impact of new-onset diabetes mellitus on cardiac outcomes in the Valsartan Antihypertensive Long-term Use Evaluation (VALUE) trial population. Hypertension 2007;50:467-473.
8. Cohen-Solal A, Beauvais F, Logeart D: Heart failure and diabetes mellitus: epidemiology and management of an alarming association. J Card Fail 2008;14:615-625.
9. Ellison GM, Waring CD, Vicinanza C, Torella D: Physiological cardiac remodelling in response to endurance exercise training: cellular and molecular mechanisms. Heart Br Card Soc 2012;98:5-10.
10. Tabet JY, Meurin P, Driss AB, Weber H, Renaud N, Grosdemouge A, Beauvais F, Cohen-Solal A: Benefits of exercise training in chronic heart failure. Arch Cardiovasc Dis 2009;102:721-730.
11. Mann N, Rosenzweig A: Can exercise teach us how to treat heart disease? Circulation 2012;126:2625-2635.
12. De Angelis KL, Oliveira AR, Dall'Ago P, Peixoto LR, Gadonski G, Lacchini S, Fernandes TG, Irigoyen MC: Effects of exercise training on autonomic and myocardial dysfunction in streptozotocin-diabetic rats. Braz J Med Biol Res Rev Bras Pesqui Médicas E Biológicas Soc Bras Biofísica Al 2000;33:635-641.
13. Bidasee KR, Zheng H, Shao C-H, Parbhu SK, Rozanski GJ, Patel KP: Exercise training initiated after the onset of diabetes preserves myocardial function: effects on expression of beta-adrenoceptors. J Appl Physiol Bethesda Md 1985 2008;105:907-914.
14. Li S, Culver B, Ren J: Benefit and risk of exercise on myocardial function in diabetes. Pharmacol Res Off J Ital Pharmacol Soc 2003;48:127-132.
15. Loganathan R, Novikova L, Boulatnikov IG, Smirnova IV: Exercise-induced cardiac performance in autoimmune (type 1) diabetes is associated with a decrease in myocardial diacylglycerol. J Appl Physiol Bethesda Md 1985 2012;113:817-826.
16. Castellar A, Remedio RN, Barbosa RA, Gomes RJ, Caetano FH: Collagen and reticular fibers in left ventricular muscle in diabetic rats: physical exercise prevents its changes? Tissue Cell 2011;43:24-28.
17. Epp RA, Susser SE, Morissette MP, Kehler DS, Jassal DS, Duhamel TA: Exercise training prevents the development of cardiac dysfunction in the low-dose streptozotocin diabetic rats fed a high-fat diet. Can J Physiol Pharmacol 2013;91:80-89.
18. Hafstad AD, Lund J, Hadler-Olsen E, Höper AC, Larsen TS, Aasum E: High- and moderate-intensity training normalizes ventricular function and mechanoenergetics in mice with diet-induced obesity. Diabetes 2013;62:2287-2294.
19. Korte FS, Mokelke EA, Sturek M, McDonald KS: Exercise improves impaired ventricular function and alterations of cardiac myofibrillar proteins in diabetic dyslipidemic pigs. J Appl Physiol Bethesda Md 1985 2005;98:461-467.
20. Loganathan R, Bilgen M, Al-Hafez B, Zhero SV, Alenezy MD, Smirnova IV: Exercise training improves cardiac performance in diabetes: in vivo demonstration with quantitative cine-MRI analyses. J Appl Physiol Bethesda Md 1985 2007;102:665-672.
21. Saraceni C, Broderick TL: Cardiac and metabolic consequences of aerobic exercise training in experimental diabetes. Curr Diabetes Rev 2007;3:75-84.
22. Searls YM, Smirnova IV, Fegley BR, Stehno-Bittel L: Exercise attenuates diabetes-induced ultrastructural changes in rat cardiac tissue. Med Sci Sports Exerc 2004;36:1863-1870.
23. Silva E, Natali AJ, Silva MF, Gomes GJ, Cunha DNQ, Ramos RM, Toledo MM, Drummond FR, Belfort FG, Novaes RD, Maldonado IR: Ventricular remodeling in growing rats with experimental diabetes: The impact of swimming training. Pathol Res Pract 2013;209:618-626.
24. Mandavia CH, Aroor AR, Demarco VG, Sowers JR: Molecular and metabolic mechanisms of cardiac dysfunction in diabetes. Life Sci 2013;92:601-608.
25. Zhang X, Chen C: A new insight of mechanisms, diagnosis and treatment of diabetic cardiomyopathy. Endocrine 2012;41:398-409.
26. Bernardo BC, Weeks KL, Pretorius L, McMullen JR: Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol Ther 2010;128:191-227.
27. Kwak H-B, Kim J, Joshi K, Yeh A, Martinez DA, Lawler JM: Exercise training reduces fibrosis and matrix metalloproteinase dysregulation in the aging rat heart. FASEB J Off Publ Fed Am Soc Exp Biol 2011;25:1106-1117.
28. Kwak H-B: Effects of aging and exercise training on apoptosis in the heart. J Exerc Rehabil 2013;9:212-219.
29. Ren J, Pulakat L, Whaley-Connell A, Sowers JR: Mitochondrial biogenesis in the metabolic syndrome and cardiovascular disease. J Mol Med Berl Ger 2010;88:993-1001.
30. Russell LK, Mansfield CM, Lehman JJ, Kovacs A, Courtois M, Saffitz JE, Medeiros DM, Valencik ML, McDonald JA, Kelly DP: Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ Res 2004;94:525-533.
31. Sebastiani M, Giordano C, Nediani C, Travaglini C, Borchi E, Zani M, Feccia M, Mancini M, Petrozza V, Cossarizza A, Gallo P, Taylor RW, d'Amati G: Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. J Am Coll Cardiol 2007;50:1362-1369.
32. Leone TC, Lehman JJ, Finck BN, Schaeffer PJ, Wende AR, Boudina S, Courtois M, Wozniak DF, Sambandam N, Bernal-Mizrachi C, Chen Z, Holloszy JO, Medeiros DM, Schmidt RE, Saffitz JE, Abel ED, Semenkovich CF, Kelly DP: PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol 2005;3:e101.
33. Watson PA, Reusch JEB, McCune SA, Leinwand LA, Luckey SW, Konhilas JP, Brown DA, Chicco AJ, Sparagna GC, Long CS, Moore RL: Restoration of CREB function is linked to completion and stabilization of adaptive cardiac hypertrophy in response to exercise. Am J Physiol Heart Circ Physiol 2007;293:H246-259.
34. Arany Z, Novikov M, Chin S, Ma Y, Rosenzweig A, Spiegelman BM: Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc Natl Acad Sci U S A 2006;103:10086-10091.
35. Sihag S, Cresci S, Li AY, Sucharov CC, Lehman JJ: PGC-1α and ERRα target gene downregulation is a signature of the failing human heart. J Mol Cell Cardiol 2009;46:201-212.
36. Ventura-Clapier R, Garnier A, Veksler V: Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res 2008;79:208-217.
37. Anderson R, Prolla T: PGC-1alpha in aging and anti-aging interventions. Biochim Biophys Acta 2009 Oct;1790:1059-1066.
38. Botta A, Laher I, Beam J, Decoffe D, Brown K, Halder S, Devlin A, Gibson DL, Ghosh S: Short term exercise induces PGC-1α, ameliorates inflammation and increases mitochondrial membrane proteins but fails to increase respiratory enzymes in aging diabetic hearts. PloS One 2013;8:e70248.
39. Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX, Aziz S, Johnson JI, Bugger H, Zaha VG, Abel ED: Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 2007;56:2457-2466.
40. Pohjoismäki JLO, Boettger T, Liu Z, Goffart S, Szibor M, Braun T: Oxidative stress during mitochondrial biogenesis compromises mtDNA integrity in growing hearts and induces a global DNA repair response. Nucleic Acids Res 2012;40:6595-6607.
41. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP: Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 2000;106:847-856.
42. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, Muslin AJ: Akt1 is required for physiological cardiac growth. Circulation 2006;113:2097-2104.
43. Shiraishi I, Melendez J, Ahn Y, Skavdahl M, Murphy E, Welch S, Schaefer E, Walsh K, Rosenzweig A, Torella D, Nurzynska D, Kajstura J, Leri A, Anversa P, Sussman MA: Nuclear targeting of Akt enhances kinase activity and survival of cardiomyocytes. Circ Res 2004;94:884-891.
44. Kitagishi Y, Nakanishi A, Minami A, Asai Y, Yasui M, Iwaizako A, Suzuki M, Ono Y, Ogura Y, Matsuda S: Certain Diet and Lifestyle May Contribute to Islet β-cells Protection in Type-2 Diabetes via the Modulation of Cellular PI3K/AKT Pathway. Open Biochem J 2014;8:74-82.
45. Pulakat L, Aroor AR, Gul R, Sowers JR: Cardiac insulin resistance and microRNA modulators. Exp Diabetes Res 2012;2012:654904.