Enhanced skeletal muscle expression of extracellular superoxide dismutase mitigates streptozotocin-induced diabetic cardiomyopathy by reducing oxidative stress and aberrant cell signaling

Circulation: Heart Failure

Volumn 8, Issue 1, 2015, Pages 188-197

  Call, Jarrod A ^a,b   Chain, Kristopher H ^a,b   Martin, Kyle S ^c   Lira, Vitor A ^a,b   Okutsu, Mitsuharu ^a,b   Zhang, Mei ^a,b   Yan, Zhen ^a,b  

^a Department of Pharmacology Center for Skeletal Muscle Research   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c University of Virginia   (United States)

Author keywords

Antioxidants; Cardiomyocyte; Diabetic cardiomyopathies; Exercise; Hypertrophy; Oxidative stress

Indexed keywords

EXTRACELLULAR SUPEROXIDE DISMUTASE; STREPTOZOCIN; DNA; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CACHEXIA; CIRCULATION; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; ENZYME LOCALIZATION; EXERCISE; GENE OVEREXPRESSION; HEART; HEART DISEASE; HEART FUNCTION; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SOLEUS MUSCLE; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETICS; HEART MUSCLE CELL; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC CARDIOMYOPATHIES; DNA; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SKELETAL; MYOCYTES, CARDIAC; OXIDATIVE STRESS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84925021484     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.114.001540     Document Type: Article

References (50)

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. Hayat SA, Patel B, Khattar RS, Malik RA. Diabetic cardiomyopathy: mechanisms, diagnosis and treatment. Clin Sci (Lond). 2004;107:539-557. doi: 10.1042/CS20040057.
3. Role of cardiovascular risk factors in prevention and treatment of macrovascular disease in diabetes. American Diabetes Association. Diabetes Care. 1989;12:573-579.
4. 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.
5. Choi KM, Zhong Y, Hoit BD, Grupp IL, Hahn H, Dilly KW, Guatimosim S, Lederer WJ, Matlib MA. Defective intracellular Ca(2+) signaling contributes to cardiomyopathy in Type 1 diabetic rats. Am J Physiol Heart Circ Physiol. 2002;283:H1398-H1408. doi: 10.1152/ ajpheart.00313.2002.
6. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res. 2006;98:596-605. doi: 10.1161/01.RES.0000207406.94146.c2.
7. Shimizu M, Umeda K, Sugihara N, Yoshio H, Ino H, Takeda R, Okada Y, Nakanishi I. Collagen remodelling in myocardia of patients with diabetes. J Clin Pathol. 1993;46:32-36.
8. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes. 1991;40:405-412.
9. Maritim AC, Sanders RA, Watkins JB III. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol. 2003;17:24-38. doi: 10.1002/jbt.10058.
10. Giugliano D, Ceriello A, Paolisso G. Oxidative stress and diabetic vascular complications. Diabetes Care. 1996;19:257-267.
11. Cai L, Kang YJ. Oxidative stress and diabetic cardiomyopathy: a brief review. Cardiovasc Toxicol. 2001;1:181-193.
12. Westermann D, Rutschow S, Van Linthout S, Linderer A, Bücker-Gärtner C, Sobirey M, Riad A, Pauschinger M, Schultheiss HP, Tschöpe C. Inhibition of p38 mitogen-activated protein kinase attenuates left ventricular dysfunction by mediating pro-inflammatory cardiac cytokine levels in a mouse model of diabetes mellitus. Diabetologia. 2006;49:2507-2513. doi: 10.1007/s00125-006-0385-2.
13. Turkseven S, Kruger A, Mingone CJ, Kaminski P, Inaba M, Rodella LF, Ikehara S, Wolin MS, Abraham NG. Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol. 2005;289:H701-H707. doi: 10.1152/ajpheart.00024.2005.
14. Hamblin M, Smith HM, Hill MF. Dietary supplementation with vitamin E ameliorates cardiac failure in type I diabetic cardiomyopathy by suppressing myocardial generation of 8-iso-prostaglandin F2alpha and oxidized glutathione. J Card Fail. 2007;13:884-892. doi: 10.1016/j. cardfail.2007.07.002.
15. Shen X, Zheng S, Metreveli NS, Epstein PN. Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes. 2006;55:798-805.
16. Flaherty JT, Pitt B, Gruber JW, Heuser RR, Rothbaum DA, Burwell LR, George BS, Kereiakes DJ, Deitchman D, Gustafson N. Recombinant human superoxide dismutase (h-SOD) fails to improve recovery of ventricular function in patients undergoing coronary angioplasty for acute myocardial infarction. Circulation. 1994;89:1982-1991.
17. Celik T, Yuksel C, Iyisoy A. Alpha tocopherol use in the management of diabetic cardiomyopathy: lessons learned from randomized clinical trials. J Diabetes Complications. 2010;24:286-288. doi: 10.1016/j. jdiacomp.2009.02.005.
18. Wang X, Jian C, Zhang X, Huang Z, Xu J, Hou T, Shang W, Ding Y, Zhang W, Ouyang M, Wang Y, Yang Z, Zheng M, Cheng H. Superoxide flashes: elemental events of mitochondrial ROS signaling in the heart. J Mol Cell Cardiol. 2012;52:940-948. doi: 10.1016/j. yjmcc.2012.02.007.
19. Chu Y, Iida S, Lund DD, Weiss RM, DiBona GF, Watanabe Y, Faraci FM, Heistad DD. Gene transfer of extracellular superoxide dismutase reduces arterial pressure in spontaneously hypertensive rats: role of heparin-binding domain. Circ Res. 2003;92:461-468. doi: 10.1161/01. RES.0000057755.02845.F9.
20. Okutsu M, Call JA, Lira VA, Zhang M, Donet JA, French BA, Martin KS, Peirce-Cottler SM, Rembold CM, Annex BH, Yan Z. Extracellular superoxide dismutase ameliorates skeletal muscle abnormalities, cachexia, and exercise intolerance in mice with congestive heart failure. Circ Heart Fail. 2014;7:519-530. doi: 10.1161/CIRCHEARTFAILURE.113.000841.
21. Chu Y, Piper R, Richardson S, Watanabe Y, Patel P, Heistad DD. Endocytosis of extracellular superoxide dismutase into endothelial cells: role of the heparin-binding domain. Arterioscler Thromb Vasc Biol. 2006;26:1985-1990. doi: 10.1161/01.ATV.0000234921.88489.5c.
22. Shao CH, Wehrens XH, Wyatt TA, Parbhu S, Rozanski GJ, Patel KP, Bidasee KR. Exercise training during diabetes attenuates cardiac ryanodine receptor dysregulation. J Appl Physiol (1985). 2009;106:1280-1292. doi: 10.1152/japplphysiol.91280.2008.
23. Atalay M, Laaksonen DE. Diabetes, oxidative stress and physical exercise. J Sports Sci Med. 2002;1:1-14.
24. 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 (1985). 2005;98:461-467. doi: 10.1152/japplphysiol.00551.2004.
25. Akimoto T, Ribar TJ, Williams RS, Yan Z. Skeletal muscle adaptation in response to voluntary running in Ca2+/calmodulin-dependent protein kinase IV-deficient mice. Am J Physiol Cell Physiol. 2004;287:C1311-C1319. doi: 10.1152/ajpcell.00248.2004.
26. Yan Z, Choi S, Liu X, Zhang M, Schageman JJ, Lee SY, Hart R, Lin L, Thurmond FA, Williams RS. Highly coordinated gene regulation in mouse skeletal muscle regeneration. J Biol Chem. 2003;278:8826-8836. doi: 10.1074/jbc.M209879200.
27. Konkalmatt PR, Wang F, Piras BA, Xu Y, O'Connor DM, Beyers RJ, Epstein FH, Annex BH, Hossack JA, French BA. Adeno-associated virus serotype 9 administered systemically after reperfusion preferentially targets cardiomyocytes in the infarct border zone with pharmacodynamics suitable for the attenuation of left ventricular remodeling. J Gene Med. 2012;14:609-620. doi: 10.1002/jgm.2673.
28. Saqib A, Prasad KM, Katwal AB, Sanders JM, Lye RJ, French BA, Annex BH. Adeno-associated virus serotype 9-mediated overexpression of extracellular superoxide dismutase improves recovery from surgical hind-limb ischemia in BALB/c mice. J Vasc Surg. 2011;54:810-818. doi: 10.1016/j.jvs.2011.03.278.
29. Yu Z, Li P, Zhang M, Hannink M, Stamler JS, Yan Z. Fiber type-specific nitric oxide protects oxidative myofibers against cachectic stimuli. PLoS One. 2008;3:e2086. doi: 10.1371/journal.pone.0002086.
30. Maillet M, Davis J, Auger-Messier M, York A, Osinska H, Piquereau J, Lorenz JN, Robbins J, Ventura-Clapier R, Molkentin JD. Heart-specific deletion of CnB1 reveals multiple mechanisms whereby calcineurin regulates cardiac growth and function. J Biol Chem. 2010;285:6716-6724. doi: 10.1074/jbc.M109.056143.
31. Lim HW, Molkentin JD. Calcineurin and human heart failure. Nat Med. 1999;5:246-247. doi: 10.1038/6430.
32. Stanford KI, Middelbeek RJ, Townsend KL, An D, Nygaard EB, Hitchcox KM, Markan KR, Nakano K, Hirshman MF, Tseng YH, Goodyear LJ. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2013;123:215-223. doi: 10.1172/JCI62308.
33. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol. 2012;8:457-465. doi: 10.1038/nrendo.2012.49.
34. Heineke J, Auger-Messier M, Xu J, Sargent M, York A, Welle S, Molkentin JD. Genetic deletion of myostatin from the heart prevents skeletal muscle atrophy in heart failure. Circulation. 2010;121:419-425. doi: 10.1161/CIRCULATIONAHA.109.882068.
35. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Boström EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Højlund K, Gygi SP, Spiegelman BM. A PGC1-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481:463-468. doi: 10.1038/nature10777.
36. Laakso M. Glycemic control and the risk for coronary heart disease in patients with non-insulin-dependent diabetes mellitus. The Finnish studies. Ann Intern Med. 1996;124(1 pt 2):127-130.
37. Tokudome T, Horio T, Yoshihara F, Suga S, Kawano Y, Kohno M, Kangawa K. Direct effects of high glucose and insulin on protein synthesis in cultured cardiac myocytes and DNA and collagen synthesis in cardiac fibroblasts. Metabolism. 2004;53:710-715.
38. Palmieri V, Capaldo B, Russo C, Iaccarino M, Pezzullo S, Quintavalle G, Di Minno G, Riccardi G, Celentano A. Uncomplicated type 1 diabetes and preclinical left ventricular myocardial dysfunction: insights from echocardiography and exercise cardiac performance evaluation. Diabetes Res Clin Pract. 2008;79:262-268. doi: 10.1016/j.diabres.2007.09.014.
39. Yu CM, Lin H, Yang H, Kong SL, Zhang Q, Lee SW. Progression of systolic abnormalities in patients with "isolated" diastolic heart failure and diastolic dysfunction. Circulation. 2002;105:1195-1201.
40. Crabtree GR, Olson EN. NFAT signaling: choreographing the social lives of cells. Cell. 2002;109(suppl):S67-S79.
41. Ruwhof C, van der Laarse A. Mechanical stress-induced cardiac hypertrophy: mechanisms and signal transduction pathways. Cardiovasc Res. 2000;47:23-37.
42. Song Y, Wang J, Li Y, Du Y, Arteel GE, Saari JT, Kang YJ, Cai L. Cardiac metallothionein synthesis in streptozotocin-induced diabetic mice, and its protection against diabetes-induced cardiac injury. Am J Pathol. 2005;167:17-26. doi: 10.1016/S0002-9440(10)62949-5.
43. Malhotra A, Kang BP, Vashistha H, Yadav VS, Meggs LG. Overexpression of Gsalpha compensates for myocyte loss in diabetic cardiomyopathy. Can J Physiol Pharmacol. 2008;86:122-130. doi: 10.1139/y08-015.
44. Rajesh M, Mukhopadhyay P, Bátkai S, Mukhopadhyay B, Patel V, Haskó G, Szabó C, Mabley JG, Liaudet L, Pacher P. Xanthine oxidase inhibitor allopurinol attenuates the development of diabetic cardiomyopathy. J Cell Mol Med. 2009;13(8B):2330-2341. doi: 10.1111/j.1582-4934.2008.00564.x.
45. Li J, Zhu H, Shen E, Wan L, Arnold JM, Peng T. Deficiency of rac1 blocks NADPH oxidase activation, inhibits endoplasmic reticulum stress, and reduces myocardial remodeling in a mouse model of type 1 diabetes. Diabetes. 2010;59:2033-2042. doi: 10.2337/db09-1800.
46. Ye G, Metreveli NS, Donthi RV, Xia S, Xu M, Carlson EC, Epstein PN. Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes. 2004;53:1336-1343.
47. Matsushima S, Kinugawa S, Ide T, Matsusaka H, Inoue N, Ohta Y, Yokota T, Sunagawa K, Tsutsui H. Overexpression of glutathione peroxidase attenuates myocardial remodeling and preserves diastolic function in diabetic heart. Am J Physiol Heart Circ Physiol. 2006;291:H2237-H2245. doi: 10.1152/ajpheart.00427.2006.
48. Sesso HD, Buring JE, Christen WG, Kurth T, Belanger C, MacFadyen J, Bubes V, Manson JE, Glynn RJ, Gaziano JM. Vitamins E and C in the prevention of cardiovascular disease in men: the Physicians' Health Study II randomized controlled trial. JAMA. 2008;300:2123-2133. doi: 10.1001/jama.2008.600.
49. Deel ED van, Lu Z, Xu X, Zhu G, Hu X, Oury TD, Bache RJ, Duncker DJ, Chen Y. Extracellular superoxide dismutase protects the heart against oxidative stress and hypertrophy after myocardial infarction. Free Radic Biol Med. 2008;44:1305-1313.
50. Giusti B, Marini M, Rossi L, Lapini I, Magi A, Capalbo A, Lapalombella R, di Tullio S, Samaja M, Esposito F, Margonato V, Boddi M, Abbate R, Veicsteinas A. Gene expression profile of rat left ventricles reveals persisting changes following chronic mild exercise protocol: implications for cardioprotection. BMC Genomics. 2009;10:342. doi: 10.1186/1471-2164-10-342.