Heart, Lung and Circulation
Volume 18, Issue 1 , Pages 11-18 , February 2009

Evidence for a Causal Role of Oxidative Stress in the Myocardial Complications of Insulin Resistance

References 

  1. King H, Aubert RE, Herman WH. Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projections. Diabetes Care. 1998;21:1414–1431
  2. 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
  3. Jandeleit-Dahm KAM, Tikellis C, Reid CM, Johnston CI, Cooper ME. Why blockade of the renin-angiotensin system reduces the incidence of new-onset diabetes. J Hypertens. 2005;23:463–473
  4. Devereux RB, Roman MJ, Paranicas M, O’Grady MJ, Lee ET, Welty TK, et al. Impact of diabetes on cardiac structure and function: the strong heart study. Circulation. 2000;101:2271–2276
  5. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation. 2007;115:3213–3223
  6. 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
  7. Ostenson CG. The pathophysiology of type 2 diabetes mellitus: an overview. Acta Physiol Scand. 2001;171:241–247
  8. Witteles RM, Fowler MB. Insulin-resistant cardiomyopathy clinical evidence, mechanisms, and treatment options. J Am Coll Cardiol. 2008;51:93–102
  9. Novoa FJ, Boronat M, Saavedra P, Diaz-Cremades JM, Varillas VF, La Roche F, et al. Differences in cardiovascular risk factors, insulin resistance, and insulin secretion in individuals with normal glucose tolerance and in subjects with impaired glucose regulation: the Telde Study. Diabetes Care. 2005;28:2388–2393
  10. Sorescu D, Griendling KK. Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest Heart Fail. 2002;8:132–140
  11. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol. 1996;271:C1424–C1437
  12. Cai L. Suppression of nitrative damage by metallothionein in diabetic heart contributes to the prevention of cardiomyopathy. Free Radic Biol Med. 2006;41:851–861
  13. Mitchell JB, Samuni A, Krishna MC, DeGraff WG, Ahn MS, Samuni U, et al. Biologically active metal-independent superoxide dismutase mimics. Biochemistry. 1990;29:2802–2807
  14. Selemidis S, Sobey CG, Schmidt HHHW, Wingler K, Drummond GR. NADPH oxidases in the vasculature: molecular features, roles in disease and pharmacological inhibition. Pharmacol Ther. 2008;120:254–291
  15. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414:813–820
  16. Sawyer DB, Siwik DA, Xiao L, Pimentel DR, Singh K, Colucci WS. Role of oxidative stress in myocardial hypertrophy and failure. J Mol Cell Cardiol. 2002;34:379–388
  17. Cave A, Grieve D, Johar S, Zhang M, Shah AM. NADPH oxidase-derived reactive oxygen species in cardiac pathophysiology. Philos Trans R Soc Lond B Biol Sci. 2005;360:2327–2334
  18. Ritchie RH, Delbridge LMD. Cardiac hypertrophy, substrate utilization and metabolic remodelling: cause or effect?. Clin Exp Pharmacol Physiol. 2006;33:171–178
  19. Laskowski A, Woodman OL, Cao AH, Drummond GR, Marshall T, Kaye DM, et al. Antioxidant actions contribute to the antihypertrophic effects of atrial natriuretic peptide in neonatal rat cardiomyocytes. Cardiovasc Res. 2006;72:112–123
  20. Cooper SA, Whaley-Connell A, Habibi J, Wei Y, Lastra G, Manrique C, et al. Renin-angiotensin-aldosterone system and oxidative stress in cardiovascular insulin resistance. Am J Physiol Heart Circ Physiol. 2007;293:H2009–H2023
  21. Dhalla AK, Hill MF, Singal PK. Role of oxidative stress in transition of hypertrophy to heart failure. J Am Coll Cardiol. 1996;28:506–514
  22. Fang ZY, Prins JB, Marwick TH. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev. 2004;25:543–567
  23. Saraiva RM, Duarte DM, Duarte MPC, Martins AF, Poltronieri AVG, Ferreira ME, et al. Tissue Doppler imaging identifies asymptomatic normotensive diabetics with diastolic dysfunction and reduced exercise tolerance. Echocardiography. 2005;22:561–570
  24. Galderisi M. Diastolic dysfunction and diabetic cardiomyopathy: evaluation by Doppler echocardiography. J Am Coll Cardiol. 2006;48:548–555
  25. Fang ZY, Najos-Valencia O, Leano R, Marwick TH. Patients with early diabetic heart disease demonstrate a normal myocardial response to dobutamine. J Am Coll Cardiol. 2003;42:611–617
  26. van der Meer RW, Diamant M, Westenberg JJM, Doornbos J, Bax JJ, de Roos A, et al. Magnetic resonance assessment of aortic pulse wave velocity, aortic distensibility, and cardiac function in uncomplicated type 2 diabetes mellitus. J Cardiovasc Magn Reson. 2007;9:645–651
  27. Poirier P, Bogaty P, Garneau C, Marois L, Dumesnil JG. Diastolic dysfunction in normotensive men with well-controlled type 2 diabetes: importance of maneuvers in echocardiographic screening for preclinical diabetic cardiomyopathy. Diabetes Care. 2001;24:5–10
  28. Zabalgoitia M, Ismaeil MF, Anderson L, Maklady FA. Prevalence of diastolic dysfunction in normotensive, asymptomatic patients with well-controlled type 2 diabetes mellitus. Am J Cardiol. 2001;87:320–323
  29. Di Bello V, Santini F, Di Cori A, Pucci A, Palagi C, Delle Donne MG, et al. Relationship between preclinical abnormalities of global and regional left ventricular function and insulin resistance in severe obesity: a color Doppler imaging study. Int J Obes (Lond). 2006;30:948–956
  30. Fischer M, Baessler A, Hense HW, Hengstenberg C, Muscholl M, Holmer S, et al. Prevalence of left ventricular diastolic dysfunction in the community—results from a Doppler echocardiographic-based survey of a population sample. Eur Heart J. 2003;24:320–328
  31. Watanabe K, Sekiya M, Tsuruoka T, Funada J, Kameoka H. Effect of insulin resistance on left ventricular hypertrophy and dysfunction in essential hypertension. J Hypertens. 1999;17:1153–1160
  32. Zizek B, Poredos P, Trojar A, Zeljko T. Diastolic dysfunction is associated with insulin resistance, but not with aldosterone level in normotensive offspring of hypertensive families. Cardiology. 2008;111:8–15
  33. Stewart KJ, Ouyang P, Bacher AC, Lima S, Shapiro EP. Exercise effects on cardiac size and left ventricular diastolic function: relationships to changes in fitness, fatness, blood pressure and insulin resistance. Heart. 2006;92:893–898
  34. Hsu KL, Tsai CH, Chiang FT, Lo HM, Tseng CD, Wang SM, et al. Myocardial mechanics and titin in experimental insulin-resistant rats. Jpn Heart J. 1997;38:717–728
  35. Huggins CE, Domenighetti AA, Ritchie ME, Khalil N, Favaloro JM, Proietto J, et al. Functional and metabolic remodelling in GLUT4-deficient hearts confers hyper-responsiveness to substrate intervention. J Mol Cell Cardiol. 2008;44:270–280
  36. Severson DL. Diabetic cardiomyopathy: recent evidence from mouse models of type 1 and type 2 diabetes. Can J Physiol Pharmacol. 2004;82:813–823
  37. Davidoff AJ, Mason MM, Davidson MB, Carmody MW, Hintz KK, Wold LE, et al. Sucrose-induced cardiomyocyte dysfunction is both preventable and reversible with clinically relevant treatments. Am J Physiol Endocrinol Metab. 2004;286:E718–E724
  38. Dutta K, Podolin DA, Davidson MB, Davidoff AJ. Cardiomyocyte dysfunction in sucrose-fed rats is associated with insulin resistance. Diabetes. 2001;50:1186–1192
  39. Donthi RV, Ye G, Wu C, McClain DA, Lange AJ, Epstein PN. Cardiac expression of kinase-deficient 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase inhibits glycolysis, promotes hypertrophy, impairs myocyte function, and reduces insulin sensitivity. J Biol Chem. 2004;279:48085–48090
  40. Whaley-Connell A, Habibi J, Cooper SA, Demarco VG, Hayden MR, Stump CS, et al. Effect of renin inhibition and AT1R blockade on myocardial remodeling in the transgenic Ren2 rat. Am J Physiol Endocrinol Metab. 2008;295:E103–E109
  41. Whaley-Connell A, Govindarajan G, Habibi J, Hayden MR, Cooper SA, Wei Y, et al. Angiotensin II-mediated oxidative stress promotes myocardial tissue remodeling in the transgenic (mRen2) 27 Ren2 rat. Am J Physiol Endocrinol Metab. 2007;293:E355–E363
  42. Fulop N, Mason MM, Dutta K, Wang P, Davidoff AJ, Marchase RB, et al. Impact of Type 2 diabetes and aging on cardiomyocyte function and O-linked N-acetylglucosamine levels in the heart. Am J Physiol Cell Physiol. 2007;292:C1370–C1378
  43. Wold LE, Dutta K, Mason MM, Ren J, Cala SE, Schwanke ML, et al. Impaired SERCA function contributes to cardiomyocyte dysfunction in insulin resistant rats. J Mol Cell Cardiol. 2005;39:297–307
  44. Jordan JE, Simandle SA, Tulbert CD, Busija DW, Miller AW. Fructose-fed rats are protected against ischemia/reperfusion injury. J Pharmacol Exp Ther. 2003;307:1007–1011
  45. Elliott SS, Keim NL, Stern JS, Teff K, Havel PJ. Fructose, weight gain, and the insulin resistance syndrome. Am J Clin Nutr. 2002;76:911–922
  46. Rajasekar P, Palanisamy N, Anuradha CV. Increase in nitric oxide and reductions in blood pressure, protein kinase C beta II and oxidative stress by l-carnitine: a study in the fructose-fed hypertensive rat. Clin Exp Hypertens. 2007;29:517–530
  47. Joyeux-Faure M, Rossini E, Ribuot C, Faure P. Fructose-fed rat hearts are protected against ischemia-reperfusion injury. Exp Biol Med (Maywood). 2006;231:456–462
  48. Delbosc S, Paizanis E, Magous R, Araiz C, Dimo T, Cristol J-P, et al. Involvement of oxidative stress and NADPH oxidase activation in the development of cardiovascular complications in a model of insulin resistance, the fructose-fed rat. Atherosclerosis. 2005;179:43–49
  49. Al-Awwadi NA, Bornet A, Azay J, Araiz C, Delbosc S, Cristol J-P, et al. Red wine polyphenols alone or in association with ethanol prevent hypertension, cardiac hypertrophy, and production of reactive oxygen species in the insulin-resistant fructose-fed rat. J Agric Food Chem. 2004;52:5593–5597
  50. Xia Z, Kuo K-H, Nagareddy PR, Wang F, Guo Z, Guo T, et al. N-Acetylcysteine attenuates PKCbeta2 overexpression and myocardial hypertrophy in streptozotocin-induced diabetic rats. Cardiovasc Res. 2007;73:770–782
  51. Matsushima S, Kinugawa S, Ide T, Matsusaka H, Inoue N, Ohta Y, et al. Overexpression of glutathione peroxidase attenuates myocardial remodeling and preserves diastolic function in diabetic heart. Am J Physiol Heart Circ Physiol. 2006;291:H2237–H2245
  52. Hiranandani N, Bupha-Intr T, Janssen PML. SERCA overexpression reduces hydroxyl radical injury in murine myocardium. Am J Physiol Heart Circ Physiol. 2006;291:H3130–H3135
  53. Ritchie RH, Quinn JM, Cao AH, Drummond GR, Kaye DM, Favaloro JM, et al. The antioxidant tempol inhibits cardiac hypertrophy in the insulin-resistant GLUT4-deficient mouse in vivo. J Mol Cell Cardiol. 2007;42:1119–1128
  54. Yaras N, Bilginoglu A, Vassort G, Turan B. Restoration of diabetes-induced abnormal local Ca2+ release in cardiomyocytes by angiotensin II receptor blockade. Am J Physiol Heart Circ Physiol. 2007;292:H912–H920
  55. Sakata S, Lebeche D, Sakata Y, Sakata N, Chemaly ER, Liang LF, et al. Mechanical and metabolic rescue in a type II diabetes model of cardiomyopathy by targeted gene transfer. Mol Ther. 2006;13:987–996
  56. Zhao X-Y, Hu S-J, Li J, Mou Y, Chen B-P, Xia Q. Decreased cardiac sarcoplasmic reticulum Ca2+-ATPase activity contributes to cardiac dysfunction in streptozotocin-induced diabetic rats. J Physiol Biochem. 2006;62:1–8
  57. Pereira L, Matthes J, Schuster I, Valdivia HH, Herzig S, Richard S, et al. Mechanisms of Ca2+ i transient decrease in cardiomyopathy of db/db type 2 diabetic mice. Diabetes. 2006;55:608–615
  58. Trost SU, Belke DD, Bluhm WF, Meyer M, Swanson E, Dillmann WH. Overexpression of the sarcoplasmic reticulum Ca(2+)-ATPase improves myocardial contractility in diabetic cardiomyopathy. Diabetes. 2002;51:1166–1171
  59. Lopaschuk GD, Tahiliani AG, Vadlamudi RV, Katz S, McNeill JH. Cardiac sarcoplasmic reticulum function in insulin- or carnitine-treated diabetic rats. Am J Physiol. 1983;245:H969–H976
  60. Li Q, Wu S, Li S-Y, Lopez FL, Du M, Kajstura J, et al. Cardiac-specific overexpression of insulin-like growth factor 1 attenuates aging-associated cardiac diastolic contractile dysfunction and protein damage. Am J Physiol Heart Circ Physiol. 2007;292:H1398–H1403
  61. Vasanji Z, Cantor EJF, Juric D, Moyen M, Netticadan T. Alterations in cardiac contractile performance and sarcoplasmic reticulum function in sucrose-fed rats is associated with insulin resistance. Am J Physiol Cell Physiol. 2006;291:C772–C780
  62. Xu S, Ying J, Jiang B, Guo W, Adachi T, Sharov V, et al. Detection of sequence-specific tyrosine nitration of manganese SOD and SERCA in cardiovascular disease and aging. Am J Physiol Heart Circ Physiol. 2006;290:H2220–H2227
  63. Adachi T, Weisbrod RM, Pimentel DR, Ying J, Sharov VS, Schoneich C, et al. S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med. 2004;10:1200–1207
  64. Kowluru RA, Engerman RL, Kern TS. Diabetes-induced metabolic abnormalities in myocardium: effect of antioxidant therapy. Free Radic Res. 2000;32:67–74
  65. Cosenzi A, Bernobich E, Plazzotta N, Seculin P, Odoni G, Bellini G. Lacidipine reduces high blood pressure and the target organ damage induced by high fructose diet in rats. J Hypertens. 1999;17:965–971
  66. Iyer SN, Katovich MJ. Effect of acute and chronic losartan treatment on glucose tolerance and insulin sensitivity in fructose-fed rats. Am J Hypertens. 1996;9:662–668
  67. Kamide K, Rakugi H, Higaki J, Okamura A, Nagai M, Moriguchi K, et al. The renin-angiotensin and adrenergic nervous system in cardiac hypertrophy in fructose-fed rats. Am J Hypertens. 2002;15:66–71
  68. Mizushige K, Yao L, Noma T, Kiyomoto H, Yu Y, Hosomi N, et al. Alteration in left ventricular diastolic filling and accumulation of myocardial collagen at insulin-resistant prediabetic stage of a type II diabetic rat model. Circulation. 2000;101:899–907
  69. Kaczmarczyk SJ, Andrikopoulos S, Favaloro J, Domenighetti AA, Dunn A, Ernst M, et al. Threshold effects of glucose transporter-4 (GLUT4) deficiency on cardiac glucose uptake and development of hypertrophy. J Mol Endocrinol. 2003;31:449–459
  70. Candido R, Forbes JM, Thomas MC, Thallas V, Dean RG, Burns WC, et al. A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res. 2003;92:785–792
  71. Bendall JK, Cave AC, Heymes C, Gall N, Shah AM. Pivotal role of a gp91(phox)-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation. 2002;105:293–296
  72. Belke DD, Larsen TS, Gibbs EM, Severson DL. Altered metabolism causes cardiac dysfunction in perfused hearts from diabetic (db/db) mice. Am J Physiol Endocrinol Metab. 2000;279:E1104–E1113
  73. Finck BN, Kelly DP. Peroxisome proliferator-activated receptor alpha (PPARalpha) signaling in the gene regulatory control of energy metabolism in the normal and diseased heart. J Mol Cell Cardiol. 2002;34:1249–1257
  74. How O-J, Aasum E, Severson DL, Chan WYA, Essop MF, Larsen TS. Increased myocardial oxygen consumption reduces cardiac efficiency in diabetic mice. Diabetes. 2006;55:466–473
  75. Rodrigo R, Guichard C, Charles R. Clinical pharmacology and therapeutic use of antioxidant vitamins. Fundam Clin Pharmacol. 2007;21:111–127
  76. Macao LB, Wilhelm Filho D, Pedrosa RC, Pereira A, Backes P, Torres MA, et al. Antioxidant therapy attenuates oxidative stress in chronic cardiopathy associated with Chagas’ disease. Int J Cardiol. 2007;123:43–49
  77. Lonn E, Yusuf S, Hoogwerf B, Pogue J, Yi QL, Zinman B, et al. Effects of vitamin E on cardiovascular and microvascular outcomes in high-risk patients with diabetes—results of the HOPE study and MICRO-HOPE substudy. Diabetes Care. 2002;25:1919–1927
  78. Munzel T, Keaney JF. Are ACE inhibitors a “magic bullet” against oxidative stress?. Circulation. 2001;104:1571–1574
  79. Lara-Padilla E, Kormanovski A, Grave PA, Olivares-Corichi IM, Santillan RM, Hicks JJ. Increased antioxidant capacity in healthy volunteers taking a mixture of oral antioxidants versus vitamin C or E supplementation. Adv Ther. 2007;24:50–59
  80. Upston JM, Witting PK, Brown AJ, Stocker R, Keaney JF. Effect of vitamin E on aortic lipid oxidation and intimal proliferation after arterial injury in cholesterol-fed rabbits. Free Radic Biol Med. 2001;31:1245–1253
  81. Wang X, Quinn PJ, Vitamin . E and its function in membranes. Prog Lipid Res. 1999;38:309–336
  82. Lindholm LH, Ibsen H, Dahlof B, Devereux RB, Beevers G, de Faire U, et al. Cardiovascular morbidity and mortality in patients with diabetes in the Losartan intervention for endpoint reduction in hypertension study (LIFE): a randomised trial against atenolol. Lancet. 2002;359:1004–1010
  83. Goh SSC, Woodman OL, Pepe S, Cao AH, Qin C, Ritchie RH. The red wine antioxidant resveratrol prevents cardiomyocyte injury following ischemia-reperfusion via multiple sites and mechanisms. Antioxid Redox Signal. 2007;9:101–113
  84. Hodgson JM, Watts GF. Can coenzyme Q10 improve vascular function and blood pressure? Potential for effective therapeutic reduction in vascular oxidative stress. BioFactors. 2003;18:129–136
  85. Pirola L, Frojdo S. Resveratrol: one molecule, many targets. IUBMB Life. 2008;60:323–332
  86. Hodgson JM, Watts GF, Playford DA, Burke V, Croft KD. Coenzyme Q10 improves blood pressure and glycaemic control: a controlled trial in subjects with type 2 diabetes. Eur J Clin Nutr. 2002;56:1137–1142
  87. Watts GF, Playford DA, Croft KD, Ward NC, Mori TA, Burke V. Coenzyme Q(10) improves endothelial dysfunction of the brachial artery in Type II diabetes mellitus. Diabetologia. 2002;45:420–426
  88. Shephard RJ, Balady GJ. Exercise as cardiovascular therapy. Circulation. 1999;99:963–972
  89. Sigal RJ, Kenny GP, Wasserman DH, Castaneda-Sceppa C, White RD. Physical activity/exercise and type 2 diabetes: a consensus statement from the American Diabetes Association. Diabetes Care. 2006;29:1433–1438
  90. Colberg SR. Being active; a commentary. Diabetes Educucator. 2007;33:989–990
  91. Linke A, Adams V, Schulze PC, Erbs S, Gielen S, Fiehn E, et al. Antioxidative effects of exercise training in patients with chronic heart failure: increase in radical scavenger enzyme activity in skeletal muscle. Circulation. 2005;111:1763–1770
  92. Brassard P, Legault S, Garneau C, Bogaty P, Dumesnil J-G, Poirier P. Normalization of diastolic dysfunction in type 2 diabetics after exercise training. Med Sci Sports Exerc. 2007;39:1896–1901
  93. Fossum E, Gleim GW, Kjeldsen SE, Kizer JR, Julius S, Devereux RB, et al. The effect of baseline physical activity on cardiovascular outcomes and new-onset diabetes in patients treated for hypertension and left ventricular hypertrophy: the LIFE study. J Intern Med. 2007;262:439–448
  94. Belardinelli R, Georgiou D, Ginzton L, Cianci G, Purcaro A. Effects of moderate exercise training on thallium uptake and contractile response to low-dose dobutamine of dysfunctional myocardium in patients with ischemic cardiomyopathy. Circulation. 1998;97:553–561
  95. Powers SK, Criswell D, Lawler J, Martin D, Lieu FK, Ji LL, et al. Rigorous exercise training increases superoxide dismutase activity in ventricular myocardium. Am J Physiol. 1993;265:193–201
  96. Libonati JR, Kendrick ZV, Houser SR. Sprint training improves postischemic, left ventricular diastolic performance. J Appl Physiol. 2005;99:2121–2127
  97. Morris GS, Baldwin KM, Lash JM, Hamlin RL, Sherman WM. Exercise alters cardiac myosin isozyme distribution in obese Zucker and Wistar rats. J Appl Physiol. 1990;69:380–383
  98. McMullen JR, Amirahmadi F, Woodcock EA, Schinke-Braun M, Bouwman RD, Hewitt KA, et al. Protective effects of exercise and phosphoinositide 3-kinase(p110alpha) signaling in dilated and hypertrophic cardiomyopathy. Proc Natl Acad Sci USA. 2007;104:612–617

PII: S1443-9506(08)00948-7

doi: 10.1016/j.hlc.2008.11.003

Heart, Lung and Circulation
Volume 18, Issue 1 , Pages 11-18 , February 2009