Ca2+ mishandling and cardiac dysfunction in obesity and insulin resistance: Role of oxidative stress

Cell Calcium

Volumn 56, Issue 5, 2014, Pages 408-415

  Carvajal, Karla ^a   Balderas Villalobos, Jaime ^a,b   Bello Sanchez, Ma Dolores ^b   Phillips Farfán, Bryan ^a   Molina Muñoz, Tzindilu ^b   Aldana Quintero, Hugo ^b   Gómez Viquez, Norma L ^b  

^a INSTITUTO NACIONAL DE PEDIATRÍA   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Ca2+ handling; Cardiomyopathy; Insulin resistance; Obesity; Oxidative stress

Indexed keywords

CALCIUM ION; INSULIN; REACTIVE OXYGEN METABOLITE; CALCIUM;

CALCIUM HOMEOSTASIS; DEATH; DIASTOLIC DYSFUNCTION; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE EXACERBATION; HEART FAILURE; HUMAN; INSULIN RESISTANCE; LIFESTYLE MODIFICATION; METABOLIC DISORDER; MORBIDITY; NONHUMAN; OBESITY; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PREVALENCE; REVIEW; SYSTOLIC DYSFUNCTION; CALCIUM SIGNALING; GENETICS; HEART MITOCHONDRION; METABOLISM; PATHOLOGY;

CALCIUM; CALCIUM SIGNALING; HUMANS; INSULIN; INSULIN RESISTANCE; MITOCHONDRIA, HEART; OBESITY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84912139703     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.08.003     Document Type: Review

References (111)

1. Martin B.C., Warram J.H., Krolewski A.S., Soeldner J.S., Kahn C.R., Bergman R.N. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study. Lancet 1992, 340:925-929.
2. Scognamiglio R., Avogaro A., Negut C., Piccolotto R., Vigili de Kreutzenberg S., Tiengo A. Early myocardial dysfunction in the diabetic heart: current research and clinical applications. Am. J. Cardiol. 2004, 93:17A-20A.
3. Witteles R.M., Fowler M.B. Insulin-resistant cardiomyopathy clinical evidence, mechanisms, and treatment options. J. Am. Coll. Cardiol. 2008, 51:93-102.
4. Krauss R.M., Winston M., Fletcher R.N., Grundy S.M. Obesity: impact of cardiovascular disease. Circulation 1998, 98:1476-1486.
5. Boudina S., Abel E.D. Diabetic cardiomyopathy, causes and effects. Rev. Endocr. Metab. Disord. 2010, 11:31-39.
6. Fang Z.Y., Prins J.B., Marwick T.H. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr. Rev. 2004, 25:543-567.
7. Arnlöv J., Lind L., Zethelius B., et al. Several factors associated with the insulin resistance syndrome are predictors of left ventricular systolic dysfunction in a male population after 20 years of follow-up. Am. Heart J. 2001, 142:720-724.
8. Arnlöv J., Lind L., Sundström J., Andrén B., Vessby B., Lithell H. Insulin resistance, dietary fat intake and blood pressure predict left ventricular diastolic function 20 years later. Nutr. Metab. Cardiovasc. Dis. 2005, 15:242-249.
9. Dinh F.R., Lankisch M., Nickl W., Gies M., Scheyer D., Kramer F., Scheffold T., Krahns T., Sause A. Metabolic syndrome with or without diabetes contributes to left ventricular diastolic dysfunction. Acta Cardiol. 2011, 66:167-174.
10. Ceriello A., Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler. Thromb. Vasc. Biol. 2004, 24:816-823.
11. Park J.D.J., Gross M., Lee D.H., Holvoet P., Himes J.H., Shikany J.M. Oxidative stress and insulin resistance: the coronary artery risk development in young adults study. Diabetes Care 2009, 32:1302-1307.
12. Rains J.L., Jain S.K. Oxidative stress, insulin signaling, and diabetes. Free Radic. Biol. Med. 2011, 50:567-575.
13. Fernández-Sánchez A., Madrigal-Santillán E., Bautista M., et al. Inflammation, oxidative stress, and obesity. Int. J. Mol. Sci. 2011, 12:3117-3132.
14. Carvajal B.G., El-Hafidi M. Myocardial damage due to ischemia and reperfusion in hypertriglyceridemic and hypertensive rats: participation of free radicals and calcium overload. J. Hypertens. 1999, 17:1607-1616.
15. 2+-ATPase and myosin heavy chain isozyme switch. Diabetologia 2006, 49:1434-1446.
16. Dong F., Fang C.X., Yang X., Zhang X., Lopez F.L., Ren J. Cardiac overexpression of catalase rescues cardiac contractile dysfunction induced by insulin resistance: role of oxidative stress, protein carbonyl formation and insulin sensitivity. Diabetologia 2006, 49:1421-1433.
17. Balderas-Villalobos J., Molina-Muñoz T., Mailloux-Salinas P., Bravo G., Carvajal K., Gómez-Viquez N.L. Oxidative stress in cardiomyocytes contributes to decreased SERCA2a activity in rats with metabolic syndrome. Am. J. Physiol. Heart Circ. Physiol. 2013, 305:H1344-H1353.
18. Caballero B. The global epidemic of obesity: an overview. Epidemiol. Rev. 2007, 29:1-5.
19. World Health Organization, Obesity and Overweight.
20. Hu F.B., Manson J.E., Stampfer M.J., Colditz G., Liu S., Solomon C.G. Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N. Engl. J. Med. 2001, 345:790-797.
21. Kannel W.B., McGee D.L. Diabetes and cardiovascular disease: the Framingham study. J. Am. Med. Assoc. 1979, 241:2035-2038.
22. Hu F.B., Stampfer M.J., Haffner S.M., Solomon C.G., Willett W.C., Manson J.E. Elevated risk of cardiovascular disease prior to clinical diagnosis of type 2 diabetes. Diabetes Care 2002, 25:1129-1134.
23. Kenchaiah V.R., Evans J.C., Levy D., Wilson P.W., Benjamin E.J., Larson M.G., Kannel W.B. Obesity and the risk of heart failure. N. Engl. J. Med. 2002, 347:305-313.
24. Nichols G.A., Gullion C.M., Koro C.E., Ephross S.A., Brown J.B. The incidence of congestive heart failure in type 2 diabetes: an update. Diabetes Care 2004, 27:1879-1884.
25. Kannel W.B., Hjortland M., Castelli W.P. Role of diabetes in congestive heart failure: the Framingham study. Am. J. Cardiol. 1974, 34:29-34.
26. Cardiovascular Disease, World Health Organization.
27. Wilson P.W. Diabetes mellitus and coronary heart disease. Endocrinol. Metab. Clin. North Am. 2001, 30:857-881.
28. Reaven G.M. Insulin resistance: the link between obesity and cardiovascular disease. Med. Clin. North Am. 2011, 95:875-892.
29. Ingelsson E., Sundström J., Arnlöv J., Zethelius B., Lind L. Insulin resistance and risk of congestive heart failure. J. Am. Med. Assoc. 2005, 294:334-341.
30. Vasan R.S. Cardiac function and obesity. Heart 2003, 89:1127-1129.
31. Ingelsson E., Arnlöv J., Sundström J., Zethelius B., Vessby B., Lind L. Novel metabolic risk factors for heart failure. J. Am. Coll. Cardiol. 2005, 46:2054-2060.
32. Kosmala W., Wong C., Kuliczkowska J., Leano R., Przewlocka-Kosmala M., Marwick T.H. Use of body weight and insulin resistance to select obese patients for echocardiographic assessment of subclinical left ventricular dysfunction. Am. J. Cardiol. 2008, 101:1334-1340.
33. Ichikawa R., Daimon M., Miyazaki T., et al. Influencing factors on cardiac structure and function beyond glycemic control in patients with type 2 diabetes mellitus. Cardiovasc. Diabetol. 2013, 12:38.
34. Abel E.D., Litwin S.E., Sweeney G. Cardiac remodelling in obesity. Physiol. Rev. 2008, 88:389-419.
35. Peterson L.R., Waggoner A.D., Schechtman K.B., et al. Alterations in left ventricular structure and function in young healthy obese women: assessment by echocardiography and tissue Doppler imaging. J. Am. Coll. Cardiol. 2004, 43:1399-1404.
36. Pascual M., Pascual D.A., Soria F., et al. Effects of isolated obesity on systolic and diastolic left ventricular function. Heart 2003, 89:1152-1156.
37. LR P. Obesity and insulin resistance: effects on cardiac structure, function, and substrate metabolism. Curr. Hypertens. Rep. 2006, 8:451-456.
38. Pulakat L., Demarco V.G., Whaley-Connell A., Sowers J.R. The impact of overnutrition on insulin metabolic signaling in the heart and the kidney. Cardiorenal Med. 2011, 1:102-112.
39. Mandavia C.H., Aroor A.R., Demarco V.G., Sowers J.R. Molecular and metabolic mechanisms of cardiac dysfunction in diabetes. Life Sci. 2013, 92:601-608.
40. Rutter M.K. Impact of glucose intolerance and insulin resistance on cardiac structure and function: sex-related differences in the Framingham heart study. Circulation 2003, 107:448-454.
41. Novo G., Pugliesi M., Visconti C., et al. Early subclinical ventricular dysfunction in patients with insulin resistance. J. Cardiovasc. Med. 2014, 15:110-114.
42. Wong C.Y., O'Moore-Sullivan T., Leano R., Byrne N., Beller E., Marwick T.H. Alterations of left ventricular myocardial characteristics associated with obesity. Circulation 2004, 110:3081-3087.
43. Di Bello V., Santini F., Di Cori A., 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.
44. Alpert M.A., Lambert C.R., Panayiotou H., et al. Relation of duration of morbid obesity to left ventricular mass, systolic function, and diastolic filling, and effect of weight loss. Am. J. Cardiol. 1995, 76:1194-1197.
45. Abe T., Ohga Y., Tabayashi N., et al. Left ventricular diastolic dysfunction in type 2 diabetes mellitus model rats. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H138-H148.
46. Pelleymounter M.A., Cullen M.J., Baker M.B., et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science 1995, 269:540-543.
47. Davidoff A.J., Mason M.M., Davidson M.B., et al. Sucrose-induced cardiomyocyte dysfunction is both preventable and reversible with clinically relevant treatments. Am. J. Physiol. Endocrinol. Metab. 2004, 286:E718-E724.
48. Dutta K., Podolin D.A., Davidson M.B., Davidoff A.J. Cardiomyocyte dysfunction in sucrose-fed rats is associated with insulin resistance. Diabetes 2001, 50:1188-1192.
49. Hintz K.K., Ren J. Prediabetic insulin resistance is not permissive to the development of cardiac resistance to insulin-like growth factor I in ventricular myocytes. Diabetes Res. Clin. Pract. 2002, 55:89-98.
50. Hintz K.K., Aberle N.S., Ren J. Insulin resistance induces hyperleptinemia, cardiac contractile dysfunction but not cardiac leptin resistance in ventricular myocytes. Int. J. Obes. Relat. Metab. Disord. 2003, 27:1196-1203.
51. Pierce G.N., Lockwood M.K., Eckhert C.D. Cardiac contracile protein ATPase activity in a diet induced model of noninsulin dependent diabetes mellitus. Can. J. Cardiol. 1989, 5:117-120.
52. Wold L.E., Dutta K., Mason M.M., et al. Impaired SERCA function contributes to cardiomyocyte dysfunction in insulin resistant rats. J. Mol. Cell. Cardiol. 2005, 39:297-307.
53. Deng J., Huang J., Lu L., Hung L. Impairment of cardiac insulin signaling and myocardial contractile performance in high-cholesterol/fructose-fed rats. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:978-987.
54. Vasanji Z., Cantor E.J.F., 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, 291:772-780.
55. Carvajal B.G. Myocardial function and effect of serum in isolated heart from hypertriglyceridemic and hypertensive rats. Clin. Exp. Hypertens. 2002, 24:235-248.
56. Bugger H., Abel E.D. Molecular mechanisms of diabetic cardiomyopathy. Diabetologia 2014, 57:660-671.
57. Park S., Cho Y., Kim H., et al. Unraveling the temporal pattern of diet-induced insulin in C57BL/6 mice. Diabetes 2005, 54:3530-3540.
58. Serpillon S., Floyd B.C., Gupte R.S., et al. Superoxide production by NAD(P)H oxidase and mitochondria is increased in genetically obese and hyperglycemic rat heart and aorta before the development of cardiac dysfunction: the role of glucose-6-phosphate dehydrogenase-derived NADPH. Am. J. Physiol Heart Circ. Physiol. 2009, 1:H153-H162.
59. Demarco V.G., Ford D.A., Henriksen E.J., et al. Obesity-related alterations in cardiac lipid profile and nondipping blood pressure pattern during transition to diastolic dysfunction in male db/db mice. Endocrinology 2014, 154:159-171.
60. Manrique C., DeMarco V.G., Aroor A.R., et al. Obesity and insulin resistance induce early development of diastolic dysfunction in young female mice fed a Western diet. Endocrinology 2013, 154:3632-3642.
61. Ansley D.M., Wang B. Oxidative stress and myocardial injury in the diabetic heart. J. Pathol. 2013, 229:232-241.
62. Abel E.D., O'Shea K.M., Ramasamy R. Insulin resistance: metabolic mechanisms and consequences in the heart. Arterioscler. Thromb. Vasc. Biol. 2012, 32:2068-2076.
63. Gray S., Kim J.K. New insights into insulin resistance in the diabetic heart. Trends Endocrinol. Metab. 2011, 22:394-403.
64. Roberts C.K., Sindhu K.K. Oxidative stress and metabolic syndrome. Life Sci. 2009, 84:705-712.
65. Boudina S., Abel E.D. Diabetic cardiomyopathy revisited. Circulation 2007, 115:3213-3223.
66. Ouwens D.M., Diamant M. Myocardial insulin action and the contribution of insulin resistance to the pathogenesis of diabetic cardiomyopathy. Arch. Physiol. Biochem. 2007, 113:76-86.
67. Ko H.J., Zhang Z., Jung D.Y., et al. Nutrient stress activates inflammation and reduces glucose metabolism by suppressing AMP-activated protein kinase in the heart. Diabetes 2009, 11:2536-2546.
68. Peterson L.R. Obesity and insulin resistance: effects on cardiac structure, function, and substrate metabolism. Curr. Hypertens. Rep. 2006, 8:451-456.
69. Battiprolu P.K., Gillette T.G., Wang Z.V., Lavandero S., Hill J.A. Diabetic cardiomyopathy: mechanisms and therapeutic targets. Drug Discov. Today Dis. Mech. 2010, 7:e135-e143.
70. Zhang L., Keung W., Samokhvalov V., Wang W., Lopaschuk G.D. Role of fatty acid uptake and fatty acid beta-oxidation in mediating insulin resistance in heart and skeletal muscle. Biochim. Biophys. Acta 2010, 1801:1-22.
71. Kim J.K., Kim Y., Fillmore J.J., et al. Prevention of fat-induced insulin resistance by salicylate. J. Clin. Invest. 2001, 108:437-446.
72. Ouwens A.D.M., Boer C., Fodor M., de Galan P., Heine R.J., Maassen J.A., Diamant M. Cardiac dysfunction induced by high-fat diet is associated with altered myocardial insulin signalling in rats. Diabetologia 2005, 48:1229-1237.
73. Boudina A.E., Bugger H., Sena S., O'Neill B.T., Zaha V.G., Ilkun O., Wright J.J., Mazumder P.K., Palfreyman E., Tidwell T.J., Theobald H., Khalimonchuk O., Wayment B., Sheng X., Rodnick K.J., Centini R., Chen D., Litwin S.E., Weimer B.E. Contribution of impaired myocardial insulin signaling to mitochondrial dysfunction and oxidative stress in the heart. Circulation 2009, 119:1272-1283.
74. Boudina A.E., Sena S., O'Neill B.T., Tathireddy P., Young M.E. Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 2005, 112:2686-2695.
75. Carvajal K., El Hafidi M., Marin-Hernández A., Moreno-Sánchez R. Structural and functional changes in heart mitochondria from sucrose-fed hypertriglyceridemic rats. Biochim. Biophys. Acta 2005, 1709:231-239.
76. Battiprolu P.K., Gillette T.G., Wang Z.V., Lavandero S., Hill J.A. Diabetic cardiomyopathy: mechanisms and therapeutic targets. Drug Discov. Today Dis. 2011, 7:1-15.
77. Doenst A.E., Nguyen T.D. Cardiac metabolism in heart failure: implications beyond ATP production. Circ. Res. 2013, 113:709-724.
78. Fauconnier W.H., Andersson D.C., Zhang S.J., Lanner J.T., Wibom R., Katz A., Bruton J.D. Effects of palmitate on Ca(2+) handling in adult control and ob/ob cardiomyocytes: impact of mitochondrial reactive oxygen species. Diabetes 2007, 56:1136-1142.
79. Ye G., Metreveli N.S., Donthi R.V., et al. Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes 2004, 53:1336-1343.
80. Shen X., Zheng S., Metreveli N.S., Epstein P.N. Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes 2006, 55:798-805.
81. 2+-handling protein profile in obese rats. Hypertension 2010, 56:629-635.
82. Buchanan J., Mazumder P.K., Hu P., et al. 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.
83. Dincer U.D., Araiza A., Knudson J.D., Shao C.H., Bidasee K.R., Tune J.D. Dysfunction of cardiac ryanodine receptors in the metabolic syndrome. J. Mol. Cell. Cardiol. 2006, 41:108-114.
84. Aasum E., Hafstad A.D., Severson D.L., Larsen T.S. Age-dependent changes in metabolism, contractile function, and ischemic sensitivity in hearts from db/db Mice. Diabetes 2003, 2:434-441.
85. Ren J., Sowers J.R., Walsh M.F., a Brown R. Reduced contractile response to insulin and IGF-I in ventricular myocytes from genetically obese Zucker rats. Am. J. Physiol. Heart Circ. Physiol. 2000, 279:H1708-H1714.
86. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
87. 2+ pump of sarcoplasmic reticulum. Nature 1989, 342:90-92.
88. Miklós Z., Kemecsei P., Bíró T., et al. Early cardiac dysfunction is rescued by upregulation of SERCA2a pump activity in a rat model of metabolic syndrome. Acta Physiol. 2012, 205:381-393.
89. Flepisi T.B., Lochner A., Huisamen B. The consequences of long-term glycogen synthase kinase-3 inhibition on normal and insulin resistant rat hearts. Cardiovasc. Drugs Ther. 2013, 27:381-392.
90. Lima-Leopoldo A.P., Leopoldo A.S., Silva D.C.T., et al. Influence of long-term obesity on myocardial gene expression. Arq. Bras. Cardiol. 2013, 100:229-236.
91. Trafford A.W., Díaz M.E., O'Neill S.C., Eisner D.A. Integrative analysis of calcium signalling in cardiac muscle. Front. Biosci. 2002, 1:d843-d852.
92. 2+ spikes in rat cardiac myocytes. J. Physiol. 1998, 512:677-691.
93. Lin Y.-C., Huang J., Kan H., Castranova V., Frisbee J.C., Yu H.-G. Defective calcium inactivation causes long QT in obese insulin-resistant rat. Am. J. Physiol. Heart Circ. Physiol. 2012, 302:H1013-H1022.
94. Perjés S.I., Kubin A.M., Kónyi A., Szabados S., Cziráki A., Skoumal R., Ruskoaho H. Physiological regulation of cardiac contractility by endogenous reactive oxygen species. Acta Physiol. 2012, 205:26-40.
95. 2+ cycling defect in the diabetic heart. Heart Fail. Rev. 2014, 19:101-112.
96. Lancel C.W., Qin F., Lennon S.L., Zhang J., Tong X., Mazzini M.J., Kang Y.J., Siwik D.A., Cohen R.A. Oxidative posttranslational modifications mediate decreased SERCA activity and myocyte dysfunction in Galphaq-overexpressing mice. Circ. Res. 2011, 107:228-232.
97. 2+ leak in chronic heart failure. Circ. Res. 2008, 103:1466-1472.
98. Qin C.W., Siwik D.A., Luptak I., Hou X., Wang L., Higuchi A., Weisbrod R.M., Ouchi N., Tu V.H., Calamaras T.D., Miller E.J., Verbeuren T.J., Walsh K., Cohen R.A. The polyphenols resveratrol and S17834 prevent the structural and functional sequelae of diet-induced metabolic heart disease in mice. Circulation 2013, 125:1757-1764.
99. Cutler M.J., Plummer B.N., Wan X., et al. Aberrant S-nitrosylation mediates calcium-triggered ventricular arrhythmia in the intact heart. Proc. Natl. Acad. Sci. U. S. A. 2012, 44:18186-18191.
100. Zima A.V., Blatter L.A. Redox regulation of cardiac calcium channels and transporters. Cardiovasc. Res. 2006, 71:310-321.
101. Santos C.X.C., Anilkumar N., Zhang M., Brewer A.C., Shah A.M. Redox signaling in cardiac myocytes. Free Radic. Biol. Med. 2011, 50:777-793.
102. Hills A.P., Byrne N.M., Lindstrom R., Hill J.O. Small changes to diet and physical activity behaviors for weight management. Obes. Facts 2013, 6:228-238.
103. Strasser B. Physical activity in obesity and metabolic syndrome. Ann. N. Y. Acad. Sci. 2013, 1281:141-159.
104. Vissers D., Hens W., Taeymans J., Baeyens J.-P., Poortmans J., Van Gaal L. The effect of exercise on visceral adipose tissue in overweight adults: a systematic review and meta-analysis. PLOS ONE 2013, 8:e56415.
105. Fiuza-Luces L.A., Garatachea N., Berger N.A. Exercise is the real polypill. Physiology (Bethesda) 2013, 28:350-358.
106. Ilkun O., Boudina S. Cardiac dysfunction and oxidative stress in the metabolic syndrome: an update on antioxidant therapies. Curr. Pharm. Des. 2013, 19:4806-4817.
107. Huang W.-Y., Davidge S.T., Wu J. Bioactive natural constituents from food sources-potential use in hypertension prevention and treatment. Crit. Rev. Food Sci. Nutr. 2013, 53:615-630.
108. Eilat-Adar S., Sinai T., Yosefy C., Henkin Y. Nutritional recommendations for cardiovascular disease prevention. Nutrients 2013, 17:3646-3683.
109. Kashyap S.R., Gatmaitan P., Brethauer S. Bariatric surgery for type 2 diabetes: weighing the impact for obese patients. Cleve. Clin. J. Med. 2011, 77:468-476.
110. Castagneto M., Mingrone G. The effect of gastrointestinal surgery on insulin resistance and insulin secretion. Curr. Atheroscler. Rep. 2012, 14:624-630.
111. Williams S., Cunningham E., Pories W.J. Surgical treatment of metabolic syndrome. Med. Princ. Pract. 2012, 21:301-309.