Lowering body weight in obese mice with diastolic heart failure improves cardiac insulin sensitivity and function: Implications for the obesity paradox

Diabetes

Volumn 64, Issue 5, 2015, Pages 1643-1657

  Sankaralingam, Sowndramalingam ^a   Alrob, Osama Abo ^a,b   Zhang, Liyan ^a   Jaswal, Jagdip S ^a   Wagg, Cory S ^a   Fukushima, Arata ^a   Padwal, Raj S ^a   Johnstone, David E ^a   Sharma, Arya M ^a   Lopaschuk, Gary D ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b YARMOUK UNIVERSITY   (Jordan)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; MITOGEN ACTIVATED PROTEIN KINASE P38; STAT3 PROTEIN; TRANSCRIPTION FACTOR FKHR; TRIACYLGLYCEROL; FAT INTAKE; FATTY ACID; INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIASTOLIC HEART FAILURE; ECHOCARDIOGRAPHY; ENERGY METABOLISM; FATTY ACID OXIDATION; GLUCOSE BLOOD LEVEL; GLUCOSE OXIDATION; HEART FUNCTION; HEART MUSCLE METABOLISM; HEART VENTRICLE HYPERTROPHY; INSULIN SENSITIVITY; LIPID DIET; LOW FAT DIET; MALE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OBESITY; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TISSUE DOPPLER IMAGING; WEIGHT REDUCTION; ANIMAL; FAT INTAKE; HEART; INSULIN RESISTANCE; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; DIETARY FATS; FATTY ACIDS; HEART; HEART FAILURE, DIASTOLIC; INSULIN; INSULIN RESISTANCE; MICE; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION; WEIGHT LOSS;

EID: 84933529046     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-1050     Document Type: Article

References (70)

1. Alpert MA. Obesity cardiomyopathy: pathophysiology and evolution of the clinical syndrome. Am J Med Sci 2001;321:225-236.
2. Murphy NF, MacIntyre K, Stewart S, Hart CL, Hole D, McMurray JJ. Longterm cardiovascular consequences of obesity: 20-year follow-up of more than 15 000 middle- Aged men and women (the Renfrew-Paisley study). Eur Heart J 2006;27:96-106.
3. Gardin JM, McClelland R, Kitzman D, et al. M-mode echocardiographic predictors of six- To seven-year incidence of coronary heart disease, stroke, congestive heart failure, and mortality in an elderly cohort (the Cardiovascular Health Study). Am J Cardiol 2001;87:1051-1057.
4. Vasan RS, Larson MG, Benjamin EJ, Evans JC, Levy D. Left ventricular dilatation and the risk of congestive heart failure in people without myocardial infarction. N Engl J Med 1997;336:1350-1355.
5. Kenchaiah S, Evans JC, Levy D, et al. Obesity and the risk of heart failure. N Engl J Med 2002;347:305-313.
6. Kenchaiah S, Sesso HD, Gaziano JM. Body mass index and vigorous physical activity and the risk of heart failure among men. Circulation 2009;119: 44-52.
7. Oreopoulos A, Padwal R, Kalantar-Zadeh K, Fonarow GC, Norris CM, McAlister FA. Body mass index and mortality in heart failure: A meta- Analysis. Am Heart J 2008;156:13-22.
8. Padwal R, McAlister FA, McMurray JJ, et al.; Meta- Analysis Global Group in Chronic Heart Failure (MAGGIC). The obesity paradox in heart failure patients with preserved versus reduced ejection fraction: A meta- Analysis of individual patient data. Int J Obes (Lond) 2014;38:1110-1114.
9. Davos CH, Doehner W, Rauchhaus M, et al. Body mass and survival in patients with chronic heart failure without cachexia: The importance of obesity. J Card Fail 2003;9:29-35.
10. Lavie CJ, Osman AF, Milani RV, Mehra MR. Body composition and prognosis in chronic systolic heart failure: The obesity paradox. Am J Cardiol 2003;91:891-894.
11. Curtis JP, Selter JG, Wang Y, et al. The obesity paradox: body mass index and outcomes in patients with heart failure. Arch Intern Med 2005;165:55-61.
12. Gustafsson F, Kragelund CB, Torp-Pedersen C, et al.; DIAMOND study group. Effect of obesity and being overweight on long- Term mortality in congestive heart failure: influence of left ventricular systolic function. Eur Heart J 2005;26:58-64.
13. Shah R, Gayat E, Januzzi JL Jr, et al.; GREAT (Global Research on Acute Conditions Team) Network. Body mass index and mortality in acutely decompensated heart failure across the world: A global obesity paradox. J Am Coll Cardiol 2014;63:778-785.
14. Stanley WC, Dabkowski ER, Ribeiro RF Jr, O'Connell KA. Dietary fat and heart failure: moving from lipotoxicity to lipoprotection. Circ Res 2012;110:764- 776.
15. Alpert MA, Terry BE, Lambert CR, et al. Factors influencing left ventricular systolic function in nonhypertensive morbidly obese patients, and effect of weight loss induced by gastroplasty. Am J Cardiol 1993;71:733-737.
16. Rider OJ, Francis JM, Tyler D, Byrne J, Clarke K, Neubauer S. Effects of weight loss on myocardial energetics and diastolic function in obesity. Int J Cardiovasc Imaging 2013;29:1043-1050.
17. Lopaschuk GD, Folmes CD, Stanley WC. Cardiac energy metabolism in obesity. Circ Res 2007;101:335-347.
18. Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev 2010;90:207-258.
19. Buchanan J, Mazumder PK, 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.
20. Zhang L, Ussher JR, Oka T, Cadete VJ, Wagg C, Lopaschuk GD. Cardiac diacylglycerol accumulation in high fat-fed mice is associated with impaired insulin-stimulated glucose oxidation. Cardiovasc Res 2011;89:148-156.
21. Peterson LR, Herrero P, Schechtman KB, et al. Effect of obesity and insulin resistance on myocardial substrate metabolism and efficiency in young women. Circulation 2004;109:2191-2196.
22. Doenst T, Pytel G, Schrepper A, et al. Decreased rates of substrate oxidation ex vivo predict the onset of heart failure and contractile dysfunction in rats with pressure overload. Cardiovasc Res 2010;86:461-470.
23. Neubauer S. The failing heart- An engine out of fuel. N Engl J Med 2007; 356:1140-1151.
24. Zhang L, Jaswal JS, Ussher JR, et al. Cardiac insulin-resistance and decreased mitochondrial energy production precede the development of systolic heart failure after pressure-overload hypertrophy. Circ Heart Fail 2013;6:1039- 1048.
25. Mori J, Alrob OA, Wagg CS, Harris RA, Lopaschuk GD, Oudit GY. ANG II causes insulin resistance and induces cardiac metabolic switch and inefficiency: A critical role of PDK4. Am J Physiol Heart Circ Physiol 2013;304: H1103-H1113.
26. Mori J, Basu R, McLean BA, et al. Agonist-induced hypertrophy and diastolic dysfunction are associated with selective reduction in glucose oxidation: A metabolic contribution to heart failure with normal ejection fraction. Circ Heart Fail 2012;5:493-503.
27. Zhabyeyev P, Gandhi M, Mori J, et al. Pressure-overload-induced heart failure induces a selective reduction in glucose oxidation at physiological afterload. Cardiovasc Res 2013;97:676-685.
28. Ussher JR, Koves TR, Cadete VJ, et al. Inhibition of de novo ceramide synthesis reverses diet-induced insulin resistance and enhances whole-body oxygen consumption. Diabetes 2010;59:2453-2464.
29. Schwartz K, de la Bastie D, Bouveret P, Oliviéro P, Alonso S, Buckingham M. Alpha-skeletal muscle actin mRNA's accumulate in hypertrophied adult rat hearts. Circ Res 1986;59:551-555.
30. Brunet A, Sweeney LB, Sturgill JF, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004;303:2011- 2015.
31. Daitoku H, Hatta M, Matsuzaki H, et al. Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity. Proc Natl Acad Sci U S A 2004;101:10042-10047.
32. Motta MC, Divecha N, Lemieux M, et al. Mammalian SIRT1 represses forkhead transcription factors. Cell 2004;116:551-563.
33. Yang Y, Hou H, Haller EM, Nicosia SV, Bai W. Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J 2005;24:1021-1032.
34. Sundaresan NR, Pillai VB, Wolfgeher D, et al. The deacetylase SIRT1 promotes membrane localization and activation of Akt and PDK1 during tumorigenesis and cardiac hypertrophy. Sci Signal 2011;4:ra46.
35. Xi X, Han J, Zhang JZ. Stimulation of glucose transport by AMP- Activated protein kinase via activation of p38 mitogen- Activated protein kinase. J Biol Chem 2001;276:41029-41034.
36. Hirschey MD, Shimazu T, Goetzman E, et al. SIRT3 regulates mitochondrial fatty- Acid oxidation by reversible enzyme deacetylation. Nature 2010;464:121- 125.
37. Jing E, O'Neill BT, Rardin MJ, et al. Sirt3 regulates metabolic flexibility of skeletal muscle through reversible enzymatic deacetylation. Diabetes 2013;62: 3404-3417.
38. Zhao S, Xu W, Jiang W, et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010;327:1000-1004.
39. Alrob OA, Sankaralingam S, Ma C, et al. Obesity-induced lysine acetylation increases cardiac fatty acid oxidation and impairs insulin signalling. Cardiovasc Res 2014;103:485-497.
40. Mashili F, Chibalin AV, Krook A, Zierath JR. Constitutive STAT3 phosphorylation contributes to skeletal muscle insulin resistance in type 2 diabetes. Diabetes 2013;62:457-465.
41. Ueki K, Kondo T, Kahn CR. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol Cell Biol 2004; 24:5434-5446.
42. Emanuelli B, Peraldi P, Filloux C, et al. SOCS-3 inhibits insulin signaling and is up-regulated in response to tumor necrosis factor- Alpha in the adipose tissue of obese mice. J Biol Chem 2001;276:47944-47949.
43. Senn JJ, Klover PJ, Nowak IA, et al. Suppressor of cytokine signaling-3 (SOCS-3), a potential mediator of interleukin-6-dependent insulin resistance in hepatocytes. J Biol Chem 2003;278:13740-13746.
44. Ueki K, Kondo T, Tseng YH, Kahn CR. Central role of suppressors of cytokine signaling proteins in hepatic steatosis, insulin resistance, and the metabolic syndrome in the mouse. Proc Natl Acad Sci U S A 2004;101:10422-10427.
45. Yang Z, Hulver M, McMillan RP, et al. Regulation of insulin and leptin signaling by muscle suppressor of cytokine signaling 3 (SOCS3). PLoS ONE 2012; 7:e47493.
46. Goode N, Hughes K, Woodgett JR, Parker PJ. Differential regulation of glycogen synthase kinase-3 beta by protein kinase C isotypes. J Biol Chem 1992; 267:16878-16882.
47. Fang X, Yu SX, Lu Y, Bast RC Jr, Woodgett JR, Mills GB. Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci U S A 2000;97:11960-11965.
48. De Mesquita DD, Zhan Q, Crossley L, Badwey JA. p90-RSK and Akt may promote rapid phosphorylation/inactivation of glycogen synthase kinase 3 in chemoattractant-stimulated neutrophils. FEBS Lett 2001;502:84-88.
49. Belin de Chantemèle EJ, Mintz JD, Rainey WE, Stepp DW. Impact of leptinmediated sympatho- Activation on cardiovascular function in obese mice. Hypertension 2011;58:271-279.
50. Randle PJ, Garland PB, Hales CN, Newsholme EA. The glucose fatty- Acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1963;1:785-789.
51. Ussher JR, Koves TR, Jaswal JS, et al. Insulin-stimulated cardiac glucose oxidation is increased in high-fat diet-induced obese mice lacking malonyl CoA decarboxylase. Diabetes 2009;58:1766-1775.
52. He L, Kim T, Long Q, et al. Carnitine palmitoyltransferase-1b deficiency aggravates pressure overload-induced cardiac hypertrophy caused by lipotoxicity. Circulation 2012;126:1705-1716.
53. Kolwicz SC Jr, Olson DP, Marney LC, Garcia-Menendez L, Synovec RE, Tian R. Cardiac-specific deletion of acetyl CoA carboxylase 2 prevents metabolic remodeling during pressure-overload hypertrophy. Circ Res 2012;111:728-738.
54. Lerin C, Rodgers JT, Kalume DE, Kim SH, Pandey A, Puigserver P. GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1alpha. Cell Metab 2006;3:429-438.
55. Xiong S, Salazar G, San Martin A, et al. PGC-1 alpha serine 570 phosphorylation and GCN5-mediated acetylation by angiotensin II drive catalase down-regulation and vascular hypertrophy. J Biol Chem 2010;285:2474-2487.
56. Sinclair D, Verdin E. The longevity of sirtuins. Cell Reports 2012;2:1473- 1474.
57. Nasrin N, Wu X, Fortier E, et al. SIRT4 regulates fatty acid oxidation and mitochondrial gene expression in liver and muscle cells. J Biol Chem 2010;285: 31995-32002.
58. Suter MA, Chen A, Burdine MS, et al. A maternal high-fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates. FASEB J 2012;26:5106-5114.
59. Fang CX, Dong F, Thomas DP, Ma H, He L, Ren J. Hypertrophic cardiomyopathy in high-fat diet-induced obesity: Role of suppression of forkhead transcription factor and atrophy gene transcription. Am J Physiol Heart Circ Physiol 2008;295:H1206-H1215.
60. Ni YG, Berenji K, Wang N, et al. Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling. Circulation 2006;114:1159-1168.
61. Sandri M, Sandri C, Gilbert A, et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004;117:399-412.
62. Wang J, Liu X, Arneja AS, Dhalla NS. Alterations in protein kinase A and protein kinase C levels in heart failure due to genetic cardiomyopathy. Can J Cardiol 1999;15:683-690.
63. Takeishi Y, Bhagwat A, Ball NA, Kirkpatrick DL, Periasamy M, Walsh RA. Effect of angiotensin-converting enzyme inhibition on protein kinase C and SR proteins in heart failure. Am J Physiol 1999;276:H53-H62.
64. Shubeita HE, Martinson EA, Van Bilsen M, Chien KR, Brown JH. Transcriptional activation of the cardiac myosin light chain 2 and atrial natriuretic factor genes by protein kinase C in neonatal rat ventricular myocytes. Proc Natl Acad Sci U S A 1992;89:1305-1309.
65. Pucéat M, Vassort G. Signalling by protein kinase C isoforms in the heart. Mol Cell Biochem 1996;157:65-72.
66. Li HL, Yin R, Chen D, et al. Long- Term activation of adenosine monophosphate- Activated protein kinase attenuates pressure-overload-induced cardiac hypertrophy. J Cell Biochem 2007;100:1086-1099.
67. Dolinsky VW, Chan AY, Robillard Frayne I, Light PE, Des Rosiers C, Dyck JR. Resveratrol prevents the prohypertrophic effects of oxidative stress on LKB1. Circulation 2009;119:1643-1652.
68. Yamamoto Y, Hoshino Y, Ito T, et al. Atrogin-1 ubiquitin ligase is upregulated by doxorubicin via p38-MAP kinase in cardiac myocytes. Cardiovasc Res 2008;79:89-96.
69. Zhang G, Li YP. p38b MAPK upregulates atrogin1/MAFbx by specific phosphorylation of C/EBPb. Skelet Muscle 2012;2:20.
70. Anker SD, Negassa A, Coats AJ, et al. Prognostic importance of weight loss in chronic heart failure and the effect of treatment with angiotensin-convertingenzyme inhibitors: An observational study. Lancet 2003;361:1077-1083.