Agonist-induced hypertrophy and diastolic dysfunction are associated with selective reduction in glucose oxidation a metabolic contribution to heart failure with normal ejection fraction

Circulation: Heart Failure

Volumn 5, Issue 4, 2012, Pages 493-503

  Mori, Jun ^a,b   Basu, Ratnadeep ^a,b   McLean, Brent A ^a,b   Das, Subhash K ^a,c   Zhang, Liyan ^b   Patel, Vaibhav B ^b   Wagg, Cory S ^b   Kassiri, Zamaneh ^c   Lopaschuk, Gary D ^a   Oudit, Gavin Y ^c  

^a Department of Pediatrics and Pharmacology ^*  (Canada)

^b MAZANKOWSKI ALBERTA HEART INSTITUTE   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Angiotensin II; Cardiac metabolism; Diastolic dysfunction; Heart failure; Phenylephrine; Pyruvate dehydrogense 4

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR; CARBOHYDRATE; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE RETINOBLASTOMA PROTEIN E2F; IRBESARTAN; PHENYLEPHRINE; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE KINASE 4; TRICARBOXYLIC ACID; TRICARBOXYLIC ACID ACETYL COENZYME A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DISEASE ASSOCIATION; ECHOCARDIOGRAPHY; ENERGY METABOLISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SYNTHESIS; FATTY ACID OXIDATION; GLUCOSE OXIDATION; GLYCOLYSIS; HEART EJECTION FRACTION; HEART FAILURE; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE METABOLISM; LACTIC ACID OXIDATION; MALE; MOUSE; NONHUMAN; OSMOTIC PUMP; OXIDATION KINETICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYSTOLE; UPREGULATION;

ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; CARDIOMEGALY; CYCLIN-DEPENDENT KINASES; E2F TRANSCRIPTION FACTORS; ENERGY METABOLISM; GLUCOSE; HEART FAILURE; MALE; MICE; MICE, INBRED C57BL; MYOCARDIUM; OXIDATION-REDUCTION; PHENYLEPHRINE; PROTEIN-SERINE-THREONINE KINASES; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTORS, ADRENERGIC, ALPHA; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; STROKE VOLUME; TIME FACTORS; VENTRICULAR FUNCTION;

EID: 84864609802     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.112.966705     Document Type: Article

References (54)

1. The SOLVD Investigators. Effect of enalapril on survival in patients with reduced left ventricular ejection fractions and congestive heart failure. N Engl J Med. 1991;325:293-302.
2. Granger CB, McMurray JJ, Yusuf S, Held P, Michelson EL, Olofsson B, Ostergren J, Pfeffer MA, Swedberg K; CHARM Investigators and Committees. Effects of candesartan in patients with chronic heart failure and reduced left-ventricular systolic function intolerant to angiotensin-converting-enzyme inhibitors: the CHARM-Alternative trial. Lancet. 2003;362:772-776.
3. Weber KT, Brilla CG. Pathological hypertrophy and cardiac interstitium. Fibrosis and renin-angiotensin-aldosterone system. Circulation. 1991;83:1849-1865.
4. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol. 2007;292:C82-C97.
5. Jensen BC, O'Connell TD, Simpson PC. Alpha-1-adrenergic receptors: targets for agonist drugs to treat heart failure. J Mol Cell Cardiol. 2011;51:518-528.
6. Zile MR, Brutsaert DL. New concepts in diastolic dysfunction and diastolic heart failure: Part I: diagnosis, prognosis, and measurements of diastolic function. Circulation. 2002;105:1387-1393.
7. Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med. 2006;355:251-259.
8. Paulus WJ, Tschöpe C, Sanderson JE, Rusconi C, Flachskampf FA, Rademakers FE, Marino P, Smiseth OA, De Keulenaer G, Leite-Moreira AF, Borbély A, Edes I, Handoko ML, Heymans S, Pezzali N, Pieske B, Dickstein K, Fraser AG, Brutsaert DL. How to diagnose diastolic heart failure: a consensus statement on the diagnosis of heart failure with normal left ventricular ejection fraction by the Heart Failure and Echocardiography Associations of the European Society of Cardiology. Eur Heart J. 2007;28:2539-2550.
9. Paulus WJ, van Ballegoij JJ. Treatment of heart failure with normal ejection fraction: an inconvenient truth! J Am Coll Cardiol. 2010;55: 526-537.
10. Neubauer S. The failing heart-an engine out of fuel. N Engl J Med. 2007;356:1140-1151.
11. Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010;90:207-258.
12. Lei B, Lionetti V, Young ME, Chandler MP, d'Agostino C, Kang E, Altarejos M, Matsuo K, Hintze TH, Stanley WC, Recchia FA. Paradoxical downregulation of the glucose oxidation pathway despite enhanced flux in severe heart failure. J Mol Cell Cardiol. 2004;36:567-576.
13. Pellieux C, Aasum E, Larsen TS, Montessuit C, Papageorgiou I, Pedrazzini T, Lerch R. Overexpression of angiotensinogen in the myocardium induces downregulation of the fatty acid oxidation pathway. J Mol Cell Cardiol. 2006;41:459-466.
14. Pellieux C, Montessuit C, Papageorgiou I, Lerch R. Angiotensin II downregulates the fatty acid oxidation pathway in adult rat cardiomyocytes via release of tumour necrosis factor-alpha. Cardiovasc Res. 2009;82:341-350.
15. Stuck BJ, Lenski M, Böhm M, Laufs U. Metabolic switch and hypertrophy of cardiomyocytes following treatment with angiotensin II are prevented by AMP-activated protein kinase. J Biol Chem. 2008;283:32562-32569.
16. Tian R, Nascimben L, Ingwall JS, Lorell BH. Failure to maintain a low ADP concentration impairs diastolic function in hypertrophied rat hearts. Circulation. 1997;96:1313-1319.
17. Lamb HJ, Beyerbacht HP, van der Laarse A, Stoel BC, Doornbos J, van der Wall EE, de Roos A. Diastolic dysfunction in hypertensive heart disease is associated with altered myocardial metabolism. Circulation. 1999;99:2261-2267.
18. Zhong J, Basu R, Guo D, Chow FL, Byrns S, Schuster M, Loibner H, Wang XH, Penninger JM, Kassiri Z, Oudit GY. Angiotensin-converting enzyme 2 suppresses pathological hypertrophy, myocardial fibrosis, and cardiac dysfunction. Circulation. 2010;122:717-728.
19. Dyck JR, Cheng JF, Stanley WC, Barr R, Chandler MP, Brown S, Wallace D, Arrhenius T, Harmon C, Yang G, Nadzan AM, Lopaschuk GD. Malonyl coenzyme a decarboxylase inhibition protects the ischemic heart by inhibiting fatty acid oxidation and stimulating glucose oxidation. Circ Res. 2004;94:e78-e84.
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. Constantin-Teodosiu D, Cederblad G, Hultman E. A sensitive radioisotopic assay of pyruvate dehydrogenase complex in human muscle tissue. Anal Biochem. 1991;198:347-351.
22. Guo D, Kassiri Z, Basu R, Chow FL, Kandalam V, Damilano F, Liang W, Izumo S, Hirsch E, Penninger JM, Backx PH, Oudit GY. Loss of PI3K? enhances cAMP-dependent MMP remodeling of the myocardial N-cadherin adhesion complexes and extracellular matrix in response to early biomechanical stress. Circ Res. 2010;107:1275-1289.
23. Ussher JR, Koves TR, Jaswal JS, Zhang L, Ilkayeva O, Dyck JR, Muoio DM, Lopaschuk GD. Insulin-stimulated cardiac glucose oxidation is increased in high-fat diet-induced obese mice lacking malonyl CoA decarboxylase. Diabetes. 2009;58:1766-1775.
24. Zaman MA, Oparil S, Calhoun DA. Drugs targeting the renin-angiotensin- aldosterone system. Nat Rev Drug Discov. 2002;1:621-636.
25. Zile MR, Brutsaert DL. New concepts in diastolic dysfunction and diastolic heart failure: Part II: causal mechanisms and treatment. Circulation. 2002;105:1503-1508.
26. Stavinoha MA, RaySpellicy JW, Essop MF, Graveleau C, Abel ED, Hart-Sailors ML, Mersmann HJ, Bray MS, Young ME. Evidence for mitochondrial thioesterase 1 as a peroxisome proliferator-activated receptor-alpha-regulated gene in cardiac and skeletal muscle. Am J Physiol Endocrinol Metab. 2004;287:E888-E895.
27. Sugden MC, Bulmer K, Holness MJ. Fuel-sensing mechanisms integrating lipid and carbohydrate utilization. Biochem Soc Trans. 2001;29: 272-278.
28. Zhang Y, Ma K, Sadana P, Chowdhury F, Gaillard S, Wang F, McDonnell DP, Unterman TG, Elam MB, Park EA. Estrogen-related receptors stimulate pyruvate dehydrogenase kinase isoform 4 gene expression. J Biol Chem. 2006;281:39897-39906.
29. Aguilar V, Fajas L. Cycling through metabolism. EMBO Mol Med. 2010;2:338-348.
30. Sugden MC, Holness MJ. Mechanisms underlying regulation of the expression and activities of the mammalian pyruvate dehydrogenase kinases. Arch Physiol Biochem. 2006;112:139-149.
31. Stanley WC, Recchia FA, Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev. 2005;85:1093-1129.
32. Sugden MC, Holness MJ. Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab. 2003;284:E855-E862.
33. Arikawa E, Ma RC, Isshiki K, Luptak I, He Z, Yasuda Y, Maeno Y, Patti ME, Weir GC, Harris RA, Zammit VA, Tian R, King GL. Effects of insulin replacements, inhibitors of angiotensin, and PKC?'s actions to normalize cardiac gene expression and fuel metabolism in diabetic rats. Diabetes. 2007;56:1410-1420.
34. Chambers KT, Leone TC, Sambandam N, Kovacs A, Wagg CS, Lopaschuk GD, Finck BN, Kelly DP. Chronic inhibition of pyruvate dehy- drogenase in heart triggers an adaptive metabolic response. J Biol Chem. 2011;286:11155-11162.
35. Kannel WB, Hjortland M, Castelli WP. Role of diabetes in congestive heart failure: the Framingham study. Am J Cardiol. 1974;34:29-34.
36. Thrainsdottir IS, Aspelund T, Thorgeirsson G, Gudnason V, Hardarson T, Malmberg K, Sigurdsson G, Rydén L. The association between glucose abnormalities and heart failure in the population-based Reykjavik study. Diabetes Care. 2005;28:612-616.
37. Csibi A, Communi D, Müller N, Bottari SP. Angiotensin II inhibits insulin- stimulated GLUT4 translocation and Akt activation through tyrosine nitration-dependent mechanisms. PLoS ONE. 2010;5:e10070.
38. Weber CR, Piacentino V 3rd, Houser SR, Bers DM. Dynamic regulation of sodium/calcium exchange function in human heart failure. Circulation. 2003;108:2224-2229.
39. Nakamura TY, Iwata Y, Arai Y, Komamura K, Wakabayashi S. Activation of Na+/H+ exchanger 1 is sufficient to generate Ca2+ signals that induce cardiac hypertrophy and heart failure. Circ Res. 2008;103:891-899.
40. Doughan AK, Harrison DG, Dikalov SI. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res. 2008;102:488-496.
41. Dai DF, Johnson SC, Villarin JJ, Chin MT, Nieves-Cintrón M, Chen T, Marcinek DJ, Dorn GW 2nd, Kang YJ, Prolla TA, Santana LF, Rabinovitch PS. Mitochondrial oxidative stress mediates angiotensin II-induced cardiac hypertrophy and Galphaq overexpression-induced heart failure. Circ Res. 2011;108:837-846.
42. Schupp M, Janke J, Clasen R, Unger T, Kintscher U. Angiotensin type 1 receptor blockers induce peroxisome proliferator-activated receptor-gamma activity. Circulation. 2004;109:2054-2057.
43. de Cavanagh EM, Inserra F, Ferder L. Angiotensin II blockade: a strategy to slow ageing by protecting mitochondria? Cardiovasc Res. 2011;89:31-40.
44. Abozguia K, Elliott P, McKenna W, Phan TT, Nallur-Shivu G, Ahmed I, Maher AR, Kaur K, Taylor J, Henning A, Ashrafian H, Watkins H, Frenneaux M. Metabolic modulator perhexiline corrects energy deficiency and improves exercise capacity in symptomatic hypertrophic cardiomyopathy. Circulation. 2010;122:1562-1569.
45. Nozato T, Ito H, Tamamori M, Adachi S, Abe S, Marumo F, Hiroe M. G1 cyclins are involved in the mechanism of cardiac myocyte hypertrophy induced by angiotensin II. Jpn Circ J. 2000;64:595-601.
46. Vara D, Bicknell KA, Coxon CH, Brooks G. Inhibition of E2F abrogates the development of cardiac myocyte hypertrophy. J Biol Chem. 2003;278:21388-21394.
47. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 1998;12:3499-3511.
48. Alt JR, Cleveland JL, Hannink M, Diehl JA. Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes Dev. 2000;14:3102-3114.
49. Busk PK, Bartkova J, Strm CC, Wulf-Andersen L, Hinrichsen R, Christoffersen TE, Latella L, Bartek J, Hauns S, Sheikh SP. Involvement of cyclin D activity in left ventricle hypertrophy in vivo and in vitro. Cardiovasc Res. 2002;56:64-75.
50. Busk PK, Hinrichsen R. Cyclin D in left ventricle hypertrophy. Cell Cycle. 2003;2:91-95.
51. Wohlschlaeger J, Schmitz KJ, Takeda A, Takeda N, Vahlhaus C, Stypmann J, Schmid C, Baba HA. Reversible regulation of the retinoblastoma protein/E2F-1 pathway during "reverse cardiac remodelling" after ventricular unloading. J Heart Lung Transplant. 2010;29:117-124.
52. Hlaing M, Spitz P, Padmanabhan K, Cabezas B, Barker CS, Bernstein HS. E2F-1 regulates the expression of a subset of target genes during skeletal myoblast hypertrophy. J Biol Chem. 2004;279:43625-43633.
53. Hsieh MC, Das D, Sambandam N, Zhang MQ, Nahlé Z. Regulation of the PDK4 isozyme by the Rb-E2F1 complex. J Biol Chem. 2008;283:27410-27417.
54. Jaswal JS, Keung W, Wang W, Ussher JR, Lopaschuk GD. Targeting fatty acid and carbohydrate oxidation-a novel therapeutic intervention in the ischemic and failing heart. Biochim Biophys Acta. 2011;1813: 1333-1350.