Energy metabolic reprogramming in the hypertrophied and early stage failing heart a multisystems approach

Circulation: Heart Failure

Volumn 7, Issue 6, 2014, Pages 1022-1031

  Lai, Ling ^b   Leone, Teresa C ^b   Keller, Mark P ^c   Martin, Ola J ^b   Broman, Aimee T ^d   Nigro, Jessica ^a   Kapoor, Kapil ^a   Koves, Timothy R ^e,h   Stevens, Robert ^e,h   Ilkayeva, Olga R ^e,h   Vega, Rick B ^b   Attie, Alan D ^c   Muoio, Deborah M ^e,f,g,h   Kelly, Daniel P ^b  

^a ST LUKE S ROOSEVELT HOSPITAL CENTER   (United States)

^b BURNHAM INSTITUTE   (United States)

^c Department of Biochemistry ^*  (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f Boston University Medical Center Place   (United States)

^g Pharmacology and Cancer Biology   (United States)

^h DUKE UNIVERSITY   (United States)

Author keywords

Energy metabolism; Heart failure; Metabolomics; Mitochondria; Transcriptome profiling

Indexed keywords

FATTY ACID; FATTY ACID TRANSPORTER; LONG CHAIN FATTY ACID; TRANSCRIPTOME; AMINO ACID;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; DOWN REGULATION; ENDURANCE TRAINING; ENERGY METABOLISM; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEART DILATATION; HEART EJECTION FRACTION; HEART FAILURE; HEART FUNCTION; HEART HYPERTROPHY; HEART STRESS; HEART VENTRICLE HYPERTROPHY; LEFT ANTERIOR DESCENDING CORONARY ARTERY; LIPOLYSIS; METABOLOME; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PH; PHENOTYPE; PRIORITY JOURNAL; UPREGULATION; ANIMAL; CARDIOMEGALY; DISEASE MODEL; GENETICS; HEART VENTRICLE REMODELING; LIPID METABOLISM; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

AMINO ACIDS; ANIMALS; CARDIOMEGALY; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; HEART FAILURE; LIPID METABOLISM; METABOLOME; MICE; UP-REGULATION; VENTRICULAR REMODELING;

EID: 84921837488     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.114.001469     Document Type: Article

References (45)

1. Bing RJ. The metabolism of the heart. Harvey Lect. 1954;50:27-70.
2. Bishop SP, Altschuld RA. Increased glycolytic metabolism in cardiac hypertrophy and congestive failure. Am J Physiol. 1970;218:153-159.
3. Allard MF, Schönekess BO, Henning SL, English DR, Lopaschuk GD. Contribution of oxidative metabolism and glycolysis to ATP production in hypertrophied hearts. Am J Physiol. 1994;267(2 Pt 2):H742-H750.
4. Christe ME, Rodgers RL. Altered glucose and fatty acid oxidation in hearts of the spontaneously hypertensive rat. J Mol Cell Cardiol. 1994;26:1371-1375.
5. Taegtmeyer H, Golfman L, Sharma S, Razeghi P, van Arsdall M. Linking gene expression to function: metabolic flexibility in the normal and diseased heart. Ann N Y Acad Sci. 2004;1015:202-213.
6. Huss JM, Kelly DP. Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest. 2005;115:547-555.
7. Stanley WC, Recchia FA, Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev. 2005;85:1093-1129.
8. Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010;90:207-258.
9. Ingwall JS, Atkinson DE, Clarke K, Fetters JK. Energetic correlates of cardiac failure: changes in the creatine kinase system in the failing myocardium. Eur Heart J. 1990;11 Suppl B:108-115.
10. Tian R, Nascimben L, Kaddurah-Daouk R, Ingwall JS. Depletion of energy reserve via the creatine kinase reaction during the evolution of heart failure in cardiomyopathic hamsters. J Mol Cell Cardiol. 1996;28:755-765.
11. Neubauer S, Horn M, Cramer M, Harre K, Newell JB, Peters W, Pabst T, Ertl G, Hahn D, Ingwall JS, Kochsiek K. Myocardial phosphocreatineto-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation. 1997;96:2190-2196.
12. Weiss RG, Gerstenblith G, Bottomley PA. ATP flux through creatine kinase in the normal, stressed, and failing human heart. Proc Natl Acad Sci U S A. 2005;102:808-813.
13. Ingwall JS. On the hypothesis that the failing heart is energy starved: lessons learned from the metabolism of ATP and creatine. Curr Hypertens Rep. 2006;8:457-464.
14. Kelly DP, Strauss AW. Inherited cardiomyopathies. N Engl J Med. 1994;330:913-919.
15. Bennett MJ, Rinaldo P, Strauss AW. Inborn errors of mitochondrial fatty acid oxidation. Crit Rev Clin Lab Sci. 2000;37:1-44.
16. Wallace DC. Mitochondrial defects in cardiomyopathy and neuromuscular disease. Am Heart J. 2000;139(2 Pt 3):S70-S85.
17. Huss JM, Imahashi K, Dufour CR, Weinheimer CJ, Courtois M, Kovacs A, Giguère V, Murphy E, Kelly DP. The nuclear receptor ERRalpha is required for the bioenergetic and functional adaptation to cardiac pressure overload. Cell Metab. 2007;6:25-37.
18. Sack MN, Rader TA, Park S, Bastin J, McCune SA, Kelly DP. Fatty acid oxidation enzyme gene expression is downregulated in the failing heart. Circulation. 1996;94:2837-2842.
19. Sack MN, Disch DL, Rockman HA, Kelly DP. A role for Sp and nuclear receptor transcription factors in a cardiac hypertrophic growth program. Proc Natl Acad Sci U S A. 1997;94:6438-6443.
20. Barger PM, Brandt JM, Leone TC, Weinheimer CJ, Kelly DP. Deactivation of peroxisome proliferator-activated receptor-alpha during cardiac hypertrophic growth. J Clin Invest. 2000;105:1723-1730.
21. Kanda H, Nohara R, Hasegawa K, Kishimoto C, Sasayama S. A nuclear complex containing PPARalpha/RXRalpha is markedly downregulated in the hypertrophied rat left ventricular myocardium with normal systolic function. Heart Vessels. 2000;15:191-196.
22. Sihag S, Cresci S, Li AY, Sucharov CC, Lehman JJ. PGC-1alpha and ERRalpha target gene downregulation is a signature of the failing human heart. J Mol Cell Cardiol. 2009;46:201-212.
23. Gao Z, Xu H, DiSilvestre D, Halperin VL, Tunin R, Tian Y, Yu W, Winslow RL, Tomaselli GF. Transcriptomic profiling of the canine tachycardia-induced heart failure model: global comparison to human and murine heart failure. J Mol Cell Cardiol. 2006;40:76-86.
24. Bugger H, Schwarzer M, Chen D, Schrepper A, Amorim PA, Schoepe M, Nguyen TD, Mohr FW, Khalimonchuk O, Weimer BC, Doenst T. Proteomic remodelling of mitochondrial oxidative pathways in pressure overload-induced heart failure. Cardiovasc Res. 2010;85:376-384.
25. Barth AS, Kumordzie A, Frangakis C, Margulies KB, Cappola TP, Tomaselli GF. Reciprocal transcriptional regulation of metabolic and signaling pathways correlates with disease severity in heart failure. Circ Cardiovasc Genet. 2011;4:475-483.
26. Xu J, Nie HG, Zhang XD, Tian Y, Yu B. Down-regulated energy metabolism genes associated with mitochondria oxidative phosphorylation and fatty acid metabolism in viral cardiomyopathy mouse heart. Mol Biol Rep. 2011;38:4007-4013.
27. Allen DL, Harrison BC, Maass A, Bell ML, Byrnes WC, Leinwand LA. Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse. J Appl Physiol (1985). 2001;90:1900-1908.
28. Martin OJ, Lai L, Soundarapandian MM, Leone TC, Zorzano A, Keller MP, Attie AD, Muoio DM, Kelly DP. A role for peroxisome proliferatoractivated receptor γ coactivator-1 in the control of mitochondrial dynamics during postnatal cardiac growth. Circ Res. 2014;114:626-636.
29. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005;1:361-370.
30. Finck BN, Kelly DP. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest. 2006;116:615-622.
31. Handschin C, Spiegelman BM. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev. 2006;27:728-735.
32. Scarpulla RC, Vega RB, Kelly DP. Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab. 2012;23:459-466.
33. Sansbury BE, DeMartino AM, Xie Z, Brooks AC, Brainard RE, Watson LJ, DeFilippis AP, Cummins TD, Harbeson MA, Brittian KR, Prabhu SD, Bhatnagar A, Jones SP, Hill BG. Metabolomic analysis of pressure-overloaded and infarcted mouse hearts. Circ Heart Fail. 2014;7:634-642.
34. Galindo CL, Skinner MA, Errami M, Olson LD, Watson DA, Li J, McCormick JF, McIver LJ, Kumar NM, Pham TQ, Garner HR. Transcriptional profile of isoproterenol-induced cardiomyopathy and comparison to exercise-induced cardiac hypertrophy and human cardiac failure. BMC Physiol. 2009;9:23.
35. Iemitsu M, Maeda S, Miyauchi T, Matsuda M, Tanaka H. Gene expression profiling of exercise-induced cardiac hypertrophy in rats. Acta Physiol Scand. 2005;185:259-270.
36. Strøm CC, Aplin M, Ploug T, Christoffersen TE, Langfort J, Viese M, Galbo H, Haunsø S, Sheikh SP. Expression profiling reveals differences in metabolic gene expression between exercise-induced cardiac effects and maladaptive cardiac hypertrophy. FEBS J. 2005;272:2684-2695.
37. Diffee GM, Seversen EA, Stein TD, Johnson JA. Microarray expression analysis of effects of exercise training: increase in atrial MLC-1 in rat ventricles. Am J Physiol Heart Circ Physiol. 2003;284:H830-H837.
38. Budiono BP, See Hoe LE, Peart JN, Sabapathy S, Ashton KJ, Haseler LJ, Headrick JP. Voluntary running in mice beneficially modulates myocardial ischemic tolerance, signaling kinases, and gene expression patterns. Am J Physiol Regul Integr Comp Physiol. 2012;302:R1091-R1100.
39. Hirschey MD, Shimazu T, Huang JY, Verdin E. Acetylation of mitochondrial proteins. Methods Enzymol. 2009;457:137-147.
40. Cai L, Tu BP. On acetyl-CoA as a gauge of cellular metabolic state. Cold Spring Harb Symp Quant Biol. 2011;76:195-202.
41. Newman JC, He W, Verdin E. Mitochondrial protein acylation and intermediary metabolism: regulation by sirtuins and implications for metabolic disease. J Biol Chem. 2012;287:42436-42443.
42. Karamanlidis G, Lee CF, Garcia-Menendez L, Kolwicz SC Jr, Suthammarak W, Gong G, Sedensky MM, Morgan PG, Wang W, Tian R. Mitochondrial complex I deficiency increases protein acetylation and accelerates heart failure. Cell Metab. 2013;18:239-250.
43. Mills E, O'Neill LA. Succinate: a metabolic signal in inflammation. Trends Cell Biol. 2014;24:313-320.
44. Rardin MJ, He W, Nishida Y, Newman JC, Carrico C, Danielson SR, Guo A, Gut P, Sahu AK, Li B, Uppala R, Fitch M, Riiff T, Zhu L, Zhou J, Mulhern D, Stevens RD, Ilkayeva OR, Newgard CB, Jacobson MP, Hellerstein M, Goetzman ES, Gibson BW, Verdin E. SIRT5 regulates the mitochondrial lysine succinylome and metabolic networks. Cell Metab. 2013;18:920-933.
45. Park J, Chen Y, Tishkoff DX, Peng C, Tan M, Dai L, Xie Z, Zhang Y, Zwaans BM, Skinner ME, Lombard DB, Zhao Y. SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways. Mol Cell. 2013;50:919-930.