Rethinking cardiac metabolism: Metabolic cycles to refuel and rebuild the failing heart

F1000Prime Reports

Volumn 6, Issue , 2014, Pages

  Taegtmeyer, Heinrich ^a   Lubrano, Genna ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONCEPTUAL FRAMEWORK; ENERGY CONVERSION; ENERGY METABOLISM; ENERGY TRANSFER; ENZYME ACTIVITY; HEART CONTRACTION; HEART CYCLE; HEART FAILURE; HEART MUSCLE METABOLISM; HOMEOSTASIS; HUMAN; MALNUTRITION; METABOLIC CYCLE; METABOLIC PARAMETERS; METABOLIC REGULATION; METABOLIC STRESS; MUSCLE REGENERATION; NONHUMAN; NUTRIENT SUPPLY; OVERNUTRITION; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; REVIEW;

EID: 84908233371     PISSN: 20517599     EISSN: 20517599     Source Type: Journal    
DOI: 10.12703/P6-90     Document Type: Review

References (78)

1. Taegtmeyer H, Hems R, Krebs HA: Utilization of energy-providing substrates in the isolated working rat heart. Biochem J 1980, 186:701-11.
2. 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, 1:785-9.
3. Hue L, Taegtmeyer H: The Randle cycle revisited: a new head for an old hat. Am J Physiol Endocrinol Metab 2009, 297:E578-91.
4. Taegtmeyer H: Carbohydrate interconversions and energy production. Circulation 1985, 72:IV1-8.
5. Taegtmeyer H: Energy metabolism of the heart: from basic concepts to clinical applications. Curr Probl Cardiol 1994, 19:59-113.
6. Scarpulla RC, Vega RB, Kelly DP: Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab 2012, 23:459-66.
7. Gropler RJ: Recent advances in metabolic imaging. J Nucl Cardiol 2013, 20:1147-72.
8. Depre C, Taegtmeyer H: Metabolic aspects of programmed cell survival and cell death in the heart. Cardiovasc Res 2000, 45:538-48.
9. Young ME, McNulty P, Taegtmeyer H: Adaptation and maladaptation of the heart in diabetes: Part II: potential mechanisms. Circulation 2002, 105:1861-70.
10. Taegtmeyer H, Stanley WC: Too much or not enough of a good thing? Cardiac glucolipotoxicity versus lipoprotection. J Mol Cell Cardiol 2011, 50:2-5.
11. Taegtmeyer H: Cardiac metabolism as a target for the treatment of heart failure. Circulation 2004, 110:894-6.
12. Beadle RM, Frenneaux M: Modification of myocardial substrate utilisation: a new therapeutic paradigm in cardiovascular disease. Heart 2010, 96:824-30.
13. Gorlin R: Coronary artery disease. Philadelphia: W.B. Saunders Co; 1976.
14. Neubauer S: The failing heart-an engine out of fuel. N Engl J Med 2007, 356:1140-51.
15. Dinicolantonio JJ, Lavie CJ, Niazi AK, O'Keefe JH, Hu T: Effects of thiamine on cardiac function in patients with systolic heart failure: systematic review and metaanalysis of randomized, double-blind, placebo-controlled trials. Ochsner J 2013, 13:495-9.
16. Roe CR, Sweetman L, Roe DS, David F, Brunengraber H: Treatment of cardiomyopathy and rhabdomyolysis in long-chain fat oxidation disorders using an anaplerotic odd-chain triglyceride. J Clin Invest 2002, 110:259-69.
17. Bohles H, Sewell AC: Metabolic cardiomyopathy. Stuttgart: Medpharm Scientific Publishers; 2004.
18. Taegtmeyer H: The failing heart. N Engl J Med 2007, 356:2545-6; author reply 2546.
19. Lincoff AM, Wolski K, Nicholls SJ, Nissen SE: Pioglitazone and risk of cardiovascular events in patients with type 2 diabetes mellitus: a meta-analysis of randomized trials. JAMA 2007, 298:1180-8.
20. Singh S, Loke YK, Furberg CD: Long-term risk of cardiovascular events with rosiglitazone: a meta-analysis. JAMA 2007, 298:1189-95.
21. Graham DJ, Ouellet-Hellstrom R, MaCurdy TE, Ali F, Sholley C, Worrall C, Kelman JA: Risk of acutemyocardial infarction, stroke, heart failure, and death in elderly Medicare patients treated with rosiglitazone or pioglitazone. JAMA 2010, 304:411-8.
22. Selker HP, Beshansky JR, Sheehan PR, Massaro JM, Griffith JL, D'Agostino RB, Ruthazer R, Atkins JM, Sayah AJ, Levy MK, Richards ME, Aufderheide TP, Braude DA, Pirrallo RG, Doyle DD, Frascone RJ, Kosiak DJ, Leaming JM, Van Gelder, Carin M, Walter G, Wayne MA, Woolard RH, Opie LH, Rackley CE, Apstein CS, Udelson JE: Out-of-hospital administration of intravenous glucose-insulin-potassium in patients with suspected acute coronary syndromes: the IMMEDIATE randomized controlled trial. JAMA 2012, 307:1925-33.
23. Schoenheimer R: The dynamic state of body constituents. Cambridge, MA: Harvard University Press; 1942.
24. Waterlow JC, Garlick PJ, Millward DJ: Protein turnover in mammalian tissues and in the whole body. Amsterdam: North-Holland Publishing Company; 1978.
25. Razeghi P, Taegtmeyer H: Cardiac remodeling: UPS lost in transit. Circ Res 2005, 97:964-6.
26. Lehninger AL: Biochemistry. New York: Worth Publishers; 1970.
27. Taegtmeyer H: Tracing cardiac metabolism in vivo: one substrate at a time. J Nucl Med 2010, 51Suppl 1:80S-87S.
28. Baldwin JE, Krebs H: The evolution of metabolic cycles. Nature 1981, 291:381-2.
29. Racker E: Energy cycles in health and disease. Curr Top Cell Regul 1981, 18:361-76.
30. Brown GC: Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem J 1992, 284 (Pt 1):1-13.
31. Carley AN, Taegtmeyer H, Lewandowski ED: Matrix revisited: mechanisms linking energy substrate metabolism to the function of the heart. Circ Res 2014, 114:717-29.
32. Razeghi P, Myers TJ, Frazier OH, Taegtmeyer H: Reverse remodeling of the failing human heart with mechanical unloading. Emerging concepts and unanswered questions. Cardiology 2002, 98:167-74.
33. Gupte AA, Hamilton DJ, Cordero-Reyes AM, Youker KA, Yin Z, Estep JD, Stevens RD, Wenner B, Ilkayeva O, Loebe M, Peterson LE, Lyon CJ, Wong, Stephen T C, Newgard CB, Torre-Amione G, Taegtmeyer H, Hsueh WA: Mechanical unloading promotes myocardial energy recovery in human heart failure. Circ Cardiovasc Genet 2014, 7:266-76.
34. Chokshi A, Drosatos K, Cheema FH, Ji R, Khawaja T, Yu S, Kato T, Khan R, Takayama H, Knöll R, Milting H, Chung CS, Jorde U, Naka Y, Mancini DM, Goldberg IJ, Schulze PC: Ventricular assist device implantation corrects myocardial lipotoxicity, reverses insulin resistance, and normalizes cardiac metabolism in patients with advanced heart failure. Circulation 2012, 125:2844-53.
35. Cordero-Reyes AM, Gupte AA, Youker KA, Loebe M, Hsueh WA, Torre-Amione G, Taegtmeyer H, Hamilton DJ: Freshly isolated mitochondria from failing human hearts exhibit preserved respiratory function. J Mol Cell Cardiol 2014, 68:98-105.
36. Müller J, Wallukat G, Weng YG, Dandel M, Spiegelsberger S, Semrau S, Brandes K, Theodoridis V, Loebe M, Meyer R, Hetzer R: Weaning from mechanical cardiac support in patients with idiopathic dilated cardiomyopathy. Circulation 1997, 96:542-9.
37. Hill JA, Olson EN: Cardiac plasticity. N Engl J Med 2008, 358:1370-80.
38. Wang X, Robbins J: Heart failure and protein quality control. Circ Res 2006, 99:1315-28.
39. Del Monte F, Hajjar RJ: Intracellular devastation in heart failure. Heart Fail Rev 2008, 13:151-62.
40. Willis MS, Patterson C: Proteotoxicity and cardiac dysfunction-Alzheimer's disease of the heart? N Engl J Med 2013, 368:455-64.
41. Chien KR: Regenerative medicine and human models of human disease. Nature 2008, 453:302-5.
42. Mazhari R, Hare JM: Translational findings from cardiovascular stem cell research. Trends Cardiovasc Med 2012, 22:1-6.
43. Anversa P, Kajstura J, Rota M, Leri A: Regenerating new heart with stem cells. J Clin Invest 2013, 123:62-70.
44. Sabbah HN, Sharov VG, Goldstein S: Cell death, tissue hypoxia and the progression of heart failure. Heart Fail Rev 2000, 5:131-8.
45. Sanganalmath SK, Bolli R: Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res 2013, 113:810-34.
46. Hsieh, Patrick C H, Segers, Vincent F M, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT: Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 2007, 13:970-4.
47. Cannon WB: The wisdom of the body. New York: W.W. Norton and Company; 1932.
48. Gross CG: Claude bernard and the constancy of the internal environment. Neuroscientist 1998, 4:380-5.
49. Thomas L: The lives of a cell: Notes of a biology watcher. New York: Viking Press; 1974.
50. Samarel AM, Parmacek MS, Magid NM, Decker RS, Lesch M: Protein synthesis and degradation during starvation-induced cardiac atrophy in rabbits. Circ Res 1987, 60:933-41.
51. Sharma S, Guthrie PH, Chan SS, Haq S, Taegtmeyer H: Glucose phosphorylation is required for insulin-dependent mTOR signalling in the heart. Cardiovasc Res 2007, 76:71-80.
52. Proud CG: mTORC1 regulates the efficiency and cellular capacity for protein synthesis. Biochem Soc Trans 2013, 41:923-6.
53. Sen S, Kundu BK, Wu HC, Hashmi SS, Guthrie P, Locke LW, Roy RJ, Matherne GP, Berr SS, Terwelp M, Scott B, Carranza S, Frazier OH, Glover DK, Dillmann WH, Gambello MJ, Entman ML, Taegtmeyer H: Glucose regulation of load-induced mTOR signaling and ER stress in mammalian heart. J Am Heart Assoc 2013, 2:e004796.
54. Kochel PJ, Kira Y, Gordon EE, Morgan HE: Effects of noncarbohydrate substrates on protein synthesis in hearts from fed and fasted rats. J Mol Cell Cardiol 1984, 16:371-83.
55. Harmancey R, Wilson CR, Taegtmeyer H: Adaptation and maladaptation of the heart in obesity. Hypertension 2008, 52:181-7.
56. Morgan HE, Earl DC, Broadus A, Wolpert EB, Giger KE, Jefferson LS: Regulation of protein synthesis in heart muscle. I. Effect of amino acid levels on protein synthesis. J Biol Chem 1971, 246:2152-62.
57. Cahill GF: Starvation in man. N Engl J Med 1970, 282:668-75.
58. Crawford PA, Crowley JR, Sambandam N, Muegge BD, Costello EK, Hamady M, Knight R, Gordon JI: Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. Proc Natl Acad Sci USA 2009, 106:11276-81.
59. Wentz AE, d'Avignon DA, Weber ML, Cotter DG, Doherty JM, Kerns R, Nagarajan R, Reddy N, Sambandam N, Crawford PA: Adaptation of myocardial substrate metabolism to a ketogenic nutrient environment. J Biol Chem 2010, 285:24447-56.
60. Cotter DG, Schugar RC, Crawford PA: Ketone body metabolism and cardiovascular disease. Am J Physiol Heart Circ Physiol 2013, 304:H1060-76.
61. Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill GF: Brain metabolism during fasting. J Clin Invest 1967, 46:1589-95.
62. Taegtmeyer H: On the inability of ketone bodies to serve as the only energy providing substrate for rat heart at physiological work load. Basic Res Cardiol 1983, 78:435-50.
63. Russell RR, Mrus JM, Mommessin JI, Taegtmeyer H: Compartmentation of hexokinase in rat heart. A critical factor for tracer kinetic analysis of myocardial glucose metabolism. J Clin Invest 1992, 90:1972-7.
64. Kim AS, Miller EJ, Young LH: AMP-activated protein kinase: a core signalling pathway in the heart. Acta Physiol (Oxf) 2009, 196:37-53.
65. Hardie DG, Carling D: The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur J Biochem 1997, 246:259-73.
66. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS: AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 2002, 277:23977-80.
67. Bungard D, Fuerth BJ, Zeng P, Faubert B, Maas NL, Viollet B, Carling D, Thompson CB, Jones RG, Berger SL: Signaling kinase AMPK activates stress-promoted transcription via histone H2B phosphorylation. Science 2010, 329:1201-5.
68. McGee SL, van Denderen, Bryce J W, Howlett KF, Mollica J, Schertzer JD, Kemp BE, Hargreaves M: AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 2008, 57:860-7.
69. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J: Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 2007, 100:914-22.
70. Baskin KK, Taegtmeyer H: AMP-activated protein kinase regulates E3 ligases in rodent heart. Circ Res 2011, 109:1153-61.
71. Baskin KK, Taegtmeyer H: An expanded role for AMP-activated protein kinase: regulator of myocardial protein degradation. Trends Cardiovasc Med 2011, 21:124-7.
72. Baskin KK, Rodriguez MR, Kansara S, Chen W, Carranza S, Frazier OH, Glass DJ, Taegtmeyer H: MAFbx/Atrogin-1 is required for atrophic remodeling of the unloaded heart. J Mol Cell Cardiol 2014, 72:168-76.
73. Ellis JM, Mentock SM, Depetrillo MA, Koves TR, Sen S, Watkins SM, Muoio DM, Cline GW, Taegtmeyer H, Shulman GI, Willis MS, Coleman RA: Mouse cardiac acyl coenzyme a synthetase 1 deficiency impairs Fatty Acid oxidation and induces cardiac hypertrophy. Mol Cell Biol 2011, 31:1252-62.
74. Glembotski CC: The role of the unfolded protein response in the heart. J Mol Cell Cardiol 2008, 44:453-9.
75. Doroudgar S, Glembotski CC: New concepts of endoplasmic reticulum function in the heart: programmed to conserve. J Mol Cell Cardiol 2013, 55:85-91.
76. Lynch JM, Maillet M, Vanhoutte D, Schloemer A, Sargent MA, Blair NS, Lynch KA, Okada T, Aronow BJ, Osinska H, Prywes R, Lorenz JN, Mori K, Lawler J, Robbins J, Molkentin JD: A thrombospondin-dependent pathway for a protective ER stress response. Cell 2012, 149:1257-68.
77. Taegtmeyer H, Beauloye C, Harmancey R, Hue L: Insulin resistance protects the heart from fuel overload in dysregulated metabolic states. Am J Physiol Heart Circ Physiol 2013, 305: H1693-7.
78. McKnight SL: On getting there from here. Science 2010, 330:1338-9.