Calcineurin-induced energy wasting in a transgenic mouse model of heart failure

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 294, Issue 3, 2008, Pages

  Pinz, Ilka ^a   Ostroy, Sanford E ^a   Hoyer, Kirsten ^a   Osinska, Hanna ^b   Robbins, Jeffrey ^b   Molkentin, Jeffery D ^b   Ingwall, Joanne S ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

31P NMR spectroscopy; Adrenergic performance; ATP

Indexed keywords

ADENOSINE TRIPHOSPHATE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CALCINEURIN; CREATINE PHOSPHATE; CYCLOSPORIN A; MITOCHONDRIAL ENZYME;

ADRENERGIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; ENERGY TRANSFER; ENZYME ACTIVITY; GENE OVEREXPRESSION; GLYCOLYSIS; HEART CONTRACTION; HEART FAILURE; HEART HYPERTROPHY; HEART MUSCLE CELL; HEART MUSCLE OXYGEN CONSUMPTION; HYDROLYSIS; ISOLATED HEART; MOUSE; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; TRANSGENIC MOUSE; ULTRASTRUCTURE; WASTING SYNDROME;

ADENOSINE DIPHOSPHATE; ADENOSINE MONOPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; CALCINEURIN; CREATINE; ENERGY METABOLISM; HEART FAILURE; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MYOCYTES, CARDIAC; OXYGEN CONSUMPTION; PHOSPHOCREATINE;

EID: 41549126311     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00911.2007     Document Type: Article

References (34)

1. Allard MF, Schonekess BO, Henning SL, English DR, Lopaschuk GD. Contribution of oxidative metabolism and glycolysis to ATP production in hypertrophied hearts. Am J Physiol Heart Circ Physiol 267: H742-H750, 1994.
2. Arany Z, He H, Lin J, Hoyer K, Handschin C, Toka O, Ahmad F, Matsui T, Chin S, Wu PH, Rybkin II, Shelton JM, Manieri M, Cinti S, Schoen FJ, Bassel-Duby R, Rosenzweig A, Ingwall JS, Spiegelman BM. Transcriptional coactivator PGC-1a controls the energy state and contractile function of cardiac muscle. Cell Metab 1: 259-271, 2005.
3. Bak MI, Ingwall JS. Acidosis during ischemia promotes adenosine triphosphate resynthesis in postischemic rat heart. In vivo regulation of 5′-nucleotidase. J Clin Invest 93: 40-49, 1994.
4. Bak MI, Ingwall JS. Regulation of cardiac AMP-specific 5′-nucleotidase during ischemia mediates ATP resynthesis on reflow. Am J Physiol Cell Physiol 274: C992-C1001, 1998.
5. 31P-SLOOP magnetic resonance spectroscopy. J Am Coll Cardiol 40: 1267-1274, 2002.
6. 2+ handling in a calcineurin transgenic model of heart failure. Cardiovasc Res 54: 105-116, 2002.
7. Chu G, Luo W, Slack JP, Tilgmann C, Sweet WE, Spindler M, Saupe KW, Boivin GP, Moravec CS, Matlib MA, Grupp IL, Ingwall JS, Kranias EG. Compensatory mechanisms associated with the hyperdynamic function of phospholamban-deficient mouse hearts. Circ Res 79: 1064-1076, 1996.
8. De Brouwer KF, Degens H, Aartsen WM, Lindhout M, Bitsch NJ, Gilde AJ, Willemsen PH, Janssen BJ, van der Vusse GJ, van Bilsen M. Specific and sustained down-regulation of genes involved in fatty acid metabolism is not a hallmark of progression to cardiac failure in mice. J Mol Cell Cardiol 40: 838-845, 2006.
9. Hoyer K, Krenz M, Robbins J, Ingwall JS. Shifts in the myosin heavy chain isozymes in the mouse heart result in increased energy efficiency. J Mol Cell Cardiol 42: 214-221, 2007.
10. Ingwall JS. ATP and the Heart. Boston: Kluwer Academic, 2002.
11. Ingwall JS. On the hypothesis that the failing heart is energy starved: lessons learned from the metabolism of ATP and creatine. Curr Hypertens Rep 8: 457-464, 2006.
12. Ingwall JS, Weiss RG. Is the failing heart energy starved? Circ Res 95: 135-145, 2004.
13. Lewandowski ED, Ingwall JS. The physiological chemistry energy production in the heart. In: The Heart: Arteries and Veins, edited by Schlant RC, Alexander RW. New York: McGraw Hill, 1994, p. 153-164.
14. Liao R, Nascimben L, Friedrich J, Gwathmey JK, Ingwall JS. Decreased energy reserve in an animal model of dilated cardiomyopathy. Relationship to contractile performance. Circ Res 78: 893-902, 1996.
15. Lim HW, Windt LJ, Mante LJ, Kimball TR, Witt SA, Sussman MA, Molkentin JD. Reversal of cardiac hypertrophy in transgenic disease models by calcineurin inhibition. J Mol Cell Cardiol 32: 697-709, 2000.
16. Lim HW, Windt LJ, Steinberg L, Taigen T, Witt SA, Kimball TR, Molkentin JD. Calcineurin expression, activation, and function in cardiac pressure-overload hypertrophy. Circulation 101: 2431-2437, 2000.
17. Mirsky I, Pasipoularides A. Elastic properties of normal and hypertrophied cardiac muscle. Fed Proc 39: 156-161, 1980.
18. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93: 215-228, 1998.
19. Nascimben L, Ingwall JS, Pauletto P, Friedrich J, Gwathmey JK, Saks V, Pessina AC, Allen PD. Creatine kinase system in failing and nonfailing human myocardium. Circulation 94: 1894-1901, 1996.
20. Neubauer S. The failing heart - an engine out of fuel. N Engl J Med 356: 1140-1151, 2007.
21. Saupe KW, Spindler M, Hopkins JC, Shen W, Ingwall JS. Kinetic, thermodynamic, and developmental consequences of deleting creatine kinase isoenzymes from the heart. Reaction kinetics of the creatine kinase isoenzymes in the intact heart. J Biol Chem 275: 19742-19746, 2000.
22. Saupe KW, Spindler M, Tian R, Ingwall JS. Impaired cardiac energetics in mice lacking muscle-specific isoenzymes of creatine kinase. Circ Res 82: 898-907, 1998.
23. Sayen MR, Gustafsson AB, Sussman MA, Molkentin JD, Gottlieb RA. Calcineurin transgenic mice have mitochondrial dysfunction and elevated superoxide production. Am J Physiol Cell Physiol 284: C562-C570, 2003.
24. Semeniuk LM, Severson DL, Kryski AJ, Swirp SL, Molkentin JD, Duff HJ. Time-dependent systolic and diastolic function in mice overexpressing calcineurin. Am J Physiol Heart Circ Physiol 284: H425-H430, 2003.
25. Shen W, Asai K, Uechi M, Mathier MA, Shannon RP, Vatner SF, Ingwall JS. Progressive loss of myocardial ATP due to a loss of total purines during the development of heart failure in dogs: a compensatory role for the parallel loss of creatine. Circulation 100: 2113-2118, 1999.
26. Shen W, Spindler M, Higgins M, Jin N, Gill R, Bloem L, Ryan T, Ingwall J. The fall in creatine levels and creatine kinase isozyme changes in the failing heart are reversible: complex post-transcriptional regulation of the components of the CK system. J Mol Cell Cardiol 39: 537-544, 2005.
27. Starling RC, Hammer DF, Altschuld RA. Human myocardial ATP content and in vivo contractile function. Mol Cell Biochem 180: 171-177, 1998.
28. Tian R, Musi N, D'Agostino J, Hirshman MF, Goodyear LJ. Increased adenosine monophosphate-activated protein kinase activity in rat hearts with pressure-overload hypertrophy. Circulation 104: 1664-1669, 2001.
29. 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 28: 755-765, 1996.
30. Tokheim AM, Martin BL. Association of calcineurin with mitochondrial proteins. Proteins 64: 28-33, 2006.
31. Van Oort R, van Rooij E, Bourajjaj M, Schimmel J, Jansen M, van der Nagel R, Doevendans P, Schneider M, van Echteld C, De Windt L. MEF2 activates a genetic program promoting chamber dilation and contractile dysfunction in calcineurin-induced heart failure. Circulation 114: 298-308, 2006.
32. Wallis J, Lygate CA, Fischer A, ten Hove M, Schneider JE, Sebag-Montefiore L, Dawson D, Hulbert K, Zhang W, Zhang MH, Watkins H, Clarke K, Neubauer S. Supranormal myocardial creatine and phosphocreatine concentrations lead to cardiac hypertrophy and heart failure: insights from creatine transporter-overexpressing transgenic mice. Circulation 112: 3131-3139, 2005.
33. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 94: 110-118, 2004.
34. Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, Bassel-Duby R, Williams RS. Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296: 349-352, 2002.