Mice over-expressing the myocardial creatine transporter develop progressive heart failure and show decreased glycolytic capacity

Journal of Molecular and Cellular Cardiology

Volumn 48, Issue 4, 2010, Pages 582-590

  Phillips, Darci ^a,b   ten Hove, Michiel ^a   Schneider, Jurgen E ^a   Wu, Colin O ^b   Sebag Montefiore, Liam ^a   Aponte, Angel M ^b   Lygate, Craig A ^a   Wallis, Julie ^a   Clarke, Kieran ^a   Watkins, Hugh ^a   Balaban, Robert S ^b   Neubauer, Stefan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Creatine content; Heart failure; Hypertrophy; Magnetic resonance imaging; Magnetic resonance spectroscopy; Myocardial energy metabolism; Proteomics

Indexed keywords

ALPHA ENOLASE; BETA ENOLASE; CARRIER PROTEIN; CREATINE; CREATINE TRANSPORTER; LACTIC ACID; LYASE; UNCLASSIFIED DRUG;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME ACTIVITY; FEMALE; GLYCOLYSIS; HEART FAILURE; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE METABOLISM; HEART VENTRICLE HYPERTROPHY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; AORTA; CARDIOMEGALY; CREATINE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GLYCOLYSIS; HEART FAILURE; HEART VENTRICLES; MAGNETIC RESONANCE IMAGING; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MYOCARDIUM; PHOSPHOCREATINE; PHOSPHOPYRUVATE HYDRATASE;

MUS;

EID: 77649272094     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.10.033     Document Type: Article

References (53)

1. Hermann G., and Decherd G.M. The chemical nature of heart failure. Ann. Intern. Med. 12 (1939) 1233-1244
2. Neubauer S. The failing heart-an engine out of fuel. N. Engl. J. Med. 356 (2007) 1140-1151
3. Olson R.E., and Schwartz W.B. Myocardial metabolism in congestive heart failure. Medicine (Baltimore) 30 (1951) 21-41
4. Ashrafian H., Frenneaux M.P., and Opie L.H. Metabolic mechanisms in heart failure. Circulation 116 (2007) 434-448
5. Ingwall J.S., and Weiss R.G. Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ. Res. 95 (2004) 135-145
6. Taegtmeyer H. Cardiac metabolism as a target for the treatment of heart failure. Circulation 110 (2004) 894-896
7. Lopaschuk G.D., and Kelly D.P. Signalling in cardiac metabolism. Cardiovasc. Res. 79 (2008) 205-207
8. Ventura-Clapier R., Garnier A., and Veksler V. Energy metabolism in heart failure. J. Physiol. 555 (2004) 1-13
9. The Cardiac Insufficiency Bisoprolol Study II (CIBIS-II): a randomised trial. Lancet 1999; 353: 9-13.
10. Cohn J.N., and Tognoni G. A randomized trial of the angiotensin-receptor blocker valsartan in chronic heart failure. N. Engl. J. Med. 345 (2001) 1667-1675
11. Swedberg K., and Kjekshus J. Effects of enalapril on mortality in severe congestive heart failure: results of the Cooperative North Scandinavian Enalapril Survival Study (CONSENSUS). Am. J. Cardiol. 62 (1988) 60A-66A
12. Packer M., Carver J.R., Rodeheffer R.J., Ivanhoe R.J., DiBianco R., Zeldis S.M., et al. Effect of oral milrinone on mortality in severe chronic heart failure. The PROMISE Study Research Group. N. Engl. J. Med. 325 (1991) 1468-1475
13. Rouleau J.L., Pitt B., Dhalla N.S., Dhalla K.S., Swedberg K., Hansen M.S., et al. Prognostic importance of the oxidized product of catecholamines, adrenolutin, in patients with severe heart failure. Am. Heart J. 145 (2003) 926-932
14. Liao R., Nascimben L., Friedrich J., Gwathmey J.K., and Ingwall J.S. Decreased energy reserve in an animal model of dilated cardiomyopathy. Relationship to contractile performance. Circ. Res. 78 (1996) 893-902
15. Nascimben L., Friedrich J., Liao R., Pauletto P., Pessina A.C., and Ingwall J.S. Enalapril treatment increases cardiac performance and energy reserve via the creatine kinase reaction in myocardium of Syrian myopathic hamsters with advanced heart failure. Circulation 91 (1995) 1824-1833
16. Nascimben L., Ingwall J.S., Pauletto P., Friedrich J., Gwathmey J.K., Saks V., et al. Creatine kinase system in failing and nonfailing human myocardium. Circulation 94 (1996) 1894-1901
17. Neubauer S., Krahe T., Schindler R., Horn M., Hillenbrand H., Entzeroth C., et al. 31P magnetic resonance spectroscopy in dilated cardiomyopathy and coronary artery disease. Altered cardiac high-energy phosphate metabolism in heart failure. Circulation 86 (1992) 1810-1818
18. Neubauer S., Horn M., Naumann A., Tian R., Hu K., Laser M., et al. Impairment of energy metabolism in intact residual myocardium of rat hearts with chronic myocardial infarction. J. Clin. Invest. 95 (1995) 1092-1100
19. Shen W., Asai K., Uechi M., Mathier M.A., Shannon R.P., Vatner S.F., et al. 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 (1999) 2113-2118
20. Zhang J., Wilke N., Wang Y., Zhang Y., Wang C., Eijgelshoven M.H., et al. Functional and bioenergetic consequences of postinfarction left ventricular remodeling in a new porcine model. MRI and 31 P-MRS study. Circulation 94 (1996) 1089-1100
21. Ingwall J.S. Transgenesis and cardiac energetics: new insights into cardiac metabolism. J. Mol. Cell. Cardiol. 37 (2004) 613-623
22. Kaasik A., Veksler V., Boehm E., Novotova M., Minajeva A., and Ventura-Clapier R. Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ. Res. 89 (2001) 153-159
23. ten H.M., Lygate C.A., Fischer A., Schneider J.E., Sang A.E., Hulbert K., et al. Reduced inotropic reserve and increased susceptibility to cardiac ischemia/reperfusion injury in phosphocreatine-deficient guanidinoacetate-N-methyltransferase-knockout mice. Circulation 111 (2005) 2477-2485
24. Wallis J., Lygate C.A., Fischer A., ten H.M., Schneider J.E., Sebag-Montefiore L., et al. Supranormal myocardial creatine and phosphocreatine concentrations lead to cardiac hypertrophy and heart failure: insights from creatine transporter-overexpressing transgenic mice. Circulation 112 (2005) 3131-3139
25. Schneider J.E., Cassidy P.J., Lygate C., Tyler D.J., Wiesmann F., Grieve S.M., et al. Fast, high-resolution in vivo cine magnetic resonance imaging in normal and failing mouse hearts on a vertical 11.7 T system. J. Magn. Reson. Imaging 18 (2003) 691-701
26. Cassidy P.J., Schneider J.E., Grieve S.M., Lygate C., Neubauer S., and Clarke K. Assessment of motion gating strategies for mouse magnetic resonance at high magnetic fields. J. Magn. Reson. Imaging 19 (2004) 229-237
27. Schneider J.E., Stork L.A., Bell J.T., ten H.M., Isbrandt D., Clarke K., et al. Cardiac structure and function during ageing in energetically compromised guanidinoacetate N-methyltransferase (GAMT)-knockout mice-a one year longitudinal MRI study. J. Cardiovasc. Magn. Reson. 10 (2008) 9
28. Schneider J.E., Tyler D.J., ten H.M., Sang A.E., Cassidy P.J., Fischer A., et al. In vivo cardiac 1H-MRS in the mouse. Magn. Reson. Med. 52 (2004) 1029-1035
29. Naressi A., Couturier C., Castang I., de B.R., and Graveron-Demilly D. Java-based graphical user interface for MRUI, a software package for quantitation of in vivo/medical magnetic resonance spectroscopy signals. Comput. Biol. Med. 31 (2001) 269-286
30. Lygate C.A., Fischer A., Sebag-Montefiore L., Wallis J., ten H.M., and Neubauer S. The creatine kinase energy transport system in the failing mouse heart. J. Mol. Cell. Cardiol. 42 (2007) 1129-1136
31. Johnson D.T., Harris R.A., French S., Blair P.V., You J., Bemis K.G., et al. Tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. Cell. Physiol. 292 (2007) C689-C697
32. Johnson DT, Harris RA, French S, Aponte A, Balaban RS. Proteomic changes associated with Diabetes in the BB-DP rat. Am J Physiol Endocrinol Metab 2008;296:E422-32.
33. Hunsucker S.W., Solomon B., Gawryluk J., Geiger J.D., Vacano G.N., Duncan M.W., et al. Assessment of post-mortem-induced changes to the mouse brain proteome. J. Neurochem. 105 (2008) 725-737
34. Viallard J.L., Murthy M.R., and Dastugue B. An ultramicro bioluminescence assay of enolase: application to human cerebrospinal fluid. Neurochem. Res. 10 (1985) 1555-1566
35. Rice J.A., and Wu C.O. Nonparametric mixed effects models for unequally sampled noisy curves. Biometrics 57 (2001) 253-259
36. Jin X., Wang L.S., Xia L., Zheng Y., Meng C., Yu Y., et al. Hyper-phosphorylation of alpha-enolase in hypertrophied left ventricle of spontaneously hypertensive rat. Biochem. Biophys. Res. Commun. 371 (2008) 804-809
37. Shen X., Zheng S., Thongboonkerd V., Xu M., Pierce Jr. W.M., Klein J.B., et al. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am. J. Physiol. Endocrinol. Metab. 287 (2004) E896-E905
38. Glyn-Jones S., Song S., Black M.A., Phillips A.R., Choong S.Y., and Cooper G.J. Transcriptomic analysis of the cardiac left ventricle in a rodent model of diabetic cardiomyopathy: molecular snapshot of a severe myocardial disease. Physiol. Genomics 28 (2007) 284-293
39. Keller A., Rouzeau J.D., Farhadian F., Wisnewsky C., Marotte F., Lamande N., et al. Differential expression of alpha-and beta-enolase genes during rat heart development and hypertrophy. Am. J. Physiol. 269 (1995) H1843-H1851
40. Saeedi R., Wambolt R.B., Parsons H., Antler C., Leong H.S., Keller A., et al. Gender and post-ischemic recovery of hypertrophied rat hearts. BMC Cardiovasc. Disord. 6 (2006) 8
41. Johnson D.T., Harris R.A., Blair P.V., and Balaban R.S. Functional consequences of mitochondrial proteome heterogeneity. Am. J. Physiol. Cell. Physiol. 292 (2007) C698-C707
42. Peterson C.C., Nagy K.A., and Diamond J. Sustained metabolic scope. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 2324-2328
43. Comi G.P., Fortunato F., Lucchiari S., Bordoni A., Prelle A., Jann S., et al. Beta-enolase deficiency, a new metabolic myopathy of distal glycolysis. Ann. Neurol. 50 (2001) 202-207
44. Aasum E., Hafstad A.D., and Larsen T.S. Changes in substrate metabolism in isolated mouse hearts following ischemia-reperfusion. Mol. Cell. Biochem. 249 (2003) 97-103
45. Lopaschuk G.D., and Barr R.L. Measurements of fatty acid and carbohydrate metabolism in the isolated working rat heart. Mol. Cell. Biochem. 172 (1997) 137-147
46. Saddik M., and Lopaschuk G.D. Myocardial triglyceride turnover and contribution to energy substrate utilization in isolated working rat hearts. J. Biol. Chem. 266 (1991) 8162-8170
47. Merkulova T., Thornell L.E., Butler-Browne G., Oberlin C., Lucas M., Lamande N., et al. The beta enolase subunit displays three different patterns of microheterogeneity in human striated muscle. J. Muscle Res. Cell. Motil. 20 (1999) 55-63
48. Merkulova T., Lucas M., Jabet C., Lamande N., Rouzeau J.D., Gros F., et al. Biochemical characterization of the mouse muscle-specific enolase: developmental changes in electrophoretic variants and selective binding to other proteins. Biochem. J. 323 Pt 3 (1997) 791-800
49. Foucault G., Vacher M., Cribier S., and rrio-Dupont M. Interactions between beta-enolase and creatine kinase in the cytosol of skeletal muscle cells. Biochem. J. 346 Pt. 1 (2000) 127-131
50. ran-Lapujade P., Rossell S., van Gulik W.M., Luttik M.A., de Groot M.J., Slijper M., et al. The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 15753-15758
51. Gaba A., Wang Z., Krishnamoorthy T., Hinnebusch A.G., and Sachs M.S. Physical evidence for distinct mechanisms of translational control by upstream open reading frames. EMBO J. 20 (2001) 6453-6463
52. Dannelly H.K., Duclos B., Cozzone A.J., and Reeves H.C. Phosphorylation of Escherichia coli enolase. Biochimie 71 (1989) 1095-1100
53. Luptak I., Yan J., Cui L., Jain M., Liao R., and Tian R. Long-term effects of increased glucose entry on mouse hearts during normal aging and ischemic stress. Circulation 116 (2007) 901-909