Impaired cytosolic NADH shuttling and elevated UCP3 contribute to inefficient citric acid cycle flux support of postischemic cardiac work in diabetic hearts

Journal of Molecular and Cellular Cardiology

Volumn 79, Issue , 2015, Pages 13-20

  Banke, Natasha H ^a   Lewandowski, E Douglas ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Db db mouse malate aspartate shuttle; Mitochondria; Oxoglutarate malate carrier; Reducing equivalents; Uncoupling protein

Indexed keywords

ASPARTIC ACID; CARRIER PROTEIN; GLUCOSE; MALIC ACID; OXOGLUTARATE MALATE CARRIER; PALMITATE C 13; RADIOPHARMACEUTICAL AGENT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 3; 2-OXOGLUTARATE-MALATE CARRIER PROTEIN; ION CHANNEL; MALIC ACID DERIVATIVE; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 2; MITOCHONDRIAL UNCOUPLING PROTEIN 3; NICOTINAMIDE ADENINE DINUCLEOTIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CARBON UTILIZATION; CITRIC ACID CYCLE; CONTROLLED STUDY; CYTOSOL; CYTOSOLIC NADH SHUTTLING IMPAIRMENT; DISEASE PREDISPOSITION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; HEART MUSCLE ISCHEMIA; HEART WORK; ISOLATED HEART; MALATE ASPARTATE SHUTTLE; MALE; METABOLISM; MOUSE; MOUSE STRAIN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; REPERFUSION INJURY; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; COMPLICATION; EXPERIMENTAL DIABETES MELLITUS; HEMODYNAMICS; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; OXIDATION REDUCTION REACTION; PATHOLOGY; PATHOPHYSIOLOGY; PERFUSION;

ANIMALS; ASPARTIC ACID; CARBON-13 MAGNETIC RESONANCE SPECTROSCOPY; CARRIER PROTEINS; CITRIC ACID CYCLE; CYTOSOL; DIABETES MELLITUS, EXPERIMENTAL; HEMODYNAMICS; ION CHANNELS; MALATES; MALE; MICE, INBRED C57BL; MITOCHONDRIAL PROTEINS; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NAD; OXIDATION-REDUCTION; PERFUSION; PPAR ALPHA;

EID: 84911416779     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.10.015     Document Type: Article

References (53)

1. Belke D.D., Severson D.L. Diabetes in mice with monogenic obesity: the db/db mouse and its use in the study of cardiac consequences. Methods Mol Biol 2012, 933:47-57.
2. Boudina S., Abel E.D. Diabetic cardiomyopathy revisited. Circulation 2007, 115:3213-3223.
3. Chambers K.T., Leone T.C., Sambandam N., Kovacs A., Wagg C.S., Lopaschuk G.D., et al. Chronic inhibition of pyruvate dehydrogenase in heart triggers an adaptive metabolic response. J Biol Chem 2011, 286:11155-11162.
4. Feuvray D., Lopaschuk G.D. Controversies on the sensitivity of the diabetic heart to ischemic injury: the sensitivity of the diabetic heart to ischemic injury is decreased. Cardiovasc Res 1997, 34:113-120.
5. Welch M.J., Lewis J.S., Kim J., Sharp T.L., Dence C.S., Gropler R.J., et al. Assessment of myocardial metabolism in diabetic rats using small-animal PET: a feasibility study. J Nucl Med 2006, 47:689-697.
6. Aasum E., Hafstad A.D., Severson D.L., Larsen T.S. Age-dependent changes in metabolism, contractile function, and ischemic sensitivity in hearts from db/db mice. Diabetes 2003, 52:434-441.
7. Mazumder P.K., O'Neill B.T., Roberts M.W., Buchanan J., Yun U.J., Cooksey R.C., et al. Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes 2004, 53:2366-2374.
8. Neely J.R., Grotyohann L.W. Role of glycolytic products in damage to ischemic myocardium. Dissociation of adenosine triphosphate levels and recovery of function of reperfused ischemic hearts. Circ Res 1984, 55:816-824.
9. Bugger H., Boudina S., Hu X.X., Tuinei J., Zaha V.G., Theobald H.A., et al. Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3. Diabetes 2008, 57:2924-2932.
10. Hafstad A.D., Khalid A.M., How O.J., Larsen T.S., Aasum E. Glucose and insulin improve cardiac efficiency and postischemic functional recovery in perfused hearts from type 2 diabetic (db/db) mice. Am J Physiol Endocrinol Metab 2007, 292:E1288-E1294.
11. Wang P., Chatham J.C. Onset of diabetes in Zucker diabetic fatty (ZDF) rats leads to improved recovery of function after ischemia in the isolated perfused heart. Am J Physiol Endocrinol Metab 2004, 286:E725-E736.
12. Cole M.A., Murray A.J., Cochlin L.E., Heather L.C., McAleese S., Knight N.S., et al. A high fat diet increases mitochondrial fatty acid oxidation and uncoupling to decrease efficiency in rat heart. Basic Res Cardiol 2011, 106:447-457.
13. Buchanan J., Mazumder P.K., Hu P., Chakrabarti G., Roberts M.W., Yun U.J., et al. Reduced cardiac efficiency and altered substrate metabolism precedes the onset of hyperglycemia and contractile dysfunction in two mouse models of insulin resistance and obesity. Endocrinology 2005, 146:5341-5349.
14. Murray A.J., Anderson R.E., Watson G.C., Radda G.K., Clarke K. Uncoupling proteins in human heart. Lancet 2004, 364:1786-1788.
15. Yu X., White L.T., Alpert N.M., Lewandowski E.D. Subcellular metabolite transport and carbon isotope kinetics in the intramyocardial glutamate pool. Biochemistry 1996, 35:6963-6968.
16. Lewandowski E.D., Yu X., LaNoue K.F., White L.T., Doumen C., O'Donnell J.M. Altered metabolite exchange between subcellular compartments in intact postischemic rabbit hearts. Circ Res 1997, 81:165-175.
17. O'Donnell J.M., Doumen C., LaNoue K.F., White L.T., Yu X., Alpert N.M., et al. Dehydrogenase regulation of metabolite oxidation and efflux from mitochondria in intact hearts. Am J Physiol 1998, 274:H467-H476.
18. Griffin J.L., O'Donnell J.M., White L.T., Hajjar R.J., Lewandowski E.D. Postnatal expression and activity of the mitochondrial 2-oxoglutarate-malate carrier in intact hearts. Am J Physiol Cell Physiol 2000, 279:C1704-C1709.
19. Griffin J.L., White L.T., Lewandowski E.D. Substrate-dependent proton load and recovery of stunned hearts during pyruvate dehydrogenase stimulation. Am J Physiol Heart Circ Physiol 2000, 279:H361-H367.
20. O'Donnell J.M., Kudej R.K., LaNoue K.F., Vatner S.F., Lewandowski E.D. Limited transfer of cytosolic NADH into mitochondria at high cardiac workload. Am J Physiol Heart Circ Physiol 2004, 286:H2237-H2242.
21. Bugger H., Abel E.D. Rodent models of diabetic cardiomyopathy. Dis Model Mech 2009, 2:454-466.
22. Boquist L., Hellman B., Lernmark A., Taljedal I.B. Influence of the mutation "diabetes" on insulin release and islet morphology in mice of different genetic backgrounds. J Cell Biol 1974, 62:77-89.
23. Belke D.D., Larsen T.S., Severson D.L. Cardiac function in perfused hearts from diabetic mice. Adv Exp Med Biol 2001, 498:241-245.
24. Harmancey R., Lam T.N., Lubrano G.M., Guthrie P.H., Vela D., Taegtmeyer H. Insulin resistance improves metabolic and contractile efficiency in stressed rat heart. FASEB J 2012, 26:3118-3126.
25. Harmancey R., Vasquez H.G., Guthrie P.H., Taegtmeyer H. Decreased long-chain fatty acid oxidation impairs postischemic recovery of the insulin-resistant rat heart. FASEB J 2013, 27:3966-3978.
26. Belke D.D., Swanson E.A., Dillmann W.H. Decreased sarcoplasmic reticulum activity and contractility in diabetic db/db mouse heart. Diabetes 2004, 53:3201-3208.
27. Banke N.H., Wende A.R., Leone T.C., O'Donnell J.M., Abel E.D., Kelly D.P., et al. Preferential oxidation of triacylglyceride-derived fatty acids in heart is augmented by the nuclear receptor PPARalpha. Circ Res 2010, 107:233-241.
28. Lopaschuk G.D., Hansen C.A., Neely J.R. Fatty acid metabolism in hearts containing elevated levels of CoA. Am J Physiol 1986, 250:H351-H359.
29. 13C NMR signal from glutamate and direct detection of tricarboxylic acid (TCA) cycle intermediates. Magn Reson Med 1996, 35:149-154.
30. O'Donnell J.M., Zampino M., Alpert N.M., Fasano M.J., Geenen D.L., Lewandowski E.D. Accelerated triacylglycerol turnover kinetics in hearts of diabetic rats include evidence for compartmented lipid storage. Am J Physiol Endocrinol Metab 2006, 290:E448-E455.
31. O'Donnell J.M., Alpert N.M., White L.T., Lewandowski E.D. Coupling of mitochondrial fatty acid uptake to oxidative flux in the intact heart. Biophys J 2002, 82:11-18.
32. O'Donnell J.M., Fields A., Xu X., Chowdhury S.A., Geenen D.L., Bi J. Limited functional and metabolic improvements in hypertrophic and healthy rat heart overexpressing the skeletal muscle isoform of SERCA1 by adenoviral gene transfer in vivo. Am J Physiol Heart Circ Physiol 2008, 295:H2483-H2494.
33. Lehman J.J., Boudina S., Banke N.H., Sambandam N., Han X., Young D.M., et al. The transcriptional coactivator PGC-1alpha is essential for maximal and efficient cardiac mitochondrial fatty acid oxidation and lipid homeostasis. Am J Physiol Heart Circ Physiol 2008, 295:H185-H196.
34. Bowyer D.E. Recovery of lipids from aortas stained with Sudan IV. Atherosclerosis 1977, 26:387-388.
35. Williamson J., Corkey B. Assays of intermediates of the citric acid cycle and related compounds of fluorometric enzyme methods 1969, Academic Press, New York, NY. S.P. Colowick, N.O. Kaplan (Eds.).
36. Lewandowski E.D., Fischer S.K., Fasano M., Banke N.H., Walker L.A., Huqi A., et al. Acute liver carnitine palmitoyltransferase I overexpression recapitulates reduced palmitate oxidation of cardiac hypertrophy. Circ Res 2013, 112:57-65.
37. 13C NMR spectra: metabolic flux, regulation, and compartmentation in hearts. Biophys J 1995, 69:2090-2102.
38. 13C NMR spectroscopy. J Biol Chem 1988, 263:6964-6971.
39. 13C-NMR spectra: theoretical analysis and practical considerations. Am J Physiol 1997, 272:C2037-C2048.
40. O'Donnell J.M., White L.T., Lewandowski E.D. Mitochondrial transporter responsiveness and metabolic flux homeostasis in postischemic hearts. Am J Physiol 1999, 277:H866-H873.
41. Banke N.H., Wende A.R., Leone T.C., O'Donnell J.M., Abel E.D., Kelly D.P., et al. Preferential oxidation of triacylglyceride-derived fatty acids in heart is augmented by the nuclear receptor PPARalpha. Circ Res 2010, 107:233-241.
42. Riehle C., Wende A.R., Zaha V.G., Pires K.M., Wayment B., Olsen C., et al. PGC-1beta deficiency accelerates the transition to heart failure in pressure overload hypertrophy. Circ Res 2011, 109:783-793.
43. Boudina S., Sena S., Theobald H., Sheng X., Wright J.J., Hu X.X., et al. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 2007, 56:2457-2466.
44. Mailloux R.J., Seifert E.L., Bouillaud F., Aguer C., Collins S., Harper M.E. Glutathionylation acts as a control switch for uncoupling proteins UCP2 and UCP3. J Biol Chem 2011, 286:21865-21875.
45. Boudina S., Abel E.D. Mitochondrial uncoupling: a key contributor to reduced cardiac efficiency in diabetes. Physiology (Bethesda) 2006, 21:250-258.
46. Carley A.N., Severson D.L. Fatty acid metabolism is enhanced in type 2 diabetic hearts. Biochim Biophys Acta 2005, 1734:112-126.
47. Boudina S., Han Y.H., Pei S., Tidwell T.J., Henrie B., Tuinei J., et al. UCP3 regulates cardiac efficiency and mitochondrial coupling in high fat-fed mice but not in leptin-deficient mice. Diabetes 2012, 61:3260-3269.
48. Murray A.J., Panagia M., Hauton D., Gibbons G.F., Clarke K. Plasma free fatty acids and peroxisome proliferator-activated receptor alpha in the control of myocardial uncoupling protein levels. Diabetes 2005, 54:3496-3502.
49. Gerber L.K., Aronow B.J., Matlib M.A. Activation of a novel long-chain free fatty acid generation and export system in mitochondria of diabetic rat hearts. Am J Physiol Cell Physiol 2006, 291:C1198-C1207.
50. Rame J.E., Barouch L.A., Sack M.N., Lynn E.G., Abu-Asab M., Tsokos M., et al. Caloric restriction in leptin deficiency does not correct myocardial steatosis: failure to normalize PPAR{alpha}/PGC1{alpha} and thermogenic glycerolipid/fatty acid cycling. Physiol Genomics 2011, 43:726-738.
51. Zhou Y.T., Shimabukuro M., Koyama K., Lee Y., Wang M.Y., Trieu F., et al. Induction by leptin of uncoupling protein-2 and enzymes of fatty acid oxidation. Proc Natl Acad Sci U S A 1997, 94:6386-6390.
52. Lopaschuk G.D., Ussher J.R., Folmes C.D., Jaswal J.S., Stanley W.C. Myocardial fatty acid metabolism in health and disease. Physiol Rev 2010, 90:207-258.
53. Lewandowski E.D., Johnston D.L., Roberts R. Effects of inosine on glycolysis and contracture during myocardial ischemia. Circ Res 1991, 68:578-587.