Regulation of energy substrate metabolism in the diabetic heart

Cardiovascular Research

Volumn 34, Issue 1, 1997, Pages 25-33

  Stanley, William C ^a   Lopaschuk, Gary D ^b   McCormack, James G ^c  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c NOVO NORDISK A S   (Denmark)

Author keywords

Diabetes; Fatty acids; Glycolyis; Lactate; Myocardial ischemia; Myocardial metabolism; Pyruvate dehydrogenase

Indexed keywords

FATTY ACID; INSULIN; LACTIC ACID; PYRUVATE DEHYDROGENASE;

CARDIOMYOPATHY; CITRIC ACID CYCLE; CONGESTIVE HEART FAILURE; DIABETES MELLITUS; ENERGY METABOLISM; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; GLUCOSE TRANSPORT; GLYCOLYSIS; HEART INFARCTION; HEART MITOCHONDRION; HEART MUSCLE METABOLISM; HEART MUSCLE OXYGEN CONSUMPTION; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

ANIMALS; CARDIOMYOPATHIES; DIABETES COMPLICATIONS; DIABETES MELLITUS; ENERGY METABOLISM; FATTY ACIDS; GLUCOSE; GLYCOLYSIS; HUMANS; INSULIN; MITOCHONDRIA, HEART; MYOCARDIUM; RATS;

EID: 0342506484     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(97)00047-3     Document Type: Review

References (110)

1. Stone PH, Muller JE, Hartwell T, et al. The effect of diabetes mellitus on prognosis and serial left ventricular function after acute myocardial infarction: contribution of both coronary disease and diastolic left ventricular dysfunction to the adverse prognosis. J Am Coll Cardiol 1989;14:49-57.
2. Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham study. J Am Med Assoc 1979;241:2035-2038.
3. Camici P, Ferrannini E, Opie LH. Myocardial metabolism in ischemia heart disease: basic principles and application to imaging by positron emission tomography. Prog Cardiovasc Dis 1989;32:217-238.
4. Liedtke AJ. Alterations of carbohydrate and lipid metabolism in the acutely ischemic heart. Prog Cardiovasc Dis 1981;23:321.
5. Opie LH. Metabolism of the heart in health and disease. Am Heart J 1968;76:685-689.
6. Stanley WC, Lopaschuk GD, Hall JL, McCormack JG. Regulation of myocardial carbohydrate metabolism under normal and ischemic conditions: Potential for pharmacological interventions. Cardiovasc Res 1997;33:243-257.
7. Taegtmeyer H. Energy metabolism of the heart: from basic concepts to clinical applications. Curr Prob Cardiol 1994;19:59-113.
8. Jeffrey FMH, Diczku V, Sherry AD, Malloy CR. Substrate selection in the isolated working rat heart: effects of reperfusion, afterload and concentration. Basic Res Cardiol 1995;90:388-396.
9. Myears DW, Sobel BE, Bergmann SR. Substrate use in ischemic and reperfused canine myocardium: quantitative considerations. Am J Physiol 1987;253:H107-H114.
10. Lewandowski ED, White LT. Pyruvate dehydrogenase influences postischemic heart function. Circulation 1995;91:2071-2079.
11. Lopaschuk GD, Wambolt RB, Barr RL. An imbalance between glycolysis and glucose oxidation is a possible explanation for the detrimental effects of high levels of fatty acids during aerobic reperfusion of ischemic hearts. J Pharmacol Exp Ther 1993;264:135-144.
12. Lopaschuk GD, Belke DD, Gamble J, Itoi T, Schönekess BO. Regulation of fatty acid oxidation in the mammalian heart in health and disease. Biochim Biophys Acta 1994;1213:263-276.
13. Renstrom B, Nellis SH, Liedtke AJ. Metabolic oxidation of pyruvate and lactate during early myocardial reperfusion. Cire Res 1990;66:282-288.
14. Renstrom B, Nellis SH, Liedtke AJ. Metabolic oxidation of glucose during early myocardial reperfusion. Cire Res 1989;65:1094-1101.
15. Schwaiger M, Neese RA Araujo L, et al. Sustained monoxidative glucose utilization and depletion of glycogen in reperfused canine myocardium. J Am Coll Cardiol 1989;13:745-754.
16. 13C-NMR study of glucose oxidation in the intact functioning rat heart following diabetes-induced cardiomyopathy. J Mol Cell Cardiol 1993;25:1203-1213.
17. Gamble J, Lopaschuk GD. Glycolysis and glucose oxidation during reperfusion of ischemic hearts from diabetic rats. Biochim Biophys Acta 1994;1225:191-199.
18. Barrett EJ, Schwartz RG, Francis CK, Zaret BL. Regulation by insulin of myocardial glucose and fatty acid metabolism in the conscious dog. J Clin Invest 1984;74:1073-1079.
19. Garland PB, Randle PJ. Regulation of glucose uptake by muscle. X. Effects of alloxan-diabetes, starvation, hypophysectomy and adrenalectomy and of fatty acids, ketone bodies and pyruvate on the glycerol output and concentrations of free fatty acids, long-chain fatty acyl coenzyme A, glycerol phosphate and citrate cycle inter-mediates in rat hearts and diaphragm muscles. Biochem J 1964;93:678-687.
20. Morgan HE, Cadenas E, Regan DM. Regulation of glucose uptake in muscle. II. Rate-limiting steps and effects of insulin and anoxia in heart muscle from diabetic rats. J Biol Chem 1961;236:262-268.
21. Newsholme EA, Randle PJ. Regulation of glucose uptake by muscle. Effects of fatty acids, ketone bodies and pyruvate, and of alloxan diabetes, starvation, hypophysectomy and adrenalectomy, on the concentrations of hexose phosphates, nucleotides and inorganic phosphate in perfused rat heart. Biochem J 1964;93:641-651.
22. Bell GI, Kayano T, Buse JB, et al. Molecular biology of mammalian glucose transporters. Diabetes Care 1990;13:198-208.
23. James DE, Strube M, Mueckler M. Molecular cloning and characterization of an insulin regulatable glucose transporter. Nature 1989;338:83-87.
24. Camps MA, Castello P, Munoz M, et al. Effect of diabetes and fasting on GLUT-4 (muscle-fat) glucose-transporter expression in insulin-sensitive tissues. Biochem J 1992;282:765-772.
25. Garvey WT, Hardin D, Juhaszova M, Dominguez JH. Effects of diabetes on myocardial glucose transport system in rats: implications for diabetic cardiomyopathy. Am J Physiol 1993;264:H837-H844.
26. Hall JL, Sexton W, Stanley WC. Differential regulation of myocardial glucose transporters with exercise training in streptozotcin-induced diabetic rats. J Appl Physiol 1995;78:76-81.
27. Stanley WC, Hall JL, Smith KR, Cartee GD, Hacker TA, Wisneski JA. Myocardial glucose transporters and glycolytic metabolism during ischemia in hyperglycemic diabetic swine. Metabolism 1994;43:61-69.
28. Stanley WC, Hall JL, Hacker TA, Hernandez LA, Whitesell LF. Decreased myocardial glucose uptake during ischemia in diabetic swine. Metabolism 1997;46:168-172.
29. Wall SR, Lopaschuk GD. Glucose oxidation rates in fatty acid-perfused isolated working hearts from diabetic rat. Biochim Biophys Acta 1989; 1006:97-103.
30. Chen V, Ianuzzo CD, Fong BC, Spitzer JJ. The effects of acute and chronic diabetes on myocardial metabolism in rats. Diabetes 1984;33:1078-1084.
31. Chappell JD, Robinson BH. Penetration of the mitochondrial membrane by tricarboxylic acid anions. Biochem Soc Symp 1968;27:123-133.
32. Lopaschuk GD. Abnormal mechanical function in diabetes: relationship to altered myocardial carbohydrate/lipid metabolism. Coron Artery Dis 1996;7:116-123.
33. Hall JL, Henderson J, Hernandez LA, Stanley WC. Hyperglycemia causes an increase in myocardial interstitial glucose and glucose uptake during ischemia in swine. Metabolism 1996;45:542-549.
34. Barrett EJ, Schwartz RG, Francis CK, Zaret BL. Regulation by insulin of myocardial glucose and fatty acid metabolism in the conscious dog. J Clin Invest 1984;74:1073-1079.
35. Randle PJ, Priesman DA. Short term and longer term regulation of pyruvate dehydrogenase kinase. In: Patel MS, Roche TE, Harris RA, eds. Alpha-Keto Acid Dehydrogenase Complexes. Basel: Birkhäuser Verlag, 1996:151-161.
36. Avogaro A, Nosadini R, Doria A, et al. Myocardial metabolism in insulin-deficient diabetic humans without coronary artery disease. Am J Physiol 1990;258:E606-E618.
37. Hall JL, Stanley WC, Lopaschuk GD, et al. Impaired pyruvate oxidation but not glucose uptake in diabetic pig heart during dobutamine stress. Am J Physiol 1996;271:H2320-H2329
38. Randle PJ, Hales CN, Garland PB, Newsholme EA The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetic mellitus. Lancet 1963;1:785-789.
39. Wieland O, Funcke HV, Loffler, G. Interconversion of pyruvate dehydrogenase in rat heart muscle upon perfusion with fatty acids or ketone bodies. FEBS Lett 1971;15:295-298.
40. Wieland O, Siess E, Schulze-Wethmar FH, Funcke HG, Winton B. Active and inactive forms of pyruvate dehydrogenase in rat heart and kidney: effect of diabetes, fasting and refeeding on pyruvate dehydrogenase interconversion. Arch Biochem Biophys 1971;143:593-601.
41. Hansford RG, Cohen L. Relative importance of pyruvate dehydrogenase interconversion and feed-back inhibition in the effect of fatty acids on pyruvate oxidation by rat heart mitochondria. Arch Biochem Biophys 1978;191:65-81.
42. McCormack JG, Halestrap AP, Denton RM. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 1990;70:391-425.
43. Yeaman SJ. The 2-oxo acid dehydrogenase complexes: recent advances. Biochem J 1989;257:625-632.
44. Kerbey AL, Radcliffe PM, Randle PJ. Diabetes and the control of pyruvate dehydrogenase in rat heart mitochondria by concentration ratios of adenosine triphosphate/adenosine diphosphate, of reduced/oxidized nicotinamide-adenine dinucleotide and acetylcoenzyme A/coenzyme A. Biochem J 1977;164:509-519.
45. Kuo TH, Giacomelli F, Wiener J, Lapanowski-Netzel K. Pyruvate dehydrogenase activity in cardiac mitochondria from genetically diabetic mice. Diabetes 1985;34:1075-1081.
46. Nicholl TA, Lopaschuk GD, McNeill JH. Effects of free fatty acids and dichloroacetate on isolated working diabetic rat heart. Am J Physiol 1991;261:H1053-H1059.
47. 2+ and pyruvate in the regulation of rat heart pyruvate dehydrogenase activity. Biochem J 1982;202:419-427.
48. Lopaschuk GD, Belke DD, Gamble J, Itoi T, Schönekess BO. Regulation of fatty acid oxidation in the mammalian heart in health and disease. Biochim Biophys Acta 1994;1213:263-276.
49. Kreisberg RA. Effects of diabetes and starvation on myocardial triglyceride and free fatty acid utilization. Am J Physiol 1966;210:379-384.
50. Rodrigues B, Braun JE, Spooner M, Severson DL. Regulation of lipoprotein lipase activity in cardiac myocytes from control and diabetic rat hearts by plasma lipids. Can J Physiol Pharmacol 1992;70:1271-1279.
51. Rodrigues B, Severson DL. Acute diabetes does not reduce heparin-releasable lipoprotein lipase activity in perfused hearts from Wistar-Kyoto rats. Can J Physiol Pharmacol 1993;71:657-661.
52. Braun JE, Severson DL. Diabetes reduces heparin- and phospholipase C-releasable lipoprotein lipase from cardiomyocytes. Am J Physiol 1991;260:E477-E485.
53. Denton RM, Randle PJ. Concentration of glycerides and phospholipids in rat heart and gastrocnemius muscles. Biochem J 1967;104:416-422.
54. Murthy VK, Shipp JC. Accumulation of myocardial triacylglycerols in ketotic diabetes. Diabetes 1977;26:222-229.
55. Rizza RA, Crass MF, Shipp JC. Effect of insulin treatment in vivo on heart glycerides and glycogen of alloxan-diabetic rats. Metabolism 1974;20:539-543.
56. Lopaschuk GD, Tsang H. Metabolism of palmitate in isolated working hearts from spontaneously diabetic 'BB' Wistar rats. Circ Res 1987;61:853-858.
57. Saddik M, Lopaschuk GD. Triacylglycerol turnover in isolated working heart of acutely diabetic rats. Can J Physiol Pharmacol 1994;72:1110-1119.
58. McGarry JD, Leatherman GF, Foster DW. Carnitine palmitoyltransferase I. The site of inhibition of hepatic fatty acid oxidation by malonyl-CoA. J Biol Chem 1978;253:4128-4136.
59. Blanchi A, Evans JL, Iverson AJ, Nordlund A, Watts TD, Witters LA Identification of an isozymic form of acetyl-CoA carboxylase. J Biol Chem 1990;265:1502-1509.
60. McGarry JD, Mills SE, Long CS, Foster DW. Observations on the affinity for carnitine, and malonyl-CoA sensitivity, of carnitine palmitoyltransferase I in animal and human tissues. Biochem J 1983;214:21-28.
61. Lopaschuk GD, Witters LA, Itoi T, Barr R, Barr A. Acetyl-CoA carboxylase involvement in the rapid maturation of fatty acid oxidation in the newborn rabbit heart. J Biol Chem 1994;269:25871-25878.
62. Kudo N, Gillespie JG, Kung L, et al. Characterization of 5′AMP-activated protein kinase activity in the heart and its role in inhibiting acetyl-CoA carboxylase during reperfusion following ischemia. Biochim Biophys Acta 1996;1301:67-75
63. Hardie DG. Regulation of fatty acid and cholesterol metabolism by the AMP-activated protein kinase. Biochim Biophys Acta 1992;1123:231-238.
64. Lopaschuk GD, Gamble J. Acetyl-CoA carboxylase: An important regulator of fatty acid oxidation in the heart. Can J Physiol Pharmacol 1994;72:1101-1109.
65. Saddik M, Gamble J, Witters LA, Lopaschuk GD. Acetyl-CoA carboxylase regulation of fatty acid oxidation in the heart. J Biol Chem 1993;268:25836-25845.
66. Kudo N, Barr AJ, Barr RL, Desai S, Lopaschuk GD. High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl CoA levels due to an increase in 5′-AMP-activated protein kinase inhibition of acetyl CoA carboxylase. J Biol Chem 1995;270:17513-17520.
67. Awan MM, Saggerson ED. Malonyl-CoA metabolism in cardiac myocytes and its relevance to the control of fatty acid oxidation. Biochem J 1993;295:61-66.
68. Glatz JFC, van Breda E, Keizer HA, et al. Rat heart fatty acid-binding protein content is increased in experimental diabetes. Biochem Biophys Res Commun 1994;199:639-646.
69. Chen V, Ianuzzo D, Fong BC, Spitzer JJ. The effects of acute diabetes on myocardial metabolism in rats. Metabolism 1984;33:1078-1084.
70. Mokhtar N, Lavoie J-P, Rousseau-Migneron S, Nadeau A. Physical training reverses defect in mitochondrial energy production in heart of chronically diabetic rats. Diabetes 1993;42:686-687.
71. Kuo TH, Moore KH, Giomelli F, Wiener J. Defective oxidative metabolism of heart mitochondria from genetically diabetic mice. Diabetes 1983;32:781-787.
72. Pierce GN, Dhalla NS. Heart mitochondrial function in chronic experimental diabetes in rats. Can J Cardiol 1984;1:48-54.
73. Savabi F. Mitochondrial creatine phosphokinase deficiency in diabetic rat heart. Biochem Biophys Res Commun 1984;154:469-475.
74. Russell RR, Taegtmeyer H. Changes in citric acid cycle flux and anaplerosis antedate the functional decline in isolated rat hearts. J Clin Invest 1991;87:384-390.
75. Bradley RF, Bryfogle JW Survival of diabetic patients after myocardial infarction. Am J Med 1956;30:207-216.
76. Kesler I. Mortality experience of diabetic patients: a twenty-six year follow-up study. Am J Med 1971;51:715-724.
77. Partamian JO, Bradley RF. Acute myocardial infarction in 258 cases of diabetes. N Engl J Med 1965;273:455.
78. Rytter L, Troelsen S, Beck-Nielsen H. Prevalence and mortality of acute myocardial infarction in patients with diabetes. Diabetes Care 1985;8:230-234.
79. Ulvenstam G, Aberg A, Bergstrand R, et al. Long-term prognosis after myocardial infarction in men with diabetes. Diabetes 1985;34:787-792.
80. Borrow KM, Jaspan JB, Williams KA, Neumann A, Wolinski-Walley P, Lang RM. Myocardial mechanics in young adult patient with diabetes mellitus: Effects of altered load, inotropic state and dynamic exercise. J Am Coll Cardiol 1990;15:1508-1517.
81. Fein FS, Sonnenblick. Diabetic cardiomyopathy. Prog Cardiovasc Dis 1985;4:255-270.
82. Hamby RI, Zoneraich S, Sherman L. Diabetic cardiomyopathy. J Am Med Assoc 1974;229:1749-1754.
83. Ledet T. Diabetic cardiomyopathy: quantitative histological studies of the heart from young juvenile diabetics. Acta Pathol Microbiol Scand 1976;84:421-428.
84. Mustonen JN, Uusitupa MIJ, Tahvanainen K, et al. Impaired left ventricular systolic function during exercise in middle-aged insulin-dependent and noninsulin-dependent diabetic subjects without clinically evident cardiovascular disease. Am J Cardiol 1988;62:1273-1279.
85. Seneviratne BIB. Diabetic cardiomyopathy: The preclinical phase. Br Med J 1977;1:1444.
86. Shapiro LM, Howat AP, Calter MM. Left ventricular function in diabetes mellitus. I. Methodology, and prevalence and spectrum of abnormalities. Br Heart J 1991;45:122-128.
87. Uusitupa M, Mustonen J, Laalso M, et al. Impairment of diastolic function in middle-aged Type 1 (insulin-dependent) and Type 2 (non-insulin-dependent) diabetic patients free of cardiovascular disease. Diabetologia 1988;31:783-791.
88. Vered Z, Battler A, Segal P, et al. Exercise-induced left ventricular dysfunction in young men with asymptomatic diabetes mellitus (diabetic cardiomyopathy). Am J Cardiol 1984;54:633-637.
89. Gwilt DJ, Petri M, Lewis PW, Nattrass M, Pentecost BL Myocardial infarct size and mortality in diabetic patients. Br Heart J 1985;54:466-472.
90. Harrower AD, Clarke BF. Experience of coronary care in diabetics. Br Med J 1976;a:126-128.
91. Jaffe AS, Spadaro JJ, Schechtman K, Roberts R, Geltman EM, Sobel BE. Increased congestive heart failure after myocardial infarction of modest extent in patients with diabetes mellitus. Am Heart J 1984;108:31-37.
92. Gotzsche O. Myocardial cell dysfunction in diabetes mellitus. Diabetes 1986;35:1158-62.
93. Oswald B, Corcovan S, Yudkin JS. Prevalence and risks of hyperglycemia and undiagnosed diabetes in patients with acute myocardial infarction Lancet 1984;1:1264-1267.
94. Oswald GA, Smith CCT, Betteridge DJ, Yudkin JS. Determinants and importance of stress hyperglycaemia in non-diabetic patients with myocardial infarction. Br Med J 1986;293:917-922.
95. Bellodi G, Manicardi V, Malavasi V, et al. Hyperglycemia and prognosis of acute myocardial infarction in patients without diabetes mellitus. Am J Cardiol 1989;64:885-888.
96. Miller TB. Cardiac performance of isolated perfused heart from alloxan diabetic rats. Am J Physiol 1972;236:H808-H812.
97. Paulson DJ, Shug AL, Jurak R, Schmidt M. The role of altered lipid metabolism in the cardiac dysfunction associated with diabetes. In: Nagano M, Dhalla NS, eds. The Diabetic Heart, Raven Press, New York, 1991:395-407.
98. Penpargkul S, Schaible TF, Yipintsoi T, Scheuer J. The effect of diabetes on performance and metabolism of rat hearts. Circ Res 1980;47:911-921.
99. Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Brauwood AW, Grishman AA. A new type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 1972;30:595-602.
100. Shapiro LM. Specific heart disease in diabetes mellitus. Br Med J 1982;284:140-141.
101. Tahiliani AG, McNeill JH. Diabetes-induced abnormalities in the myocardium. Life Sci 1986;38:959-974.
102. Tomlinson KC, Gardiner SM, Hebden RA, Bennett T. Functional consequences of streptozotocin-induced diabetes mellitus, with particular reference to the cardiovascular system. Pharmacol Rev 1992;44:103-150.
103. Oliver MF, Kurien VA, Greenwood TW. Relation between serumfree-fatty-acids and arrhythmias and death after acute myocardial infarction. Lancet 1968;1:710-715.
104. Feuvray D, Idell-Wenger JA, Neely JR. Effects of ischemia on rat myocardial function and metabolism in diabetes. Circ Res 1979;44:322-329.
105. Dhalla NS, Elimban V, Rupp H. Paradoxical role of lipid metabolism in heart function and dysfunction. Mol Cell Biochem 1992;116:3-9.
106. Clarke B, Wyatt KM, McCormack JG. Ranolazine increases active pyruvate dehydrogenase in perfused normoxic rat hearts: evidence for an indirect mechanism. J Mol Cell Cardiol 1996;28:341-350.
107. Fantini E, Demaison L, Sentex E, Grynberg A, Athias P. Some biochemical aspects of the protective effect of trimetazidine on rat cardiomyocytes during hypoxia and reoxygenation. J Mol Cell Cardiol 1994;26:949-958.
108. Higgins AJ, Morville M, Burges RA, Blackburn KJ. Mechanism of action of oxfenicine on muscle metabolism. Biochem Biophys Res Commun 1981;100:291-296.
109. Broderick TL, Quinney HA, Lopaschuk GD. Carnitine stimulation of glucose oxidation in the fatty acid perfused isolated working rat heart. J Biol Chem 1992;267:3758-3763.
110. Broderick TL, Quinney, HA, Barker CC Lopaschuk GD. Beneficial effect of carnitine on mechanical recovery of rat hearts reperfused after a transient period of global ischemia is accompanied by a stimulation of glucose oxidation. Circulation 1993;87:972-981.