Type 2 diabetes, mitochondrial biology and the heart

Journal of Molecular and Cellular Cardiology

Volumn 46, Issue 6, 2009, Pages 842-849

  Sack, Michael N ^a  

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

Author keywords

Db db; Diabetic cardiomyopathy; Mitochondria; Ob ob; Type 2 diabetes

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; [2 METHYL 4 [4 METHYL 2 (4 TRIFLUOROMETHYLPHENYL) 5 THIAZOLYLMETHYLTHIO]PHENOXY]ACETIC ACID; ANTIOXIDANT; ENZYME ACTIVATOR; LIPOPROTEIN LIPASE; LONG CHAIN FATTY ACID COENZYME A LIGASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; RESVERATROL; ROSIGLITAZONE; SIRTUIN;

ATHEROSCLEROSIS; DIASTOLIC DYSFUNCTION; DISEASE COURSE; HEART; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; INFLAMMATION; INSULIN RESISTANCE; ISCHEMIA; MITOCHONDRION; MOLECULAR BIOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; RISK FACTOR; THROMBOGENICITY; TRANSCRIPTION REGULATION; VASCULAR DISEASE;

ANIMALS; CARDIOMYOPATHIES; DIABETES MELLITUS, TYPE 2; HUMANS; MITOCHONDRIA, HEART; MODELS, BIOLOGICAL;

EID: 67349249847     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.02.001     Document Type: Review

References (125)

1. Fox C.S., Coady S., Sorlie P.D., D'Agostino Sr. R.B., Pencina M.J., Vasan R.S., Meigs J.B., Levy D., and Savage P.J. Increasing cardiovascular disease burden due to diabetes mellitus: the Framingham Heart Study. Circulation 115 12 (2007) 1544-1550
2. Hossain P., Kawar B., and El Nahas M. Obesity and diabetes in the developing world-a growing challenge. N. Engl. J. Med. 356 3 (2007) 213-215
3. Ludwig S., and Shen G.X. Statins for diabetic cardiovascular complications. Curr. Vasc. Pharmacol. 4 3 (2006) 245-251
4. Goldberg I.J. Why does diabetes increase atherosclerosis? I don't know!. J. Clin. Invest. 114 5 (2004) 613-615
5. Renard C.B., Kramer F., Johansson F., Lamharzi N., Tannock L.R., von Herrath M.G., Chait A., and Bornfeldt K.E. Diabetes and diabetes-associated lipid abnormalities have distinct effects on initiation and progression of atherosclerotic lesions. J. Clin. Invest. 114 5 (2004) 659-668
6. Boudina S., and Abel E.D. Diabetic cardiomyopathy revisited. Circulation 115 25 (2007) 3213-3223
7. Opie L.H. Fuels: aerobic and anaerobic metabolism. In: Opie L.H. (Ed). The heart, physiology, from cell to circulation. 4th edition (2004), Lippincott-Raven, Philadelphia 306-354
8. Lowell B.B., and Shulman G.I. Mitochondrial dysfunction and type 2 diabetes. Science 307 5708 (2005) 384-387
9. Schrauwen-Hinderling V.B., Roden M., Kooi M.E., Hesselink M.K., and Schrauwen P. Muscular mitochondrial dysfunction and type 2 diabetes mellitus. Curr. Opin. Clin. Nutr. Metab. Care 10 6 (2007) 698-703
10. McLeod C.J., Pagel I., and Sack M.N. The mitochondrial biogenesis regulatory program in cardiac adaptation to ischemia-a putative target for therapeutic intervention. Trends Cardiovasc. Med. 15 3 (2005) 118-123
11. Clementi E., and Nisoli E. Nitric oxide and mitochondrial biogenesis: a key to long-term regulation of cellular metabolism. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 142 2 (2005) 102-110
12. Johnson D.T., Harris R.A., French S., Blair P.V., You J., Bemis K., Wang M., and Balaban R.S. The tissue heterogeneity of the mammalian mitochondrial proteome. Am. J. Physiol. Cell Physiol. (2006)
13. Li B., Holloszy J.O., and Semenkovich C.F. Respiratory uncoupling induces delta-aminolevulinate synthase expression through a nuclear respiratory factor-1-dependent mechanism in HeLa cells. J. Biol. Chem. 274 25 (1999) 17534-17540
14. Herzig R.P., Scacco S., and Scarpulla R.C. Sequential serum-dependent activation of CREB and NRF-1 leads to enhanced mitochondrial respiration through the induction of cytochrome c. J. Biol. Chem. 275 17 (2000) 13134-13141
15. Scarpulla R.C. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286 1 (2002) 81-89
16. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., and Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98 1 (1999) 115-124
17. Huss J.M., Torra I.P., Staels B., Giguere V., and Kelly D.P. Estrogen-related receptor {alpha} directs peroxisome proliferator-activated receptor {alpha} signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell Biol. 24 20 (2004) 9079-9091
18. Huss J.M., and Kelly D.P. Nuclear receptor signaling and cardiac energetics. Circ. Res. 95 6 (2004) 568-578
19. St-Pierre J., Lin J., Krauss S., Tarr P.T., Yang R., Newgard C.B., and Spiegelman B.M. Bioenergetic analysis of peroxisome proliferator-activated receptor gamma coactivators 1alpha and 1beta (PGC-1alpha and PGC-1beta) in muscle cells. J. Biol. Chem. 278 29 (2003) 26597-26603
20. McLeod C.J., Aziz A., Hoyt Jr. R.F., McCoy Jr. J.P., and Sack M.N. Uncoupling proteins 2 and 3 function in concert to augment tolerance to cardiac ischemia. J. Biol. Chem. 280 39 (2005) 33470-33476
21. Lehman J.J., Barger P.M., Kovacs A., Saffitz J.E., Medeiros D.M., and Kelly D.P. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106 7 (2000) 847-856
22. Arany Z., He H., Lin J., Hoyer K., Handschin C., Toka O., Ahmad F., Matsui T., Chin S., Wu P.H., Rybkin I.I., Shelton J.M., Manieri M., Cinti S., Schoen F.J., Bassel-Duby R., Rosenzweig A., Ingwall J.S., and Spiegelman B.M. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 1 4 (2005) 259-271
23. Ikeuchi M., Matsusaka H., Kang D., Matsushima S., Ide T., Kubota T., Fujiwara T., Hamasaki N., Takeshita A., Sunagawa K., and Tsutsui H. Overexpression of mitochondrial transcription factor a ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation 112 5 (2005) 683-690
24. Lee H.C., Yin P.H., Lu C.Y., Chi C.W., and Wei Y.H. Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem. J. 348 Pt 2 (2000) 425-432
25. Nisoli E., Clementi E., Paolucci C., Cozzi V., Tonello C., Sciorati C., Bracale R., Valerio A., Francolini M., Moncada S., and Carruba M.O. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299 5608 (2003) 896-899
26. Wright D.C., Geiger P.C., Han D.H., Jones T.E., and Holloszy J.O. Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J. Biol. Chem. 282 26 (2007) 18793-18799
27. Jager S., Handschin C., St-Pierre J., and Spiegelman B.M. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. U. S. A. 104 29 (2007) 12017-12022
28. Weitzel J.M., Iwen K.A., and Seitz H.J. Regulation of mitochondrial biogenesis by thyroid hormone. Exp. Physiol. 88 1 (2003) 121-128
29. Nisoli E., Falcone S., Tonello C., Cozzi V., Palomba L., Fiorani M., Pisconti A., Brunelli S., Cardile A., Francolini M., Cantoni O., Carruba M.O., Moncada S., and Clementi E. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc. Natl. Acad. Sci. U. S. A. 101 47 (2004) 16507-16512
30. Nisoli E., Clementi E., Moncada S., and Carruba M.O. Mitochondrial biogenesis as a cellular signaling framework. Biochem. Pharmacol. 67 1 (2004) 1-15
31. Shiva S., Sack M.N., Greer J.J., Duranski M., Ringwood L.A., Burwell L., Wang X., MacArthur P.H., Shoja A., Raghavachari N., Calvert J.W., Brookes P.S., Lefer D.J., and Gladwin M.T. Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer. J. Exp. Med. 204 9 (2007) 2089-2102
32. Petersen K.F., Dufour S., Savage D.B., Bilz S., Solomon G., Yonemitsu S., Cline G.W., Befroy D., Zemany L., Kahn B.B., Papademetris X., Rothman D.L., and Shulman G.I. The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc. Natl. Acad. Sci. U. S. A. 104 31 (2007) 12587-12594
33. Festa A., Williams K., D'Agostino Jr. R., Wagenknecht L.E., and Haffner S.M. The natural course of beta-cell function in nondiabetic and diabetic individuals: the Insulin Resistance Atherosclerosis Study. Diabetes 55 4 (2006) 1114-1120
34. Bonnard C., Durand A., Peyrol S., Chanseaume E., Chauvin M.A., Morio B., Vidal H., and Rieusset J. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J. Clin. Invest. 118 2 (2008) 789-800
35. Wang H., Knaub L.A., Jensen D.R., Jung D.Y., Hong E.G., Ko H.J., Coates A.M., Goldberg I.J., de la Houssaye B.A., Janssen R.C., McCurdy C.E., Rahman S.M., Choi C.S., Choi C.S., Shulman G.I., Kim J.K., Kim J.K., Friedman J.E., and Eckel R.H. Skeletal muscle-specific deletion of lipoprotein lipase enhances insulin signaling in skeletal muscle but causes insulin resistance in liver and other tissues. Diabetes (2008)
36. Mazumder P.K., O'Neill B.T., Roberts M.W., Buchanan J., Yun U.J., Cooksey R.C., Boudina S., and Abel E.D. Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes 53 9 (2004) 2366-2374
37. Tabbi-Anneni I., Buchanan J., Cooksey R.C., and Abel E.D. Captopril normalizes insulin signaling and insulin-regulated substrate metabolism in obese (ob/ob) mouse hearts. Endocrinology 149 8 (2008) 4043-4050
38. Boudina S., Sena S., O'Neill B.T., Tathireddy P., Young M.E., and Abel E.D. Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 112 17 (2005) 2686-2695
39. Boudina S., Sena S., Theobald H., Sheng X., Wright J.J., Hu X.X., Aziz S., Johnson J.I., Bugger H., Zaha V.G., and Abel E.D. Mitochondrial energetics in the heart in obesity related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes (2007)
40. Bhashyam S., Parikh P., Bolukoglu H., Shannon A.H., Porter J.H., Shen Y.T., and Shannon R.P. Aging is associated with myocardial insulin resistance and mitochondrial dysfunction. Am. J. Physiol. Heart Circ. Physiol. 293 5 (2007) H3063-H3071
41. Yang J., Sambandam N., Han X., Gross R.W., Courtois M., Kovacs A., Febbraio M., Finck B.N., and Kelly D.P. CD36 deficiency rescues lipotoxic cardiomyopathy. Circ. Res. 100 8 (2007) 1208-1217
42. Duncan J.G., Fong J.L., Medeiros D.M., Finck B.N., and Kelly D.P. Insulin-resistant heart exhibits a mitochondrial biogenic response driven by the peroxisome proliferator-activated receptor-alpha/PGC-1alpha gene regulatory pathway. Circulation 115 7 (2007) 909-917
43. Gulick T., Cresci S., Caira T., Moore D.D., and Kelly K.P. The peroxisome proliferator-activated receptor regulates mitochondrial fatty acid oxidative enzyme gene expression. Proc. Natl. Acad. Sci. 91 (1994) 11012-11016
44. Koves T.R., Ussher J.R., Noland R.C., Slentz D., Mosedale M., Ilkayeva O., Bain J., Stevens R., Dyck J.R., Newgard C.B., Lopaschuk G.D., and Muoio D.M. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 7 1 (2008) 45-56
45. Zhang D., Liu Z.X., Choi C.S., Tian L., Kibbey R., Dong J., Cline G.W., Wood P.A., and Shulman G.I. Mitochondrial dysfunction due to long-chain Acyl-CoA dehydrogenase deficiency causes hepatic steatosis and hepatic insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 104 43 (2007) 17075-17080
46. Pagel-Langenickel I., Bao J., Joseph J.J., Schwartz D.R., Mantell B.S., Xu X., Raghavachari N., and Sack M.N. PGC-1alpha integrates insulin signaling, mitochondrial regulation, and bioenergetic function in skeletal muscle. J. Biol. Chem. 283 33 (2008) 22464-22472
47. Shi X., Burkart A., Nicoloro S.M., Czech M.P., Straubhaar J., and Corvera S. Paradoxical effect of mitochondrial respiratory chain impairment on insulin signaling and glucose transport in adipose cells. J. Biol. Chem. 283 45 (2008) 30658-30667
48. Rubler S., Dlugash J., Yuceoglu Y.Z., Kumral T., Branwood A.W., and Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am. J. Cardiol. 30 6 (1972) 595-602
49. Galderisi M., Anderson K.M., Wilson P.W., and Levy D. Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). Am. J. Cardiol. 68 1 (1991) 85-89
50. Ishihara M., Inoue I., Kawagoe T., Shimatani Y., Kurisu S., Nishioka K., Kouno Y., Umemura T., Nakamura S., and Sato H. Diabetes mellitus prevents ischemic preconditioning in patients with a first acute anterior wall myocardial infarction. J. Am. Coll. Cardiol. 38 4 (2001) 1007-1011
51. Poornima I.G., Parikh P., and Shannon R.P. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ. Res. 98 5 (2006) 596-605
52. Lebeche D., Davidoff A.J., and Hajjar R.J. Interplay between impaired calcium regulation and insulin signaling abnormalities in diabetic cardiomyopathy. Nat. Clin. Pract. Cardiovasc. Med. 5 11 (2008) 715-724
53. Desai A., and Fang J.C. Heart failure with preserved ejection fraction: hypertension, diabetes, obesity/sleep apnea, and hypertrophic and infiltrative cardiomyopathy. Heart Fail. Clin. 4 1 (2008) 87-97
54. van Heerebeek L., Hamdani N., Handoko M.L., Falcao-Pires I., Musters R.J., Kupreishvili K., Ijsselmuiden A.J., Schalkwijk C.G., Bronzwaer J.G., Diamant M., Borbely A., van der Velden J., Stienen G.J., Laarman G.J., Niessen H.W., and Paulus W.J. Diastolic stiffness of the failing diabetic heart: importance of fibrosis, advanced glycation end products, and myocyte resting tension. Circulation 117 1 (2008) 43-51
55. McGavock J.M., Lingvay I., Zib I., Tillery T., Salas N., Unger R., Levine B.D., Raskin P., Victor R.G., and Szczepaniak L.S. Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 116 10 (2007) 1170-1175
56. Scheuermann-Freestone M., Madsen P.L., Manners D., Blamire A.M., Buckingham R.E., Styles P., Radda G.K., Neubauer S., and Clarke K. Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes. Circulation 107 24 (2003) 3040-3046
57. How O.J., Aasum E., Severson D.L., Chan W.Y., Essop M.F., and Larsen T.S. Increased myocardial oxygen consumption reduces cardiac efficiency in diabetic mice. Diabetes 55 2 (2006) 466-473
58. Semeniuk L.M., Kryski A.J., and Severson D.L. Echocardiographic assessment of cardiac function in diabetic db/db and transgenic db/db-hGLUT4 mice. Am. J. Physiol. Heart Circ. Physiol. 283 3 (2002) H976-H982
59. Yue P., Arai T., Terashima M., Sheikh A.Y., Cao F., Charo D., Hoyt G., Robbins R.C., Ashley E.A., Wu J., Yang P.C., and Tsao P.S. Magnetic resonance imaging of progressive cardiomyopathic changes in the db/db mouse. Am. J. Physiol. Heart Circ. Physiol. 292 5 (2007) H2106-H2118
60. Belke D.D., Larsen T.S., Gibbs E.M., and Severson D.L. Altered metabolism causes cardiac dysfunction in perfused hearts from diabetic (db/db) mice. Am. J. Physiol. Endocrinol. Metab. 279 5 (2000) E1104-E1113
61. Christoffersen C., Bollano E., Lindegaard M.L., Bartels E.D., Goetze J.P., Andersen C.B., and Nielsen L.B. Cardiac lipid accumulation associated with diastolic dysfunction in obese mice. Endocrinology 144 8 (2003) 3483-3490
62. Mizushige K., Yao L., Noma T., Kiyomoto H., Yu Y., Hosomi N., Ohmori K., and Matsuo H. Alteration in left ventricular diastolic filling and accumulation of myocardial collagen at insulin-resistant prediabetic stage of a type II diabetic rat model. Circulation 101 8 (2000) 899-907
63. Sharma N., Okere I.C., Barrows B.R., Lei B., Duda M.K., Yuan C.L., Previs S.F., Sharov V.G., Azimzadeh A.M., Ernsberger P., Hoit B.D., Sabbah H., and Stanley W.C. High-sugar diets increase cardiac dysfunction and mortality in hypertension compared to low-carbohydrate or high-starch diets. J. Hypertens 26 7 (2008) 1402-1410
64. Sack M.N. Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance. Cardiovasc. Res. 72 2 (2006) 210-219
65. Opie L.H., and Sack M.N. Metabolic plasticity and the promotion of cardiac protection in ischemia and ischemic preconditioning. J. Mol. Cell Cardiol. 34 (2002) 1077-1089
66. Stone P.H., Muller J.E., Hartwell T., York B.J., Rutherford J.D., Parker C.B., Turi Z.G., Strauss H.W., Willerson J.T., Robertson 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. The MILIS Study Group. J. Am. Coll. Cardiol. 14 1 (1989) 49-57
67. Solomon S.D., St John Sutton M., Lamas G.A., Plappert T., Rouleau J.L., Skali H., Moye L., Braunwald E., and Pfeffer M.A. Ventricular remodeling does not accompany the development of heart failure in diabetic patients after myocardial infarction. Circulation 106 10 (2002) 1251-1255
68. Aasum E., Hafstad A.D., Severson D.L., and Larsen T.S. Age-dependent changes in metabolism, contractile function, and ischemic sensitivity in hearts from db/db mice. Diabetes 52 2 (2003) 434-441
69. Panagia M., Schneider J.E., Brown B., Cole M.A., and Clarke K. Abnormal function and glucose metabolism in the type-2 diabetic db/db mouse heart. Can. J. Physiol. Pharmacol. 85 3-4 (2007) 289-294
70. Greer J.J., Ware D.P., and Lefer D.J. Myocardial infarction and heart failure in the db/db diabetic mouse. Am. J. Physiol. Heart Circ. Physiol. 290 1 (2006) H146-H153
71. McGaffin K.R., Sun C.K., Rager J.J., Romano L.C., Zou B., Mathier M.A., O'Doherty R.M., McTiernan C.F., and O'Donnell C.P. Leptin signalling reduces the severity of cardiac dysfunction and remodelling after chronic ischaemic injury. Cardiovasc. Res. 77 1 (2008) 54-63
72. Thakker G.D., Frangogiannis N.G., Bujak M., Zymek P., Gaubatz J.W., Reddy A.K., Taffet G., Michael L.H., Entman M.L., and Ballantyne C.M. Effects of diet-induced obesity on inflammation and remodeling after myocardial infarction. Am. J. Physiol. Heart Circ. Physiol. 291 5 (2006) H2504-H2514
73. Schwartz D.R., and Sack M.N. Targeting the mitochondria to augment myocardial protection. Curr. Opin. Pharmacol. 8 2 (2008) 160-165
74. Wilson-Fritch L., Nicoloro S., Chouinard M., Lazar M.A., Chui P.C., Leszyk J., Straubhaar J., Czech M.P., and Corvera S. Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J. Clin. Invest. 114 9 (2004) 1281-1289
75. How O.J., Larsen T.S., Hafstad A.D., Khalid A., Myhre E.S., Murray A.J., Boardman N.T., Cole M., Clarke K., Severson D.L., and Aasum E. Rosiglitazone treatment improves cardiac efficiency in hearts from diabetic mice. Arch. Physiol. Biochem. 113 4-5 (2007) 211-220
76. Sidell R.J., Cole M.A., Draper N.J., Desrois M., Buckingham R.E., and Clarke K. Thiazolidinedione treatment normalizes insulin resistance and ischemic injury in the Zucker fatty rat heart. Diabetes 51 4 (2002) 1110-1117
77. Lygate C.A., Hulbert K., Monfared M., Cole M.A., Clarke K., and Neubauer S. The PPARgamma-activator rosiglitazone does not alter remodeling but increases mortality in rats post-myocardial infarction. Cardiovasc. Res. 58 3 (2003) 632-637
78. Home P.D., Pocock S.J., Beck-Nielsen H., Gomis R., Hanefeld M., Jones N.P., Komajda M., and McMurray J.J. Rosiglitazone evaluated for cardiovascular outcomes-an interim analysis. N. Engl. J. Med. 357 1 (2007) 28-38
79. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., Geny B., Laakso M., Puigserver P., and Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127 6 (2006) 1109-1122
80. Baur J.A., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., Prabhu V.V., Allard J.S., Lopez-Lluch G., Lewis K., Pistell P.J., Poosala S., Becker K.G., Boss O., Gwinn D., Wang M., Ramaswamy S., Fishbein K.W., Spencer R.G., Lakatta E.G., Le Couteur D., Shaw R.J., Navas P., Puigserver P., Ingram D.K., de Cabo R., and Sinclair D.A. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444 7117 (2006) 337-342
81. Dasgupta B., and Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proc. Natl. Acad. Sci. U. S. A. 104 17 (2007) 7217-7222
82. Baur J.A., and Sinclair D.A. Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov. 5 6 (2006) 493-506
83. Penumathsa S.V., Thirunavukkarasu M., Koneru S., Juhasz B., Zhan L., Pant R., Menon V.P., Otani H., and Maulik N. Statin and resveratrol in combination induces cardioprotection against myocardial infarction in hypercholesterolemic rat. J. Mol. Cell Cardiol. 42 3 (2007) 508-516
84. Goh S.S., Woodman O.L., Pepe S., Cao A.H., Qin C., and Ritchie R.H. The red wine antioxidant resveratrol prevents cardiomyocyte injury following ischemia-reperfusion via multiple sites and mechanisms. Antioxid. Redox Signal 9 1 (2007) 101-113
85. Wood J.G., Rogina B., Lavu S., Howitz K., Helfand S.L., Tatar M., and Sinclair D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430 7000 (2004) 686-689
86. Milne J.C., Lambert P.D., Schenk S., Carney D.P., Smith J.J., Gagne D.J., Jin L., Boss O., Perni R.B., Vu C.B., Bemis J.E., Xie R., Disch J.S., Ng P.Y., Nunes J.J., Lynch A.V., Yang H., Galonek H., Israelian K., Choy W., Iffland A., Lavu S., Medvedik O., Sinclair D.A., Olefsky J.M., Jirousek M.R., Elliott P.J., and Westphal C.H. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450 7170 (2007) 712-716
87. Feige J.N., Lagouge M., Canto C., Strehle A., Houten S.M., Milne J.C., Lambert P.D., Mataki C., Elliott P.J., and Auwerx J. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab. 8 5 (2008) 347-358
88. Schaper J., Meiser E., and Stammler G. Ultrastructural morphometric analysis of myocardium from dogs, rats, hamsters, mice, and from human hearts. Circ. Res. 56 3 (1985) 377-391
89. Leone T.C., Lehman J.J., Finck B.N., Schaeffer P.J., Wende A.R., Boudina S., Courtois M., Wozniak D.F., Sambandam N., Bernal-Mizrachi C., Chen Z., Holloszy J.O., Medeiros D.M., Schmidt R.E., Saffitz J.E., Abel E.D., Semenkovich C.F., and Kelly D.P. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3 4 (2005) e101
90. Suarez J., Hu Y., Makino A., Fricovsky E., Wang H., and Dillmann W.H. Alterations in mitochondrial function and cytosolic calcium induced by hyperglycemia are restored by mitochondrial transcription factor A in cardiomyocytes. Am. J. Physiol. Cell. Physiol. 295 6 (2008) C1561-C1568
91. Finck B.N., Lehman J.J., Leone T.C., Welch M.J., Bennett M.J., Kovacs A., Han X., Gross R.W., Kozak R., Lopaschuk G.D., and Kelly D.P. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J. Clin. Invest. 109 1 (2002) 121-130
92. Finck B.N., Han X., Courtois M., Aimond F., Nerbonne J.M., Kovacs A., Gross R.W., and Kelly D.P. A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc. Natl. Acad. Sci. U. S. A. 100 3 (2003) 1226-1231
93. Yagyu H., Chen G., Yokoyama M., Hirata K., Augustus A., Kako Y., Seo T., Hu Y., Lutz E.P., Merkel M., Bensadoun A., Homma S., and Goldberg I.J. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J. Clin. Invest. 111 3 (2003) 419-426
94. Son N.H., Park T.S., Yamashita H., Yokoyama M., Huggins L.A., Okajima K., Homma S., Szabolcs M.J., Huang L.S., and Goldberg I.J. Cardiomyocyte expression of PPARgamma leads to cardiac dysfunction in mice. J. Clin. Invest. 117 10 (2007) 2791-2801
95. Chiu H.C., Kovacs A., Ford D.A., Hsu F.F., Garcia R., Herrero P., Saffitz J.E., and Schaffer J.E. A novel mouse model of lipotoxic cardiomyopathy. J. Clin. Invest. 107 7 (2001) 813-822
96. Wu P., Sato J., Zhao Y., Jaskiewicz J., Popov K.M., and Harris R.A. Starvation and diabetes increase the amount of pyruvate dehydrogenase kinase isoenzyme 4 in rat heart. Biochem. J. 329 Pt 1 (1998) 197-201
97. Wu P., Inskeep K., Bowker-Kinley M.M., Popov K.M., and Harris R.A. Mechanism responsible for inactivation of skeletal muscle pyruvate dehydrogenase complex in starvation and diabetes. Diabetes 48 8 (1999) 1593-1599
98. Razeghi P., Young M.E., Abbasi S., and Taegtmeyer H. Hypoxia in vivo decreases peroxisome proliferator-activated receptor alpha-regulated gene expression in rat heart. Biochem. Biophys. Res. Commun. 287 1 (2001) 5-10
99. Randle P.J., Garland P.B., Hales C.N., and Newsholme E.A. The glucose fatty-acid cycle, its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1 (1963) 785-789
100. Randle P.J. Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab. Rev. 14 4 (1998) 263-283
101. Hu Y., Suarez J., Fricovsky E., Wang H., Scott B.T., Trauger S.A., Han W., Hu Y., Oyeleye M.O., and Dillmann W.H. Increased Enzymatic O-GlcNAcylation of Mitochondrial Proteins Impairs Mitochondrial Function in Cardiac Myocytes Exposed to High Glucose. J. Biol. Chem. 284 1 (2009) 547-555
102. Jagasia D., Whiting J.M., Concato J., Pfau S., and McNulty P.H. Effect of non-insulin-dependent diabetes mellitus on myocardial insulin responsiveness in patients with ischemic heart disease. Circulation 103 13 (2001) 1734-1739
103. Hafstad A.D., Solevag G.H., Severson D.L., Larsen T.S., and Aasum E. Perfused hearts from Type 2 diabetic (db/db) mice show metabolic responsiveness to insulin. Am. J. Physiol. Heart. Circ. Physiol. 290 5 (2006) H1763-H1769
104. Stanley W.C., Meadows S.R., Kivilo K.M., Roth B.A., and Lopaschuk G.D. beta-Hydroxybutyrate inhibits myocardial fatty acid oxidation in vivo independent of changes in malonyl-CoA content. Am. J. Physiol. Heart Circ. Physiol. 285 4 (2003) H1626-H1631
105. Stowe K.A., Burgess S.C., Merritt M., Sherry A.D., and Malloy C.R. Storage and oxidation of long-chain fatty acids in the C57/BL6 mouse heart as measured by NMR spectroscopy. FEBS Lett. 580 17 (2006) 4282-4287
106. Hasselbaink D.M., Glatz J.F., Luiken J.J., Roemen T.H., and Van der Vusse G.J. Ketone bodies disturb fatty acid handling in isolated cardiomyocytes derived from control and diabetic rats. Biochem. J. 371 Pt 3 (2003) 753-760
107. Boudina S, Bugger H, Sena S, O'Neill BT, Zaha VG, Ilkun O, Wright JJ, Mazumder PK, Palfreyman E, Tidwell TJ, Weimer BC, Abel ED. Contribution of impaired insulin signaling to mitochondrial dysfunction and oxidative stress in the heart. Circulation 2009;In Press.
108. Galderisi M. Diastolic dysfunction and diabetic cardiomyopathy: evaluation by Doppler echocardiography. J. Am. Coll. Cardiol. 48 8 (2006) 1548-1551
109. Haffner S.M., Lehto S., Ronnemaa T., Pyorala K., and Laakso M. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N. Engl. J. Med. 339 4 (1998) 229-234
110. De Groote P., Lamblin N., Mouquet F., Plichon D., McFadden E., Van Belle E., and Bauters C. Impact of diabetes mellitus on long-term survival in patients with congestive heart failure. Eur. Heart J. 25 8 (2004) 656-662
111. Eshaghian S., Horwich T.B., and Fonarow G.C. An unexpected inverse relationship between HbA1c levels and mortality in patients with diabetes and advanced systolic heart failure. Am. Heart J. 151 1 (2006) 91
112. Boudina S., Sena S., Theobald H., Sheng X., Wright J.J., Hu X.X., Aziz S., Johnson J.I., Bugger H., Zaha V.G., and Abel E.D. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 56 10 (2007) 2457-2466
113. Ouwens D.M., Diamant M., Fodor M., Habets D.D., Pelsers M.M., El Hasnaoui M., Dang Z.C., van den Brom C.E., Vlasblom R., Rietdijk A., Boer C., Coort S.L., Glatz J.F., and Luiken J.J. Cardiac contractile dysfunction in insulin-resistant rats fed a high-fat diet is associated with elevated CD36-mediated fatty acid uptake and esterification. Diabetologia 50 9 (2007) 1938-1948
114. Sena S., Rasmussen I.R., Wende A.R., McQueen A.P., Theobald H.A., Wilde N., Pereira R.O., Litwin S.E., Berger J.P., and Abel E.D. Cardiac hypertrophy caused by peroxisome proliferator-activated receptor-gamma agonist treatment occurs independently of changes in myocardial insulin signaling. Endocrinology 148 12 (2007) 6047-6053
115. Waksman J.C. Cardiovascular risk of rosiglitazone: another perspective. J. Pharm. Pharmacol. 60 12 (2008) 1573-1582
116. Burkart E.M., Sambandam N., Han X., Gross R.W., Courtois M., Gierasch C.M., Shoghi K., Welch M.J., and Kelly D.P. Nuclear receptors PPARbeta/delta and PPARalpha direct distinct metabolic regulatory programs in the mouse heart. J. Clin. Invest. 117 12 (2007) 3930-3939
117. Oliver Jr. W.R., Shenk J.L., Snaith M.R., Russell C.S., Plunket K.D., Bodkin N.L., Lewis M.C., Winegar D.A., Sznaidman M.L., Lambert M.H., Xu H.E., Sternbach D.D., Kliewer S.A., Hansen B.C., and Willson T.M. A selective peroxisome proliferator-activated receptor delta agonist promotes reverse cholesterol transport. Proc. Natl. Acad. Sci. U. S. A. 98 9 (2001) 5306-5311
118. Wang Y.X., Zhang C.L., Yu R.T., Cho H.K., Nelson M.C., Bayuga-Ocampo C.R., Ham J., Kang H., and Evans R.M. Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol. 2 10 (2004) e294
119. Riserus U., Sprecher D., Johnson T., Olson E., Hirschberg S., Liu A., Fang Z., Hegde P., Richards D., Sarov-Blat L., Strum J.C., Basu S., Cheeseman J., Fielding B.A., Humphreys S.M., Danoff T., Moore N.R., Murgatroyd P., O'Rahilly S., Sutton P., Willson T., Hassall D., Frayn K.N., and Karpe F. Activation of peroxisome proliferator-activated receptor (PPAR)delta promotes reversal of multiple metabolic abnormalities, reduces oxidative stress, and increases fatty acid oxidation in moderately obese men. Diabetes 57 2 (2008) 332-339
120. Pesant M., Sueur S., Dutartre P., Tallandier M., Grimaldi P.A., Rochette L., and Connat J.L. Peroxisome proliferator-activated receptor delta (PPARdelta) activation protects H9c2 cardiomyoblasts from oxidative stress-induced apoptosis. Cardiovasc. Res. 69 2 (2006) 440-449
121. Ye G., Metreveli N.S., Donthi R.V., Xia S., Xu M., Carlson E.C., and Epstein P.N. Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes 53 5 (2004) 1336-1343
122. Orchard T.J., Temprosa M., Goldberg R., Haffner S., Ratner R., Marcovina S., and Fowler S. The effect of metformin and intensive lifestyle intervention on the metabolic syndrome: the Diabetes Prevention Program randomized trial. Ann. Intern. Med. 142 8 (2005) 611-619
123. Toledo F.G., Menshikova E.V., Ritov V.B., Azuma K., Radikova Z., DeLany J., and Kelley D.E. Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes. Diabetes 56 8 (2007) 2142-2147
124. Li G., Zhang P., Wang J., Gregg E.W., Yang W., Gong Q., Li H., Li H., Jiang Y., An Y., Shuai Y., Zhang B., Zhang J., Thompson T.J., Gerzoff R.B., Roglic G., Hu Y., and Bennett P.H. The long-term effect of lifestyle interventions to prevent diabetes in the China Da Qing Diabetes Prevention Study: a 20-year follow-up study. Lancet 371 9626 (2008) 1783-1789
125. Leichman J.G., Wilson E.B., Scarborough T., Aguilar D., Miller III C.C., Yu S., Algahim M.F., Reyes M., Moody F.G., and Taegtmeyer H. Dramatic reversal of derangements in muscle metabolism and left ventricular function after bariatric surgery. Am. J. Med. 121 11 (2008) 966-973