Mitochondrial dysfunction and its impact on diabetic heart

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1863, Issue 5, 2017, Pages 1098-1105

  Verma, Suresh Kumar ^a   Garikipati, Venkata Naga Srikanth ^a   Kishore, Raj ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Diabetes; Heart failure; miRNAs; Mitochondria; Oxidative stress; ROS

Indexed keywords

MICRORNA;

ARTICLE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CRITICAL ILLNESS; DIABETES MELLITUS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; HUMAN; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROSPECTIVE STUDY; ANIMAL; CARDIAC MUSCLE; CORONARY ARTERY DISEASE; DIABETIC CARDIOMYOPATHY; HEART MITOCHONDRION; HYPERTENSION; METABOLISM; PATHOLOGY;

ANIMALS; CORONARY ARTERY DISEASE; DIABETIC CARDIOMYOPATHIES; HUMANS; HYPERTENSION; MITOCHONDRIA, HEART; MYOCARDIUM; OXIDATIVE STRESS;

EID: 84992709238     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2016.08.021     Document Type: Article

References (141)

1. [1] Mozaffarian, D., Benjamin, E.J., Go, A.S., Arnett, D.K., Blaha, M.J., Cushman, M., de Ferranti, S., Despres, J.P., Fullerton, H.J., Howard, V.J., Huffman, M.D., Judd, S.E., Kissela, B.M., Lackland, D.T., Lichtman, J.H., Lisabeth, L.D., Liu, S., Mackey, R.H., Matchar, D.B., McGuire, D.K., Mohler, E.R. III, Moy, C.S., Muntner, P., Mussolino, M.E., Nasir, K., Neumar, R.W., Nichol, G., Palaniappan, L., Pandey, D.K., Reeves, M.J., Rodriguez, C.J., Sorlie, P.D., Stein, J., Towfighi, A., Turan, T.N., Virani, S.S., Willey, J.Z., Woo, D., Yeh, R.W., Turner, M.B., C. American Heart Association Statistics, S. Stroke Statistics, Heart disease and stroke statistics—2015 update: a report from the American Heart Association. Circulation 131 (2015), e29–322.
2. [2] Engelgau, M.M., Geiss, L.S., Saaddine, J.B., Boyle, J.P., Benjamin, S.M., Gregg, E.W., Tierney, E.F., Rios-Burrows, N., Mokdad, A.H., Ford, E.S., Imperatore, G., Narayan, K.M., The evolving diabetes burden in the United States. Ann. Intern. Med. 140 (2004), 945–950.
3. [3] King, H., Aubert, R.E., Herman, W.H., Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projections. Diabetes Care 21 (1998), 1414–1431.
4. [4] Kearney, M.T., Chronic heart failure and type 2 diabetes mellitus: the last battle?. Diab. Vasc. Dis. Res. 12 (2015), 226–227.
5. [5] Liang, Q., Kobayashi, S., Mitochondrial quality control in the diabetic heart. J. Mol. Cell. Cardiol. 95 (2016), 57–69.
6. [6] Cubbon, R.M., Woolston, A., Adams, B., Gale, C.P., Gilthorpe, M.S., Baxter, P.D., Kearney, L.C., Mercer, B., Rajwani, A., Batin, P.D., Kahn, M., Sapsford, R.J., Witte, K.K., Kearney, M.T., Prospective development and validation of a model to predict heart failure hospitalisation. Heart 100 (2014), 923–929.
7. [7] Cohen-Solal, A., Beauvais, F., Logeart, D., Heart failure and diabetes mellitus: epidemiology and management of an alarming association. J. Card. Fail. 14 (2008), 615–625.
8. [8] Ho, K.K., Pinsky, J.L., Kannel, W.B., Levy, D., The epidemiology of heart failure: the Framingham Study. J. Am. Coll. Cardiol. 22 (1993), 6A–13A.
9. [9] Bell, D.S., Heart failure: the frequent, forgotten, and often fatal complication of diabetes. Diabetes Care 26 (2003), 2433–2441.
10. [10] Schilling, J.D., The mitochondria in diabetic heart failure: from pathogenesis to therapeutic promise. Antioxid. Redox Signal. 22 (2015), 1515–1526.
11. [11] Sivitz, W.I., Yorek, M.A., Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid. Redox Signal. 12 (2010), 537–577.
12. [12] Huss, J.M., Kelly, D.P., Mitochondrial energy metabolism in heart failure: a question of balance. J. Clin. Invest. 115 (2005), 547–555.
13. [13] Tomita, M., Mukae, S., Geshi, E., Umetsu, K., Nakatani, M., Katagiri, T., Mitochondrial respiratory impairment in streptozotocin-induced diabetic rat heart. Jpn. Circ. J. 60 (1996), 673–682.
14. [14] Bugger, H., Abel, E.D., Molecular mechanisms for myocardial mitochondrial dysfunction in the metabolic syndrome. Clin. Sci. 114 (2008), 195–210.
15. [15] Frustaci, A., Kajstura, J., Chimenti, C., Jakoniuk, I., Leri, A., Maseri, A., Nadal-Ginard, B., Anversa, P., Myocardial cell death in human diabetes. Circ. Res. 87 (2000), 1123–1132.
16. [16] Shen, X., Zheng, S., Metreveli, N.S., Epstein, P.N., Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes 55 (2006), 798–805.
17. [17] Fiordaliso, F., Bianchi, R., Staszewsky, L., Cuccovillo, I., Doni, M., Laragione, T., Salio, M., Savino, C., Melucci, S., Santangelo, F., Scanziani, E., Masson, S., Ghezzi, P., Latini, R., Antioxidant treatment attenuates hyperglycemia-induced cardiomyocyte death in rats. J. Mol. Cell. Cardiol. 37 (2004), 959–968.
18. [18] Lonn, E., Bosch, J., Yusuf, S., Sheridan, P., Pogue, J., Arnold, J.M., Ross, C., Arnold, A., Sleight, P., Probstfield, J., Dagenais, G.R., Hope, H.-T.T. Investigators, Effects of long-term vitamin E supplementation on cardiovascular events and cancer: a randomized controlled trial. JAMA 293 (2005), 1338–1347.
19. [19] Yusuf, S., Dagenais, G., Pogue, J., Bosch, J., Sleight, P., Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N. Engl. J. Med. 342 (2000), 154–160.
20. [20] Lathief, S., Inzucchi, S.E., Approach to diabetes management in patients with CVD. Trends Cardiovasc. Med. 26 (2016), 165–179.
21. [21] Hafstad, A.D., Khalid, A.M., Hagve, M., Lund, T., Larsen, T.S., Severson, D.L., Clarke, K., Berge, R.K., Aasum, E., Cardiac peroxisome proliferator-activated receptor-alpha activation causes increased fatty acid oxidation, reducing efficiency and post-ischaemic functional loss. Cardiovasc. Res. 83 (2009), 519–526.
22. [22] Malfitano, C., de Souza Junior, A.L., Carbonaro, M., Bolsoni-Lopes, A., Figueroa, D., de Souza, L.E., Silva, K.A., Consolim-Colombo, F., Curi, R., Irigoyen, M.C., Glucose and fatty acid metabolism in infarcted heart from streptozotocin-induced diabetic rats after 2 weeks of tissue remodeling. Cardiovasc. Diabetol., 14, 2015, 149.
23. [23] Goyal, B.R., Mehta, A.A., Diabetic cardiomyopathy: pathophysiological mechanisms and cardiac dysfuntion. Hum. Exp. Toxicol. 32 (2013), 571–590.
24. [24] Banke, N.H., Wende, A.R., Leone, T.C., O'Donnell, J.M., Abel, E.D., Kelly, D.P., Lewandowski, E.D., Preferential oxidation of triacylglyceride-derived fatty acids in heart is augmented by the nuclear receptor PPARalpha. Circ. Res. 107 (2010), 233–241.
25. [25] Kolwicz, S.C. Jr., Liu, L., Goldberg, I.J., Tian, R., Enhancing cardiac triacylglycerol metabolism improves recovery from ischemic stress. Diabetes 64 (2015), 2817–2827.
26. [26] Sharma, S., Adrogue, J.V., Golfman, L., Uray, I., Lemm, J., Youker, K., Noon, G.P., Frazier, O.H., Taegtmeyer, H., Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. FASEB J. 18 (2004), 1692–1700.
27. [27] Dewald, O., Sharma, S., Adrogue, J., Salazar, R., Duerr, G.D., Crapo, J.D., Entman, M.L., Taegtmeyer, H., Downregulation of peroxisome proliferator-activated receptor-alpha gene expression in a mouse model of ischemic cardiomyopathy is dependent on reactive oxygen species and prevents lipotoxicity. Circulation 112 (2005), 407–415.
28. [28] Niu, Y.G., Evans, R.D., Myocardial metabolism of triacylglycerol-rich lipoproteins in type 2 diabetes. J. Physiol. 587 (2009), 3301–3315.
29. [29] Stanley, W.C., Chandler, M.P., Energy metabolism in the normal and failing heart: potential for therapeutic interventions. Heart Fail. Rev. 7 (2002), 115–130.
30. [30] Mori, J., Basu, R., McLean, B.A., Das, S.K., Zhang, L., Patel, V.B., Wagg, C.S., Kassiri, Z., Lopaschuk, G.D., Oudit, G.Y., Agonist-induced hypertrophy and diastolic dysfunction are associated with selective reduction in glucose oxidation: a metabolic contribution to heart failure with normal ejection fraction. Circ. Heart Fail. 5 (2012), 493–503.
31. [31] Pellieux, C., Montessuit, C., Papageorgiou, I., Pedrazzini, T., Lerch, R., Differential effects of high-fat diet on myocardial lipid metabolism in failing and nonfailing hearts with angiotensin II-mediated cardiac remodeling in mice. Am. J. Physiol. Heart Circ. Physiol. 302 (2012), H1795–H1805.
32. [32] Ardehali, H., Sabbah, H.N., Burke, M.A., Sarma, S., Liu, P.P., Cleland, J.G., Maggioni, A., Fonarow, G.C., Abel, E.D., Campia, U., Gheorghiade, M., Targeting myocardial substrate metabolism in heart failure: potential for new therapies. Eur. J. Heart Fail. 14 (2012), 120–129.
33. [33] Abdurrachim, D., Luiken, J.J., Nicolay, K., Glatz, J.F., Prompers, J.J., Nabben, M., Good and bad consequences of altered fatty acid metabolism in heart failure: evidence from mouse models. Cardiovasc. Res. 106 (2015), 194–205.
34. [34] Nickel, A., Loffler, J., Maack, C., Myocardial energetics in heart failure. Basic Res. Cardiol., 108, 2013, 358.
35. [35] Wisneski, J.A., Gertz, E.W., Neese, R.A., Mayr, M., Myocardial metabolism of free fatty acids. Studies with 14C-labeled substrates in humans. J. Clin. Invest. 79 (1987), 359–366.
36. [36] Bing, R.J., Siegel, A., Ungar, I., Gilbert, M., Metabolism of the human heart. II. Studies on fat, ketone and amino acid metabolism. Am. J. Med. 16 (1954), 504–515.
37. [37] Doenst, T., Nguyen, T.D., Abel, E.D., Cardiac metabolism in heart failure: implications beyond ATP production. Circ. Res. 113 (2013), 709–724.
38. [38] Doenst, T., Pytel, G., Schrepper, A., Amorim, P., Farber, G., Shingu, Y., Mohr, F.W., Schwarzer, M., Decreased rates of substrate oxidation ex vivo predict the onset of heart failure and contractile dysfunction in rats with pressure overload. Cardiovasc. Res. 86 (2010), 461–470.
39. [39] Kato, T., Niizuma, S., Inuzuka, Y., Kawashima, T., Okuda, J., Tamaki, Y., Iwanaga, Y., Narazaki, M., Matsuda, T., Soga, T., Kita, T., Kimura, T., Shioi, T., Analysis of metabolic remodeling in compensated left ventricular hypertrophy and heart failure. Circ. Heart Fail. 3 (2010), 420–430.
40. [40] Heather, L.C., Cole, M.A., Lygate, C.A., Evans, R.D., Stuckey, D.J., Murray, A.J., Neubauer, S., Clarke, K., Fatty acid transporter levels and palmitate oxidation rate correlate with ejection fraction in the infarcted rat heart. Cardiovasc. Res. 72 (2006), 430–437.
41. [41] Siddiqi, N., Singh, S., Beadle, R., Dawson, D., Frenneaux, M., Cardiac metabolism in hypertrophy and heart failure: implications for therapy. Heart Fail. Rev. 18 (2013), 595–606.
42. [42] Osorio, J.C., Stanley, W.C., Linke, A., Castellari, M., Diep, Q.N., Panchal, A.R., Hintze, T.H., Lopaschuk, G.D., Recchia, F.A., Impaired myocardial fatty acid oxidation and reduced protein expression of retinoid X receptor-alpha in pacing-induced heart failure. Circulation 106 (2002), 606–612.
43. [43] Zhabyeyev, P., Gandhi, M., Mori, J., Basu, R., Kassiri, Z., Clanachan, A., Lopaschuk, G.D., Oudit, G.Y., Pressure-overload-induced heart failure induces a selective reduction in glucose oxidation at physiological afterload. Cardiovasc. Res. 97 (2013), 676–685.
44. [44] Pereira, R.O., Wende, A.R., Olsen, C., Soto, J., Rawlings, T., Zhu, Y., Riehle, C., Abel, E.D., GLUT1 deficiency in cardiomyocytes does not accelerate the transition from compensated hypertrophy to heart failure. J. Mol. Cell. Cardiol. 72 (2014), 95–103.
45. [45] Sankaralingam, S., Lopaschuk, G.D., Cardiac energy metabolic alterations in pressure overload-induced left and right heart failure (2013 Grover Conference Series). Pulm. Circ. 5 (2015), 15–28.
46. [46] Amorim, P.A., Nguyen, T.D., Shingu, Y., Schwarzer, M., Mohr, F.W., Schrepper, A., Doenst, T., Myocardial infarction in rats causes partial impairment in insulin response associated with reduced fatty acid oxidation and mitochondrial gene expression. J. Thorac. Cardiovasc. Surg. 140 (2010), 1160–1167.
47. [47] Dai, D.F., Hsieh, E.J., Liu, Y., Chen, T., Beyer, R.P., Chin, M.T., MacCoss, M.J., Rabinovitch, P.S., Mitochondrial proteome remodelling in pressure overload-induced heart failure: the role of mitochondrial oxidative stress. Cardiovasc. Res. 93 (2012), 79–88.
48. [48] Davila-Roman, V.G., Vedala, G., Herrero, P., de las Fuentes, L., Rogers, J.G., Kelly, D.P., Gropler, R.J., Altered myocardial fatty acid and glucose metabolism in idiopathic dilated cardiomyopathy. J. Am. Coll. Cardiol. 40 (2002), 271–277.
49. [49] Patti, M.E., Butte, A.J., Crunkhorn, S., Cusi, K., Berria, R., Kashyap, S., Miyazaki, Y., Kohane, I., Costello, M., Saccone, R., Landaker, E.J., Goldfine, A.B., Mun, E., DeFronzo, R., Finlayson, J., Kahn, C.R., Mandarino, L.J., Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 8466–8471.
50. [50] Kristensen, J.M., Skov, V., Petersson, S.J., Ortenblad, N., Wojtaszewski, J.F., Beck-Nielsen, H., Hojlund, K., A PGC-1alpha- and muscle fibre type-related decrease in markers of mitochondrial oxidative metabolism in skeletal muscle of humans with inherited insulin resistance. Diabetologia 57 (2014), 1006–1015.
51. [51] Pitocco, D., Tesauro, M., Alessandro, R., Ghirlanda, G., Cardillo, C., Oxidative stress in diabetes: implications for vascular and other complications. Int. J. Mol. Sci. 14 (2013), 21525–21550.
52. [52] Finck, B.N., Kelly, D.P., PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116 (2006), 615–622.
53. [53] Morino, K., Petersen, K.F., Dufour, S., Befroy, D., Frattini, J., Shatzkes, N., Neschen, S., White, M.F., Bilz, S., Sono, S., Pypaert, M., Shulman, G.I., Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J. Clin. Invest. 115 (2005), 3587–3593.
54. [54] Petersen, K.F., Dufour, S., Befroy, D., Garcia, R., Shulman, G.I., Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350 (2004), 664–671.
55. [55] Ritov, V.B., Menshikova, E.V., He, J., Ferrell, R.E., Goodpaster, B.H., Kelley, D.E., Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54 (2005), 8–14.
56. [56] Kelley, D.E., He, J., Menshikova, E.V., Ritov, V.B., Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51 (2002), 2944–2950.
57. [57] Shen, X., Zheng, S., Thongboonkerd, V., Xu, M., Pierce, W.M. Jr., Klein, J.B., Epstein, P.N., Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am. J. Physiol. Endocrinol. Metab. 287 (2004), E896–E905.
58. [58] Pham, T., Loiselle, D., Power, A., Hickey, A.J., Mitochondrial inefficiencies and anoxic ATP hydrolysis capacities in diabetic rat heart. Am. J. Physiol. Cell Physiol. 307 (2014), C499–C507.
59. [59] Boudina, S., Sena, S., O'Neill, B.T., Tathireddy, P., Young, M.E., Abel, E.D., Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 112 (2005), 2686–2695.
60. [60] Kuo, T.H., Moore, K.H., Giacomelli, F., Wiener, J., Defective oxidative metabolism of heart mitochondria from genetically diabetic mice. Diabetes 32 (1983), 781–787.
61. [61] Buler, M., Aatsinki, S.M., Izzi, V., Uusimaa, J., Hakkola, J., SIRT5 is under the control of PGC-1alpha and AMPK and is involved in regulation of mitochondrial energy metabolism. FASEB J. 28 (2014), 3225–3237.
62. [62] Martin, O.J., Lai, L., Soundarapandian, M.M., Leone, T.C., Zorzano, A., Keller, M.P., Attie, A.D., Muoio, D.M., Kelly, D.P., A role for peroxisome proliferator-activated receptor gamma coactivator-1 in the control of mitochondrial dynamics during postnatal cardiac growth. Circ. Res. 114 (2014), 626–636.
63. [63] Mitra, R., Nogee, D.P., Zechner, J.F., Yea, K., Gierasch, C.M., Kovacs, A., Medeiros, D.M., Kelly, D.P., Duncan, J.G., The transcriptional coactivators, PGC-1alpha and beta, cooperate to maintain cardiac mitochondrial function during the early stages of insulin resistance. J. Mol. Cell. Cardiol. 52 (2012), 701–710.
64. [64] Duncan, J.G., Fong, J.L., Medeiros, D.M., Finck, B.N., 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 (2007), 909–917.
65. [65] Diamant, M., Lamb, H.J., Groeneveld, Y., Endert, E.L., Smit, J.W., Bax, J.J., Romijn, J.A., de Roos, A., Radder, J.K., Diastolic dysfunction is associated with altered myocardial metabolism in asymptomatic normotensive patients with well-controlled type 2 diabetes mellitus. J. Am. Coll. Cardiol. 42 (2003), 328–335.
66. [66] L. Banks, G.D. Wells, B.W. McCrindle, Cardiac energy metabolism is positively associated with skeletal muscle energy metabolism in physically active adolescents and young adults, Appl. Physiol. Nutr. Metab. = Physiologie Appliquee, Nutrition et Metabolisme, 39 (2014) 363–368.
67. [67] Scheuermann-Freestone, M., Madsen, P.L., Manners, D., Blamire, A.M., Buckingham, R.E., Styles, P., Radda, G.K., Neubauer, S., Clarke, K., Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes. Circulation 107 (2003), 3040–3046.
68. [68] Elezaby, A., Sverdlov, A.L., Tu, V.H., Soni, K., Luptak, I., Qin, F., Liesa, M., Shirihai, O.S., Rimer, J., Schaffer, J.E., Colucci, W.S., Miller, E.J., Mitochondrial remodeling in mice with cardiomyocyte-specific lipid overload. J. Mol. Cell. Cardiol. 79 (2015), 275–283.
69. [69] Anderson, E.J., Kypson, A.P., Rodriguez, E., Anderson, C.A., Lehr, E.J., Neufer, P.D., Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. J. Am. Coll. Cardiol. 54 (2009), 1891–1898.
70. [70] Margulies, K.B., Evolving challenges for targeting metabolic abnormalities in heart failure. JACC Heart Fail. 4 (2016), 567–569.
71. [71] Taegtmeyer, H., Golfman, L., Sharma, S., Razeghi, P., van Arsdall, M., Linking gene expression to function: metabolic flexibility in the normal and diseased heart. Ann. N. Y. Acad. Sci. 1015 (2004), 202–213.
72. [72] Neely, J.R., Rovetto, M.J., Oram, J.F., Myocardial utilization of carbohydrate and lipids. Prog. Cardiovasc. Dis. 15 (1972), 289–329.
73. [73] Sack, M.N., Rader, T.A., Park, S., Bastin, J., McCune, S.A., Kelly, D.P., Fatty acid oxidation enzyme gene expression is downregulated in the failing heart. Circulation 94 (1996), 2837–2842.
74. [74] Nikolaidis, L.A., Sturzu, A., Stolarski, C., Elahi, D., Shen, Y.T., Shannon, R.P., The development of myocardial insulin resistance in conscious dogs with advanced dilated cardiomyopathy. Cardiovasc. Res. 61 (2004), 297–306.
75. [75] Doehner, W., Rauchhaus, M., Ponikowski, P., Godsland, I.F., von Haehling, S., Okonko, D.O., Leyva, F., Proudler, A.J., Coats, A.J., Anker, S.D., Impaired insulin sensitivity as an independent risk factor for mortality in patients with stable chronic heart failure. J. Am. Coll. Cardiol. 46 (2005), 1019–1026.
76. [76] Banke, N.H., Lewandowski, E.D., Impaired cytosolic NADH shuttling and elevated UCP3 contribute to inefficient citric acid cycle flux support of postischemic cardiac work in diabetic hearts. J. Mol. Cell. Cardiol. 79 (2015), 13–20.
77. [77] Buchanan, J., Mazumder, P.K., Hu, P., Chakrabarti, G., Roberts, M.W., Yun, U.J., Cooksey, R.C., Litwin, S.E., Abel, E.D., 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 146 (2005), 5341–5349.
78. [78] Mazumder, P.K., O'Neill, B.T., Roberts, M.W., Buchanan, J., Yun, U.J., Cooksey, R.C., Boudina, S., Abel, E.D., Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes 53 (2004), 2366–2374.
79. [79] Skulachev, V.P., Uncoupling: new approaches to an old problem of bioenergetics. Biochim. Biophys. Acta 1363 (1998), 100–124.
80. [80] Boudina, S., Sena, S., Theobald, H., Sheng, X., Wright, J.J., Hu, X.X., Aziz, S., Johnson, J.I., Bugger, H., Zaha, V.G., 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 (2007), 2457–2466.
81. [81] Akhmedov, A.T., Rybin, V., Marin-Garcia, J., Mitochondrial oxidative metabolism and uncoupling proteins in the failing heart. Heart Fail. Rev. 20 (2015), 227–249.
82. [82] Tsutsui, H., Kinugawa, S., Matsushima, S., Oxidative stress and mitochondrial DNA damage in heart failure. Circ. J. 72:Suppl. A (2008), A31–A37.
83. [83] Siebels, I., Drose, S., Q-site inhibitor induced ROS production of mitochondrial complex II is attenuated by TCA cycle dicarboxylates. Biochim. Biophys. Acta 1827 (2013), 1156–1164.
84. [84] Ide, T., Tsutsui, H., Kinugawa, S., Utsumi, H., Kang, D., Hattori, N., Uchida, K., Arimura, K., Egashira, K., Takeshita, A., Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ. Res. 85 (1999), 357–363.
85. [85] Bayeva, M., Gheorghiade, M., Ardehali, H., Mitochondria as a therapeutic target in heart failure. J. Am. Coll. Cardiol. 61 (2013), 599–610.
86. [86] Sung, H.J., Ma, W., Wang, P.Y., Hynes, J., O'Riordan, T.C., Combs, C.A., McCoy, J.P. Jr., Bunz, F., Kang, J.G., Hwang, P.M., Mitochondrial respiration protects against oxygen-associated DNA damage. Nat. Commun., 1, 2010, 5.
87. [87] Ide, T., Tsutsui, H., Hayashidani, S., Kang, D., Suematsu, N., Nakamura, K., Utsumi, H., Hamasaki, N., Takeshita, A., Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ. Res. 88 (2001), 529–535.
88. [88] Dymkowska, D., Drabarek, B., Podszywalow-Bartnicka, P., Szczepanowska, J., Zablocki, K., Hyperglycaemia modifies energy metabolism and reactive oxygen species formation in endothelial cells in vitro. Arch. Biochem. Biophys. 542 (2014), 7–13.
89. [89] Glushakova, L.G., Judge, S., Cruz, A., Pourang, D., Mathews, C.E., Stacpoole, P.W., Increased superoxide accumulation in pyruvate dehydrogenase complex deficient fibroblasts. Mol. Genet. Metab. 104 (2011), 255–260.
90. [90] Remor, A.P., de Matos, F.J., Ghisoni, K., da Silva, T.L., Eidt, G., Burigo, M., de Bem, A.F., Silveira, P.C., de Leon, A., Sanchez, M.C., Hohl, A., Glaser, V., Goncalves, C.A., Quincozes-Santos, A., Borba Rosa, R., Latini, A., Differential effects of insulin on peripheral diabetes-related changes in mitochondrial bioenergetics: involvement of advanced glycosylated end products. Biochim. Biophys. Acta 1812 (2011), 1460–1471.
91. [91] Nishikawa, T., Edelstein, D., Du, X.L., Yamagishi, S., Matsumura, T., Kaneda, Y., Yorek, M.A., Beebe, D., Oates, P.J., Hammes, H.P., Giardino, I., Brownlee, M., Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404 (2000), 787–790.
92. [92] Munasinghe, P.E., Riu, F., Dixit, P., Edamatsu, M., Saxena, P., Hamer, N.S., Galvin, I.F., Bunton, R.W., Lequeux, S., Jones, G., Lamberts, R.R., Emanueli, C., Madeddu, P., Katare, R., Type-2 diabetes increases autophagy in the human heart through promotion of Beclin-1 mediated pathway. Int. J. Cardiol. 202 (2016), 13–20.
93. [93] Han, S.S., Wang, G., Jin, Y., Ma, Z.L., Jia, W.J., Wu, X., Wang, X.Y., He, M.Y., Cheng, X., Li, W.J., Yang, X., Liu, G.S., Investigating the mechanism of hyperglycemia-induced fetal cardiac hypertrophy. PLoS One, 10, 2015, e0139141.
94. [94] Cai, L., Wang, J., Li, Y., Sun, X., Wang, L., Zhou, Z., Kang, Y.J., Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy. Diabetes 54 (2005), 1829–1837.
95. [95] Ye, G., Metreveli, N.S., Donthi, R.V., Xia, S., Xu, M., Carlson, E.C., Epstein, P.N., Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes 53 (2004), 1336–1343.
96. [96] Yildirim, S.S., Akman, D., Catalucci, D., Turan, B., Relationship between downregulation of miRNAs and increase of oxidative stress in the development of diabetic cardiac dysfunction: junctin as a target protein of miR-1. Cell Biochem. Biophys. 67 (2013), 1397–1408.
97. [97] Baseler, W.A., Thapa, D., Jagannathan, R., Dabkowski, E.R., Croston, T.L., Hollander, J.M., miR-141 as a regulator of the mitochondrial phosphate carrier (Slc25a3) in the type 1 diabetic heart. Am. J. Physiol 303 (2012), C1244–C1251.
98. [98] Garikipati, V.N., Krishnamurthy, P., Verma, S.K., Khan, M., Abramova, T., Mackie, A.R., Qin, G., Benedict, C., Nickoloff, E., Johnson, J., Gao, E., Losordo, D.W., Houser, S.R., Koch, W.J., Kishore, R., Negative regulation of miR-375 by interleukin-10 enhances bone marrow-derived progenitor cell-mediated myocardial repair and function after myocardial infarction. Stem Cells 33 (2015), 3519–3529.
99. [99] Joladarashi, D., Srikanth Garikipati, V.N., Thandavarayan, R.A., Verma, S.K., Mackie, A.R., Khan, M., Gumpert, A.M., Bhimaraj, A., Youker, K.A., Uribe, C., Suresh Babu, S., Jeyabal, P., Kishore, R., Krishnamurthy, P., Enhanced cardiac regenerative ability of stem cells after ischemia–reperfusion injury: role of human CD34 + cells deficient in microRNA-377. J. Am. Coll. Cardiol. 66 (2015), 2214–2226.
100. [100] Khan, M., Nickoloff, E., Abramova, T., Johnson, J., Verma, S.K., Krishnamurthy, P., Mackie, A.R., Vaughan, E., Garikipati, V.N., Benedict, C., Ramirez, V., Lambers, E., Ito, A., Gao, E., Misener, S., Luongo, T., Elrod, J., Qin, G., Houser, S.R., Koch, W.J., Kishore, R., Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ. Res. 117 (2015), 52–64.
101. [101] Sahoo, S., Klychko, E., Thorne, T., Misener, S., Schultz, K.M., Millay, M., Ito, A., Liu, T., Kamide, C., Agrawal, H., Perlman, H., Qin, G., Kishore, R., Losordo, D.W., Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ. Res. 109 (2011), 724–728.
102. [102] Bartel, D.P., MicroRNAs: target recognition and regulatory functions. Cell 136 (2009), 215–233.
103. [103] Krol, J., Loedige, I., Filipowicz, W., The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11 (2010), 597–610.
104. [104] Almeida, M.I., Reis, R.M., Calin, G.A., MicroRNA history: discovery, recent applications, and next frontiers. Mutat. Res. 717 (2011), 1–8.
105. [105] Gregory, R.I., Yan, K.P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N., Shiekhattar, R., The Microprocessor complex mediates the genesis of microRNAs. Nature 432 (2004), 235–240.
106. [106] Han, J., Lee, Y., Yeom, K.H., Kim, Y.K., Jin, H., Kim, V.N., The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18 (2004), 3016–3027.
107. [107] Lee, Y., Kim, M., Han, J., Yeom, K.H., Lee, S., Baek, S.H., Kim, V.N., MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23 (2004), 4051–4060.
108. [108] Jiang, X.X., Su, Y.F., Li, X.S., Zhang, Y., Wu, Y., Mao, N., Human fetal heart-derived adherent cells with characteristics similar to mesenchymal progenitor cells. Zhongguo Shi Yan Xue Ye Xue Za Zhi 14 (2006), 1191–1194.
109. [109] Kim, V.N., Han, J., Siomi, M.C., Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10 (2009), 126–139.
110. [110] Chi, S.W., Zang, J.B., Mele, A., Darnell, R.B., Argonaute HITS-CLIP decodes microRNA–mRNA interaction maps. Nature 460 (2009), 479–486.
111. [111] H. Guo, N.T. Ingolia, J.S. Weissman, D.P. Bartel, Mammalian microRNAs predominantly act to decrease target mRNA levels, Nature, 466, 835–840.
112. [112] Hendrickson, D.G., Hogan, D.J., McCullough, H.L., Myers, J.W., Herschlag, D., Ferrell, J.E., Brown, P.O., Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol., 7, 2009, e1000238.
113. [113] Lu, H., Buchan, R.J., Cook, S.A., MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc. Res. 86 (2010), 410–420.
114. [114] Shan, Z.X., Lin, Q.X., Deng, C.Y., Zhu, J.N., Mai, L.P., Liu, J.L., Fu, Y.H., Liu, X.Y., Li, Y.X., Zhang, Y.Y., Lin, S.G., Yu, X.Y., miR-1/miR-206 regulate Hsp60 expression contributing to glucose-mediated apoptosis in cardiomyocytes. FEBS Lett. 584 (2010), 3592–3600.
115. [115] Costantino, S., Paneni, F., Luscher, T.F., Cosentino, F., MicroRNA profiling unveils hyperglycaemic memory in the diabetic heart. Eur. Heart J. 37 (2016), 572–576.
116. [116] Belke, D.D., Larsen, T.S., Gibbs, E.M., Severson, D.L., Altered metabolism causes cardiac dysfunction in perfused hearts from diabetic (db/db) mice. Am. J. Physiol. Endocrinol. Metab. 279 (2000), E1104–E1113.
117. [117] Zhou, Y.T., Grayburn, P., Karim, A., Shimabukuro, M., Higa, M., Baetens, D., Orci, L., Unger, R.H., Lipotoxic heart disease in obese rats: implications for human obesity. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 1784–1789.
118. [118] Monji, A., Mitsui, T., Bando, Y.K., Aoyama, M., Shigeta, T., Murohara, T., Glucagon-like peptide-1 receptor activation reverses cardiac remodeling via normalizing cardiac steatosis and oxidative stress in type 2 diabetes. Am. J. Physiol. Heart Circ. Physiol. 305 (2013), H295–H304.
119. [119] 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. 292 (2007), E1288–E1294.
120. [120] Riphagen, I.J., Logtenberg, S.J., Groenier, K.H., van Hateren, K.J., Landman, G.W., Struck, J., Navis, G., Kootstra-Ros, J.E., Kema, I.P., Bilo, H.J., Kleefstra, N., Bakker, S.J., Is the association of serum sodium with mortality in patients with type 2 diabetes explained by copeptin or NT-proBNP? (ZODIAC-46). Atherosclerosis 242 (2015), 179–185.
121. [121] Rosiak, M., Postula, M., Kaplon-Cieslicka, A., Trzepla, E., Czlonkowski, A., Filipiak, K.J., Opolski, G., Metformin treatment may be associated with decreased levels of NT-proBNP in patients with type 2 diabetes. Adv. Med. Sci. 58 (2013), 362–368.
122. [122] Selker, H.P., Beshansky, J.R., Sheehan, P.R., Massaro, J.M., Griffith, J.L., D'Agostino, R.B., Ruthazer, R., Atkins, J.M., Sayah, A.J., Levy, M.K., Richards, M.E., Aufderheide, T.P., Braude, D.A., Pirrallo, R.G., Doyle, D.D., Frascone, R.J., Kosiak, D.J., Leaming, J.M., Van Gelder, C.M., Walter, G.P., Wayne, M.A., Woolard, R.H., Opie, L.H., Rackley, C.E., Apstein, C.S., Udelson, J.E., Out-of-hospital administration of intravenous glucose-insulin-potassium in patients with suspected acute coronary syndromes: the IMMEDIATE randomized controlled trial. JAMA 307 (2012), 1925–1933.
123. [123] Home, P.D., Pocock, S.J., Beck-Nielsen, H., Curtis, P.S., Gomis, R., Hanefeld, M., Jones, N.P., Komajda, M., McMurray, J.J., Team, R.S., Rosiglitazone evaluated for cardiovascular outcomes in oral agent combination therapy for type 2 diabetes (RECORD): a multicentre, randomised, open-label trial. Lancet 373 (2009), 2125–2135.
124. [124] Huang, H., Shan, J., Pan, X.H., Bao, X.F., Qian, L.B., Xia, Q., Carvedilol protects early diabetic rat hearts through reducing oxidative stress, conference proceedings: … Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society Annual Conference, 1, 2005, 929–932.
125. [125] Rupp, H., Elimban, V., Dhalla, N.S., Modification of myosin isozymes and SR Ca(2 +)-pump ATPase of the diabetic rat heart by lipid-lowering interventions. Mol. Cell. Biochem. 132 (1994), 69–80.
126. [126] Zhou, X., Chen, J., Is treatment with trimetazidine beneficial in patients with chronic heart failure?. PLoS One, 9, 2014, e94660.
127. [127] Belardinelli, R., Cianci, G., Gigli, M., Mazzanti, M., Lacalaprice, F., Effects of trimetazidine on myocardial perfusion and left ventricular systolic function in type 2 diabetic patients with ischemic cardiomyopathy. J. Cardiovasc. Pharmacol. 51 (2008), 611–615.
128. [128] Kosiborod, M., Arnold, S.V., Spertus, J.A., McGuire, D.K., Li, Y., Yue, P., Ben-Yehuda, O., Katz, A., Jones, P.G., Olmsted, A., Belardinelli, L., Chaitman, B.R., Evaluation of ranolazine in patients with type 2 diabetes mellitus and chronic stable angina: results from the TERISA randomized clinical trial (type 2 diabetes evaluation of ranolazine in subjects with chronic stable angina). J. Am. Coll. Cardiol. 61 (2013), 2038–2045.
129. [129] Mourouzis, I., Mantzouratou, P., Galanopoulos, G., Kostakou, E., Dhalla, A.K., Belardinelli, L., Pantos, C., The beneficial effects of ranolazine on cardiac function after myocardial infarction are greater in diabetic than in nondiabetic rats. J. Cardiovasc. Pharmacol. Ther. 19 (2014), 457–469.
130. [130] Koshkarian, G.M., Congestive heart failure and sodium dichloroacetate. J. Am. Coll. Cardiol. 25 (1995), 804–805.
131. [131] Bersin, R.M., Wolfe, C., Kwasman, M., Lau, D., Klinski, C., Tanaka, K., Khorrami, P., Henderson, G.N., de Marco, T., Chatterjee, K., Improved hemodynamic function and mechanical efficiency in congestive heart failure with sodium dichloroacetate. J. Am. Coll. Cardiol. 23 (1994), 1617–1624.
132. [132] Ng, L.F., Gruber, J., Cheah, I.K., Goo, C.K., Cheong, W.F., Shui, G., Sit, K.P., Wenk, M.R., Halliwell, B., The mitochondria-targeted antioxidant MitoQ extends lifespan and improves healthspan of a transgenic Caenorhabditis elegans model of Alzheimer disease. Free Radic. Biol. Med. 71 (2014), 390–401.
133. [133] Lim, S., Rashid, M.A., Jang, M., Kim, Y., Won, H., Lee, J., Woo, J.T., Kim, Y.S., Murphy, M.P., Ali, L., Ha, J., Kim, S.S., Mitochondria-targeted antioxidants protect pancreatic beta-cells against oxidative stress and improve insulin secretion in glucotoxicity and glucolipotoxicity. Cell. Physiol. Biochem. 28 (2011), 873–886.
134. [134] Bhatt, N.M., Aon, M.A., Tocchetti, C.G., Shen, X., Dey, S., Ramirez-Correa, G., O'Rourke, B., Gao, W.D., Cortassa, S., Restoring redox balance enhances contractility in heart trabeculae from type 2 diabetic rats exposed to high glucose. Am. J. Physiol. Heart Circ. Physiol. 308 (2015), H291–H302.
135. [135] Beaudoin, M.S., Perry, C.G., Arkell, A.M., Chabowski, A., Simpson, J.A., Wright, D.C., Holloway, G.P., Impairments in mitochondrial palmitoyl-CoA respiratory kinetics that precede development of diabetic cardiomyopathy are prevented by resveratrol in ZDF rats. J. Physiol. 592 (2014), 2519–2533.
136. [136] McCormick, L.M., Hoole, S.P., White, P.A., Read, P.A., Axell, R.G., Clarke, S.J., O'Sullivan, M., West, N.E., Dutka, D.P., Pre-treatment with glucagon-like Peptide-1 protects against ischemic left ventricular dysfunction and stunning without a detected difference in myocardial substrate utilization. JACC Cardiovasc. Interv. 8 (2015), 292–301.
137. [137] Margulies, K.B., Anstrom, K.J., Hernandez, A.F., Redfield, M.M., Shah, M.R., Braunwald, E., Cappola, T.P., N. Heart Failure Clinical Research, GLP-1 agonist therapy for advanced heart failure with reduced ejection fraction: design and rationale for the functional impact of GLP-1 for heart failure treatment study. Circ. Heart Fail. 7 (2014), 673–679.
138. [138] Fields, A.V., Patterson, B., Karnik, A.A., Shannon, R.P., Glucagon-like peptide-1 and myocardial protection: more than glycemic control. Clin. Cardiol. 32 (2009), 236–243.
139. [139] Bhashyam, S., Fields, A.V., Patterson, B., Testani, J.M., Chen, L., Shen, Y.T., Shannon, R.P., Glucagon-like peptide-1 increases myocardial glucose uptake via p38alpha MAP kinase-mediated, nitric oxide-dependent mechanisms in conscious dogs with dilated cardiomyopathy. Circ. Heart Fail. 3 (2010), 512–521.
140. [140] Wei, Y., Mojsov, S., Distribution of GLP-1 and PACAP receptors in human tissues. Acta Physiol. Scand. 157 (1996), 355–357.
141. [141] Lepore, J.J., Olson, E., Demopoulos, L., Haws, T., Fang, Z., Barbour, A.M., Fossler, M., Davila-Roman, V.G., Russell, S.D., Gropler, R.J., Effects of the novel long-acting GLP-1 agonist, albiglutide, on cardiac function, cardiac metabolism, and exercise capacity in patients with chronic heart failure and reduced ejection fraction. JACC Heart Fail. 4 (2016), 559–566.