Mitochondrion as a target for heart failure therapy - Role of protein lysine acetylation

Circulation Journal

Volumn 79, Issue 9, 2015, Pages 1863-1870

  Lee, Chi Fung ^a   Tian, Rong ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Heart failure; Lysine acetylation; Mitochondria

Indexed keywords

ACIPIMOX; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CREATINE PHOSPHATE; LYSINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SIRTUIN; SUPEROXIDE DISMUTASE; MITOCHONDRIAL PROTEIN;

AEROBIC METABOLISM; BIOGENESIS; CALCIUM HOMEOSTASIS; CELL DEATH; CELL METABOLISM; DEACETYLATION; ENERGY METABOLISM; ENERGY RESOURCE; ENERGY TRANSFER; GENE DELETION; GLUCOSE OXIDATION; GLYCOLYSIS; HEART FAILURE; HEART STRESS; HYPERTROPHY; MITOCHONDRION; OXIDATIVE STRESS; PROTEIN ACETYLATION; RESPIRATORY CHAIN; REVIEW; ACETYLATION; HEART MITOCHONDRION; HUMAN; METABOLISM; PATHOLOGY;

ACETYLATION; HEART FAILURE; HUMANS; LYSINE; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTEINS; SIRTUINS;

EID: 84940068861     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-15-0742     Document Type: Review

References (120)

1. Roth GA, Forouzanfar MH, Moran AE, Barber R, Nguyen G, Feigin VL, et al. Demographic and epidemiologic drivers of global cardiovascular mortality. N Engl J Med 2015; 372: 1333-1341.
2. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, et al. Heart disease and stroke statistics--2014 update: A report from the American Heart Association. Circulation 2014; 129: e28-e292, doi:10.1161/01.cir.0000441139.02102.80.
3. Shioi T, Inuzuka Y. Aging as a substrate of heart failure. J Cardiol 2012; 60: 423-428.
4. Cohn JN, Ferrari R, Sharpe N. Cardiac remodeling--concepts and clinical implications: A consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling. J Am Coll Cardiol 2000; 35: 569-582.
5. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: A mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004; 287: C817-C833.
6. Marks AR. Calcium cycling proteins and heart failure: Mechanisms and therapeutics. J Clin Invest 2013; 123: 46-52.
7. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 2005; 115: 500-508.
8. Liao R, Nascimben L, Friedrich J, Gwathmey JK, Ingwall JS. Decreased energy reserve in an animal model of dilated cardiomyopathy. Relationship to contractile performance. Circ Res 1996; 78: 893-902.
9. Ahuja P, Wanagat J, Wang Z, Wang Y, Liem DA, Ping P, et al. Divergent mitochondrial biogenesis responses in human cardiomyopathy. Circulation 2013; 127: 1957-1967.
10. Sebastiani M, Giordano C, Nediani C, Travaglini C, Borchi E, Zani M, et al. Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. J Am Coll Cardiol 2007; 50: 1362-1369.
11. Kolwicz SC Jr, Olson DP, Marney LC, Garcia-Menendez L, Synovec RE, Tian R. Cardiac-specific deletion of acetyl CoA car- boxylase 2 prevents metabolic remodeling during pressure-overload hypertrophy. Circ Res 2012; 111: 728-738.
12. Dai DF, Johnson SC, Villarin JJ, Chin MT, Nieves-Cintron M, Chen T, et al. Mitochondrial oxidative stress mediates angiotensin II-induced cardiac hypertrophy and Galphaq overexpression-induced heart failure. Circ Res 2011; 108: 837-846.
13. Nakayama H, Chen X, Baines CP, Klevitsky R, Zhang X, Zhang H, et al. Ca2+- and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J Clin Invest 2007; 117: 2431-2444.
14. Elrod JW, Wong R, Mishra S, Vagnozzi RJ, Sakthievel B, Goonasekera SA, et al. Cyclophilin D controls mitochondrial poredependent Ca(2+) exchange, metabolic flexibility, and propensity for heart failure in mice. J Clin Invest 2010; 120: 3680-3687.
15. Lopaschuk GD, Spafford MA, Marsh DR. Glycolysis is predominant source of myocardial ATP production immediately after birth. Am J Physiol 1991; 261: H1698-H1705.
16. Allard MF, Henning SL, Wambolt RB, Granleese SR, English DR, Lopaschuk GD. Glycogen metabolism in the aerobic hypertrophied rat heart. Circulation 1997; 96: 676-682.
17. Yan J, Young ME, Cui L, Lopaschuk GD, Liao R, Tian R. Increased glucose uptake and oxidation in mouse hearts prevent high fatty acid oxidation but cause cardiac dysfunction in dietinduced obesity. Circulation 2009; 119: 2818-2828.
18. Starling RC, Hammer DF, Altschuld RA. Human myocardial ATP content and in vivo contractile function. Mol Cell Biochem 1998; 180: 171-177.
19. Beer M, Seyfarth T, Sandstede J, Landschutz W, Lipke C, Kostler H, et al. Absolute concentrations of high-energy phosphate metabolites in normal, hypertrophied, and failing human myocardium measured noninvasively with (31)P-SLOOP magnetic resonance spectroscopy. J Am Coll Cardiol 2002; 40: 1267-1274.
20. Neubauer S, Horn M, Cramer M, Harre K, Newell JB, Peters W, et al. Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation 1997; 96: 2190-2196.
21. Gupta A, Akki A, Wang Y, Leppo MK, Chacko VP, Foster DB, et al. Creatine kinase-mediated improvement of function in failing mouse hearts provides causal evidence the failing heart is energy starved. J Clin Invest 2012; 122: 291-302.
22. Huss JM, Kelly DP. Mitochondrial energy metabolism in heart failure: A question of balance. J Clin Invest 2005; 115: 547-555.
23. Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev 2010; 90: 207-258.
24. Kolwicz SC Jr, Tian R. Glucose metabolism and cardiac hypertrophy. Cardiovasc Res 2011; 90: 194-201.
25. Neubauer S. The failing heart: An engine out of fuel. N Engl J Med 2007; 356: 1140-1151.
26. Allard MF, Schonekess BO, Henning SL, English DR, Lopaschuk GD. Contribution of oxidative metabolism and glycolysis to ATP production in hypertrophied hearts. Am J Physiol 1994; 267: H742-H750.
27. Nascimben L, Ingwall JS, Lorell BH, Pinz I, Schultz V, Tornheim K, et al. Mechanisms for increased glycolysis in the hypertrophied rat heart. Hypertension 2004; 44: 662-667.
28. Rupert BE, Segar JL, Schutte BC, Scholz TD. Metabolic adaptation of the hypertrophied heart: Role of the malate/aspartate and alphaglycerophosphate shuttles. J Mol Cell Cardiol 2000; 32: 2287- 2297.
29. Lewandowski ED, O'Donnell JM, Scholz TD, Sorokina N, Buttrick PM. Recruitment of NADH shuttling in pressure-overloaded and hypertrophic rat hearts. Am J Physiol Cell Physiol 2007; 292: C1880-C1886.
30. Turcani M, Rupp H. Etomoxir improves left ventricular performance of pressure-overloaded rat heart. Circulation 1997; 96: 3681-3686.
31. Kantor PF, Lucien A, Kozak R, Lopaschuk GD. The antianginal drug trimetazidine shifts cardiac energy metabolism from fatty acid oxidation to glucose oxidation by inhibiting mitochondrial longchain 3-ketoacyl coenzyme A thiolase. Circ Res 2000; 86: 580- 588.
32. Piao L, Fang YH, Cadete VJ, Wietholt C, Urboniene D, Toth PT, et al. The inhibition of pyruvate dehydrogenase kinase improves impaired cardiac function and electrical remodeling in two models of right ventricular hypertrophy: Resuscitating the hibernating right ventricle. J Mol Med (Berl) 2010; 88: 47-60.
33. Liao R, Jain M, Cui L, D'Agostino J, Aiello F, Luptak I, et al. Cardiac-specific overexpression of GLUT1 prevents the development of heart failure attributable to pressure overload in mice. Circulation 2002; 106: 2125-2131.
34. Brigadeau F, Gele P, Wibaux M, Marquie C, Martin-Nizard F, Torpier G, et al. The PPARalpha activator fenofibrate slows down the progression of the left ventricular dysfunction in porcine tachycardia- induced cardiomyopathy. J Cardiovasc Pharmacol 2007; 49: 408-415.
35. Okere IC, Young ME, McElfresh TA, Chess DJ, Sharov VG, Sabbah HN, et al. Low carbohydrate/high-fat diet attenuates cardiac hypertrophy, remodeling, and altered gene expression in hypertension. Hypertension 2006; 48: 1116-1123.
36. Tuunanen H, Engblom E, Naum A, Nagren K, Hesse B, Airaksinen KE, et al. Free fatty acid depletion acutely decreases cardiac work and efficiency in cardiomyopathic heart failure. Circulation 2006; 114: 2130-2137.
37. Kolwicz SC Jr, Purohit S, Tian R. Cardiac metabolism and its interactions with contraction, growth, and survival of cardiomyocytes. Circ Res 2013; 113: 603-616.
38. Carley AN, Taegtmeyer H, Lewandowski ED. Matrix revisited: Mechanisms linking energy substrate metabolism to the function of the heart. Circ Res 2014; 114: 717-729.
39. Yin F, Sancheti H, Cadenas E. Mitochondrial thiols in the regulation of cell death pathways. Antioxid Redox Signal 2012; 17: 1714-1727.
40. Ku HJ, Ahn Y, Lee JH, Park KM, Park JW. IDH2 deficiency promotes mitochondrial dysfunction and cardiac hypertrophy in mice. Free Radic Biol Med 2015; 80: 84-92.
41. Sheeran FL, Rydstrom J, Shakhparonov MI, Pestov NB, Pepe S. Diminished NADPH transhydrogenase activity and mitochondrial redox regulation in human failing myocardium. Biochim Biophys Acta 2010; 1797: 1138-1148.
42. Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, Sadoshima J. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci USA 2010; 107: 15565- 15570.
43. Zhang M, Brewer AC, Schroder K, Santos CX, Grieve DJ, Wang M, et al. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci USA 2010; 107: 18121-18126.
44. Dai DF, Chen T, Szeto H, Nieves-Cintron M, Kutyavin V, Santana LF, et al. Mitochondrial targeted antioxidant peptide ameliorates hypertensive cardiomyopathy. J Am Coll Cardiol 2011; 58: 73-82.
45. Dai DF, Santana LF, Vermulst M, Tomazela DM, Emond MJ, MacCoss MJ, et al. Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 2009; 119: 2789-2797.
46. Steinhubl SR. Why have antioxidants failed in clinical trials? Am J Cardiol 2008; 101: 14D-19D.
47. Bers DM. Cardiac excitation-contraction coupling. Nature 2002; 415: 198-205.
48. Clapham DE. Calcium signaling. Cell 2007; 131: 1047-1058.
49. de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008; 456: 605-610.
50. Copeland DE, Dalton AJ. An association between mitochondria and the endoplasmic reticulum in cells of the pseudobranch gland of a teleost. J Biophys Biochem Cytol 1959; 5: 393-396.
51. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 1998; 280: 1763-1766.
52. Respress JL, van Oort RJ, Li N, Rolim N, Dixit SS, Dealmeida A, et al. Role of RyR2 phosphorylation at S2814 during heart failure progression. Circ Res 2012; 110: 1474-1483.
53. Zhang T, Maier LS, Dalton ND, Miyamoto S, Ross J Jr, Bers DM, et al. The deltaC isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure. Circ Res 2003; 92: 912-919.
54. Kirchhefer U, Schmitz W, Scholz H, Neumann J. Activity of cAMP-dependent protein kinase and Ca2+/calmodulin-dependent protein kinase in failing and nonfailing human hearts. Cardiovasc Res 1999; 42: 254-261.
55. Hoch B, Meyer R, Hetzer R, Krause EG, Karczewski P. Identification and expression of delta-isoforms of the multifunctional Ca2+/ calmodulin-dependent protein kinase in failing and nonfailing human myocardium. Circ Res 1999; 84: 713-721.
56. Ai X, Curran JW, Shannon TR, Bers DM, Pogwizd SM. Ca2+/ calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 2005; 97: 1314-1322.
57. Ling H, Zhang T, Pereira L, Means CK, Cheng H, Gu Y, et al. Requirement for Ca2+/calmodulin-dependent kinase II in the transi tion from pressure overload-induced cardiac hypertrophy to heart failure in mice. J Clin Invest 2009; 119: 1230-1240.
58. Kushnir A, Shan J, Betzenhauser MJ, Reiken S, Marks AR. Role of CaMKIIdelta phosphorylation of the cardiac ryanodine receptor in the force frequency relationship and heart failure. Proc Natl Acad Sci USA 2010; 107: 10274-10279.
59. Zhang T, Guo T, Mishra S, Dalton ND, Kranias EG, Peterson KL, et al. Phospholamban ablation rescues sarcoplasmic reticulum Ca(2+) handling but exacerbates cardiac dysfunction in CaMKIIdelta(C) transgenic mice. Circ Res 2010; 106: 354-362.
60. Westenbrink BD, Ling H, Divakaruni AS, Gray CB, Zambon AC, Dalton ND, et al. Mitochondrial reprogramming induced by CaMKIIdelta mediates hypertrophy decompensation. Circ Res 2015; 116: e28-e39, doi:10.1161/CIRCRESAHA.116.304682.
61. Joiner ML, Koval OM, Li J, He BJ, Allamargot C, Gao Z, et al. CaMKII determines mitochondrial stress responses in heart. Nature 2012; 491: 269-273.
62. Verdin E, Ott M. 50 years of protein acetylation: From gene regulation to epigenetics, metabolism and beyond. Nat Rev Mol Cell Biol 2015; 16: 258-264.
63. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128: 693-705.
64. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, et al. Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 2007; 27: 8807-8814.
65. Hirschey MD, Shimazu T, Huang JY, Schwer B, Verdin E. SIRT3 regulates mitochondrial protein acetylation and intermediary metabolism. Cold Spring Harb Symp Quant Biol 2011; 76: 267-277.
66. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, Lombard DB, et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 2010; 464: 121-125.
67. Hebert AS, Dittenhafer-Reed KE, Yu W, Bailey DJ, Selen ES, Boersma MD, et al. Calorie restriction and SIRT3 trigger global reprogramming of the mitochondrial protein acetylome. Mol Cell 2013; 49: 186-199.
68. Hallows WC, Yu W, Smith BC, Devries MK, Ellinger JJ, Someya S, et al. Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction. Mol Cell 2011; 41: 139-149.
69. Wagner GR, Payne RM. Widespread and enzyme-independent Nepsilon-acetylation and Nepsilon-succinylation of proteins in the chemical conditions of the mitochondrial matrix. J Biol Chem 2013; 288: 29036-29045.
70. Choudhary C, Weinert BT, Nishida Y, Verdin E, Mann M. The growing landscape of lysine acetylation links metabolism and cell signalling. Nat Rev Mol Cell Biol 2014; 15: 536-550.
71. Scott I, Webster BR, Li JH, Sack MN. Identification of a molecular component of the mitochondrial acetyl transferase programme: A novel role for GCN5L1. Biochem J 2012; 443: 655-661.
72. Lee KK, Workman JL. Histone acetyltransferase complexes: One size doesn't fit all. Nat Rev Mol Cell Biol 2007; 8: 284-295.
73. Peng L, Seto E. Deacetylation of nonhistone proteins by HDACs and the implications in cancer. Handb Exp Pharmacol 2011; 206: 39-56.
74. Cao DJ, Wang ZV, Battiprolu PK, Jiang N, Morales CR, Kong Y, et al. Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci USA 2011; 108: 4123-4128.
75. Xie M, Kong Y, Tan W, May H, Battiprolu PK, Pedrozo Z, et al. Histone deacetylase inhibition blunts ischemia/reperfusion injury by inducing cardiomyocyte autophagy. Circulation 2014; 129: 1139-1151.
76. Yoshino J, Mills KF, Yoon MJ, Imai S. Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab 2011; 14: 528-536.
77. Gomes AP, Price NL, Ling AJ, Moslehi JJ, Montgomery MK, Rajman L, et al. Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 2013; 155: 1624-1638.
78. Santidrian AF, Matsuno-Yagi A, Ritland M, Seo BB, Leboeuf SE, Gay LJ, et al. Mitochondrial complex I activity and NAD+/NADH balance regulate breast cancer progression. J Clin Invest 2013; 123: 1068-1081.
79. Canto C, Houtkooper RH, Pirinen E, Youn DY, Oosterveer MH, Cen Y, et al. The NAD(+) precursor nicotinamide riboside enhances oxidative metabolism and protects against high-fat diet-induced obesity. Cell Metab 2012; 15: 838-847.
80. Wang G, Han T, Nijhawan D, Theodoropoulos P, Naidoo J, Yadavalli S, et al. P7C3 neuroprotective chemicals function by activating the rate-limiting enzyme in NAD salvage. Cell 2014; 158: 1324-1334.
81. Yin TC, Britt JK, De Jesus-Cortes H, Lu Y, Genova RM, Khan MZ, et al. P7C3 neuroprotective chemicals block axonal degeneration and preserve function after traumatic brain injury. Cell Rep 2014; 8: 1731-1740.
82. Kemp SW, Szynkaruk M, Stanoulis KN, Wood MD, Liu EH, Willand MP, et al. Pharmacologic rescue of motor and sensory function by the neuroprotective compound P7C3 following neonatal nerve injury. Neuroscience 2015; 284: 202-216.
83. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, et al. Resveratrol improves health and survival of mice on a highcalorie diet. Nature 2006; 444: 337-342.
84. Dokmanovic M, Clarke C, Marks PA. Histone deacetylase inhibitors: Overview and perspectives. Mol Cancer Res 2007; 5: 981- 989.
85. Tanno M, Sakamoto J, Miura T, Shimamoto K, Horio Y. Nucleocytoplasmic shuttling of the NAD+-dependent histone deacetylase SIRT1. J Biol Chem 2007; 282: 6823-6832.
86. North BJ, Verdin E. Interphase nucleo-cytoplasmic shuttling and localization of SIRT2 during mitosis. PLoS One 2007; 2: e784, doi:10.1371/journal.pone.0000784.
87. Cooper HM, Spelbrink JN. The human SIRT3 protein deacetylase is exclusively mitochondrial. Biochem J 2008; 411: 279-285.
88. Feldman JL, Dittenhafer-Reed KE, Denu JM. Sirtuin catalysis and regulation. J Biol Chem 2012; 287: 42419-42427.
89. Sauve AA, Celic I, Avalos J, Deng H, Boeke JD, Schramm VL. Chemistry of gene silencing: The mechanism of NAD+-dependent deacetylation reactions. Biochemistry 2001; 40: 15456-15463.
90. Finkel T, Deng CX, Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature 2009; 460: 587-591.
91. Lu Z, Scott I, Webster BR, Sack MN. The emerging characterization of lysine residue deacetylation on the modulation of mitochondrial function and cardiovascular biology. Circ Res 2009; 105: 830-841.
92. Karamanlidis G, Lee CF, Garcia-Menendez L, Kolwicz SC Jr, Suthammarak W, Gong G, et al. Mitochondrial complex I deficiency increases protein acetylation and accelerates heart failure. Cell Metab 2013; 18: 239-250.
93. Hirschey MD, Shimazu T, Jing E, Grueter CA, Collins AM, Aouizerat B, et al. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol Cell 2011; 44: 177-190.
94. Schwer B, Eckersdorff M, Li Y, Silva JC, Fermin D, Kurtev MV, et al. Calorie restriction alters mitochondrial protein acetylation. Aging Cell 2009; 8: 604-606.
95. Yang L, Vaitheesvaran B, Hartil K, Robinson AJ, Hoopmann MR, Eng JK, et al. The fasted/fed mouse metabolic acetylome: N6-acetylation differences suggest acetylation coordinates organ-specific fuel switching. J Proteome Res 2011; 10: 4134-4149.
96. Papanicolaou KN, O'Rourke B, Foster DB. Metabolism leaves its mark on the powerhouse: Recent progress in post-translational modifications of lysine in mitochondria. Front Physiol 2014; 5: 301.
97. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 2010; 12: 662-667.
98. Hafner AV, Dai J, Gomes AP, Xiao CY, Palmeira CM, Rosenzweig A, et al. Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging (Albany NY) 2010; 2: 914-923.
99. Chi Y, Sauve AA. Nicotinamide riboside, a trace nutrient in foods, is a vitamin B3 with effects on energy metabolism and neuroprotection. Curr Opin Clin Nutr Metab Care 2013; 16: 657-661.
100. Koretsky AP, Katz LA, Balaban RS. Determination of pyridine nucleotide fluorescence from the perfused heart using an internal standard. Am J Physiol 1987; 253: H856-H862.
101. Koretsky AP, Balaban RS. Changes in pyridine nucleotide levels alter oxygen consumption and extra-mitochondrial phosphates in isolated mitochondria: A 31P-NMR and NAD(P)H fluorescence study. Biochim Biophys Acta 1987; 893: 398-408.
102. Aon MA, Cortassa S, O'Rourke B. Redox-optimized ROS balance: A unifying hypothesis. Biochim Biophys Acta 2010; 1797: 865- 877.
103. Alrob OA, Sankaralingam S, Ma C, Wagg CS, Fillmore N, Jaswal JS, et al. Obesity-induced lysine acetylation increases cardiac fatty acid oxidation and impairs insulin signalling. Cardiovasc Res 2014; 103: 485-497.
104. Wagner GR, Pride PM, Babbey CM, Payne RM. Friedreich's ataxia reveals a mechanism for coordinate regulation of oxidative metabolism via feedback inhibition of the SIRT3 deacetylase. Hum Mol Genet 2012; 21: 2688-2697.
105. Sundaresan NR, Gupta M, Kim G, Rajamohan SB, Isbatan A, Gupta MP. Sirt3 blocks the cardiac hypertrophic response by augmenting Foxo3a-dependent antioxidant defense mechanisms in mice. J Clin Invest 2009; 119: 2758-2771.
106. Porter GA, Urciuoli WR, Brookes PS, Nadtochiy SM. SIRT3 deficiency exacerbates ischemia-reperfusion injury: Implication for aged hearts. Am J Physiol Heart Circ Physiol 2014; 306: H1602- H1609.
107. Nguyen TT, Wong R, Menazza S, Sun J, Chen Y, Wang G, et al. Cyclophilin d modulates mitochondrial acetylome. Circ Res 2013; 113: 1308-1319.
108. Ahn BH, Kim HS, Song S, Lee IH, Liu J, Vassilopoulos A, et al. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci USA 2008; 105: 14447-14452.
109. Kendrick AA, Choudhury M, Rahman SM, McCurdy CE, Friederich M, Van Hove JL, et al. Fatty liver is associated with reduced SIRT3 activity and mitochondrial protein hyperacetylation. Biochem J 2011; 433: 505-514.
110. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, Jiang H, et al. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 2010; 40: 893-904.
111. Yu W, Dittenhafer-Reed KE, Denu JM. SIRT3 protein deacetylates isocitrate dehydrogenase 2 (IDH2) and regulates mitochondrial redox status. J Biol Chem 2012; 287: 14078-14086.
112. Fernandez-Marcos PJ, Jeninga EH, Canto C, Harach T, de Boer VC, Andreux P, et al. Muscle or liver-specific Sirt3 deficiency induces hyperacetylation of mitochondrial proteins without affecting global metabolic homeostasis. Sci Rep 2012; 2: 425.
113. Houtkooper RH, Canto C, Wanders RJ, Auwerx J. The secret life of NAD+: An old metabolite controlling new metabolic signaling pathways. Endocr Rev 2010; 31: 194-223.
114. Guarente L. Calorie restriction and sirtuins revisited. Genes Dev 2013; 27: 2072-2085.
115. Grillon JM, Johnson KR, Kotlo K, Danziger RS. Non-histone lysine acetylated proteins in heart failure. Biochim Biophys Acta 2012; 1822: 607-614.
116. Vadvalkar SS, Baily CN, Matsuzaki S, West M, Tesiram YA, Humphries KM. Metabolic inflexibility and protein lysine acetylation in heart mitochondria of a chronic model of type 1 diabetes. Biochem J 2013; 449: 253-261.
117. Hsu CP, Oka S, Shao D, Hariharan N, Sadoshima J. Nicotinamide phosphoribosyltransferase regulates cell survival through NAD+ synthesis in cardiac myocytes. Circ Res 2009; 105: 481-491.
118. Chan V, Fenning A, Iyer A, Hoey A, Brown L. Resveratrol improves cardiovascular function in DOCA-salt hypertensive rats. Curr Pharm Biotechnol 2011; 12: 429-436.
119. Juric D, Wojciechowski P, Das DK, Netticadan T. Prevention of concentric hypertrophy and diastolic impairment in aortic-banded rats treated with resveratrol. Am J Physiol Heart Circ Physiol 2007; 292: H2138-H2143.
120. Baeza J, Dowell JA, Smallegan MJ, Fan J, Amador-Noguez D, Khan Z, et al. Stoichiometry of site-specific lysine acetylation in an entire proteome. J Biol Chem 2014; 289: 21326-21338.