Mitochondrial protein hyperacetylation in the failing heart

JCI Insight

Volumn 1, Issue 2, 2016, Pages

  Horton, Julie L ^a   Martin, Ola J ^a   Lai, Ling ^a   Riley, Nicholas M ^b   Richards, Alicia L ^b   Vega, Rick B ^a   Leone, Teresa C ^a   Pagliarini, David J ^b   Muoio, Deborah M ^c   Bedi, Kenneth C ^d   Margulies, Kenneth B ^d   Coon, Joshua J ^b,e   Kelly, Daniel P ^a  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84988848622     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.84897     Document Type: Article

References (64)

1. Bing RJ. The metabolism of the heart. Harvey Lect. 1954; 50:27-70.
2. Bing RJ, Siegel A, Ungar I, Gilbert M. Metabolism of the human heart. II. Studies on fat, ketone and amino acid metabolism. Am J Med. 1954; 16(4):504-515.
3. Wisneski JA, Gertz EW, Neese RA, Mayr M. Myocardial metabolism of free fatty acids. Studies with 14C-labeled substrates in humans. J Clin Invest. 1987; 79(2):359-366.
4. Lopaschuk GD, Belke DD, Gamble J, Itoi T, Schonekess BO. Regulation of fatty acid oxidation in the mammalian heart in health and disease. Biochim Biophys Acta. 1994; 1213(3):263-276.
5. van der Vusse GJ, van Bilsen M, Glatz JF. Cardiac fatty acid uptake and transport in health and disease. Cardiovasc Res. 2000; 45(2):279-293.
6. Kelly DP, Strauss AW. Inherited cardiomyopathies. N Engl J Med. 1994; 330(13):913-919.
7. Bishop SP, Altschuld RA. Increased glycolytic metabolism in cardiac hypertrophy and congestive failure. Am J Physiol. 1970; 218(1):153-159.
8. Taegtmeyer H, Overturf ML. Effects of moderate hypertension on cardiac function and metabolism in the rabbit. Hypertension. 1988; 11(5):416-426.
9. 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(2 pt 2):H742-H750.
10. Christe ME, Rodgers RL. Altered glucose and fatty acid oxidation in hearts of the spontaneously hypertensive rat. J Mol Cell Cardiol. 1994; 26(10):1371-1375.
11. Paolisso G, et al. Total-body and myocardial substrate oxidation in congestive heart failure. Metabolism. 1994; 43(2):174-179.
12. Sambandam N, Lopaschuk GD, Brownsey RW, Allard MF. Energy metabolism in the hypertrophied heart. Heart Fail Rev. 2002; 7(2):161-173.
13. Chandler MP, et al. Moderate severity heart failure does not involve a downregulation of myocardial fatty acid oxidation. Am J Physiol Heart Circ Physiol. 2004; 287(4):H1538-H1543.
14. Wallhaus TR, et al. Myocardial free fatty acid and glucose use after carvedilol treatment in patients with congestive heart failure. Circulation. 2001; 103(20):2441-2446.
15. Davila-Roman VG, et al. Altered myocardial fatty acid and glucose metabolism in idiopathic dilated cardiomyopathy. J Am Coll Cardiol. 2002; 40(2):271-277.
16. de las Fuentes L, Herrero P, Peterson LR, Kelly DP, Gropler RJ, Davila-Roman VG. Myocardial fatty acid metabolism: independent predictor of left ventricular mass in hypertensive heart disease. Hypertension. 2003; 41(1):83-87.
17. Ingwall JS, et al. The creatine kinase system in normal and diseased human myocardium. New Engl J Med. 1985; 313(17):1050-1054.
18. de Roos A, Doornbos J, Luyten PR, Oosterwaal LJ, van der Wall EE, den Hollander JA. Cardiac metabolism in patients with dilated and hypertrophic cardiomyopathy: assessment with proton-decoupled P-31 MR spectroscopy. J Magn Reson Imaging. 1992; 2(6):711-719.
19. Tian R, Nascimben L, Kaddurah-Daouk R, Ingwall JS. Depletion of energy reserve via the creatine kinase reaction during the evolution of heart failure in cardiomyopathic hamsters. J Mol Cell Card. 1996; 28(4):755-765.
20. Ingwall JS, Weiss RG. Is the failing heart energy starved?. On using chemical energy to support cardiac function. Circ Res. 2004; 95(2):135-145.
21. Carley AN, Taegtmeyer H, Lewandowski ED. Matrix revisited: mechanisms linking energy substrate metabolism to the function of the heart. Circ Res. 2014; 114(4):717-729.
22. Neubauer S, et al. Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation. 1997; 96(7):2190-2196.
23. Neubauer S. The failing heart-an engine out of fuel. New Engl J Med. 2007; 356(11):1140-1151.
24. Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH, Taegtmeyer H. Metabolic gene expression in fetal and failing human heart. Circulation. 2001; 104(24):2923-2931.
25. Huss JM, Kelly DP. Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest. 2005; 115(3):547-555.
26. Sack MN, Rader TA, Park S, Bastin J, McCune SA, Kelly DP. Fatty acid oxidation enzyme gene expression is downregulated in the failing heart. Circulation. 1996; 94(11):2837-2842.
27. Chen L, Gong Q, Stice JP, Knowlton AA. Mitochondrial OPA1, apoptosis, and heart failure. Cardiovasc Res. 2009; 84(1):91-99.
28. Lai L, et al. Energy metabolic reprogramming in the hypertrophied and early stage failing heart: a multisystems approach. Circ Heart Fail. 2014; 7(6):1022-1031.
29. Bedi KC Jr, et al. Evidence for intramyocardial disruption of lipid metabolism and increased myocardial ketone utilization in advanced human heart failure [published online ahead of print January 27, 2016]. Circulation. doi:10.1161/CIRCULATIONAHA. 115.017545.
30. Fernandes J, et al. Lysine acetylation activates mitochondrial aconitase in the heart. Biochemistry. 2015; 54(25):4008-4018.
31. Baeza J, Smallegan MJ, Denu JM. Site-specific reactivity of nonenzymatic lysine acetylation. ACS Chem Biol. 2015; 10(1):122-128.
32. Dittenhafer-Reed KE, et al. SIRT3 mediates multi-tissue coupling for metabolic fuel switching. Cell Metab. 2015; 21(4):637-646.
33. Cimen H, Han MJ, Yang Y, Tong Q, Koc H, Koc EC. Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry. 2010; 49(2):304-311.
34. Huss JM, et al. The nuclear receptor ERRα is required for the bioenergetic and functional adaptation to cardiac pressure overload. Cell Metab. 2007; 6(1):25-37.
35. Weinheimer CJ, Lai L, Kelly DP, Kovacs A. Novel mouse model of left ventricular pressure overload and infarction causing predictable ventricular remodelling and progression to heart failure. Clin Exp Pharmacol Physiol. 2015; 42(1):33-40.
36. Hebert AS, et al. Calorie restriction and SIRT3 trigger global reprogramming of the mitochondrial protein acetylome. Mol Cell. 2013; 49(1):186-199.
37. Hirschey MD, et al. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol Cell. 2011; 44(2):177-190.
38. 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(40):29036-29045.
39. Aubert G, et al. The failing heart relies on ketone bodies as a fuel [published online ahead of print January 27, 2016]. Circulation. doi:10.1161/CIRCULATIONAHA.115.017355.
40. Peek CB, et al. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science. 2013; 342(6158):1243417.
41. Ahn BH, et al. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci U S A. 2008; 105(38):14447-14452.
42. Anderson KA, Hirschey MD. Mitochondrial protein acetylation regulates metabolism. Essays Biochem. 2012; 52:23-35.
43. 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(8):536-550.
44. Hirschey MD, et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature. 2010; 464(7285):121-125.
45. Fan J, et al. Tyr phosphorylation of PDP1 toggles recruitment between ACAT1 and SIRT3 to regulate the pyruvate dehydrogenase complex. Mol Cell. 2014; 53(4):534-548.
46. Jain-Ghai S, et al. Complex II deficiency - a case report and review of the literature. Am J Med Genet A. 2013; 161A(2):285-294.
47. Karamanlidis G, et al. Mitochondrial complex I deficiency increases protein acetylation and accelerates heart failure. Cell Metab. 2013; 18(2):239-250.
48. Hsu CP, et al. Silent information regulator 1 protects the heart from ischemia/reperfusion. Circulation. 2010; 122(21):2170-2182.
49. Yamamoto T, Sadoshima J. Protection of the heart against ischemia/reperfusion by silent information regulator 1. Trends Cardiovasc Med. 2011; 21(1):27-32.
50. Gu XS, et al. Resveratrol, an activator of SIRT1, upregulates AMPK and improves cardiac function in heart failure. Genet Mol Res. 2014; 13(1):323-335.
51. Still AJ, et al. Quantification of mitochondrial acetylation dynamics highlights prominent sites of metabolic regulation. J Biol Chem. 2013; 288(36):26209-26219.
52. Grimsrud PA, et al. A quantitative map of the liver mitochondrial phosphoproteome reveals posttranslational control of ketogenesis. Cell Metab. 2012; 16(5):672-683.
53. Geer LY, et al. Open mass spectrometry search algorithm. J Proteome Res. 2004; 3(5):958-964.
54. Wenger CD, Phanstiel DH, Lee MV, Bailey DJ, Coon JJ. COMPASS: a suite of pre- and post-search proteomics software tools for OMSSA. Proteomics. 2011; 11(6):1064-1074.
55. Phanstiel DH, et al. Proteomic and phosphoproteomic comparison of human ES and iPS cells. Nat Methods. 2011; 8(10):821-827.
56. Nesvizhskii AI, Aebersold R. Interpretation of shotgun proteomic data: the protein inference problem. Mol Cell Proteomics. 2005; 4(10):1419-1440.
57. Kim W, et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell. 2011; 44(2):325-340.
58. Pagliarini DJ, et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell. 2008; 134(1):112-123.
59. Saks VA, et al. Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vivo. Mol Cell Biochem. 1998; 184(1-2):81-100.
60. Liu H, Naismith JH. An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol. 2008; 8:91.
61. Salabei JK, Gibb AA, Hill BG. Comprehensive measurement of respiratory activity in permeabilized cells using extracellular flux analysis. Nat Protoc. 2014; 9(2):421-438.
62. Ackrell BA, Kearney EB, Singer TP. Mammalian succinate dehydrogenase. Methods Enzymol. 1978; 53:466-483.
63. Birch-Machin MA, Turnbull DM. Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol. 2001; 65:97-117.
64. Acin-Perez R, et al. ROS-triggered phosphorylation of complex II by Fgr kinase regulates cellular adaptation to fuel use. Cell Metab. 2014; 19(6):1020-1033.