Normalization of NAD+ Redox Balance as a Therapy for Heart Failure

Circulation

Volumn 134, Issue 12, 2016, Pages 883-894

  Lee, Chi Fung ^a   Chavez, Juan D ^a   Garcia Menendez, Lorena ^a   Choi, Yongseon ^a   Roe, Nathan D ^a   Chiao, Ying Ann ^a   Edgar, John S ^a   Goo, Young Ah ^a   Goodlett, David R ^a   Bruce, James E ^a   Tian, Rong ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

cardiac metabolism; heart failure; hypertrophy; mitochondria; permeability transition pore

Indexed keywords

ADENOSINE TRIPHOSPHATE; ASPARTIC ACID; CYCLOPHILIN D; CYCLOSPORIN A; ISOPRENALINE; LYSINE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOCHONDRIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE NUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; OLIGOMYCIN; PROTEOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); CALCIUM; CARRIER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; CALCIUM TRANSPORT; CHRONIC STRESS; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; GENETIC MODEL; HEART FAILURE; HEART FUNCTION; HEART VENTRICLE HYPERTROPHY; LUNG EDEMA; MOLECULAR DOCKING; MOUSE; MUTAGENESIS; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TRANSPORT; PROTEOMICS; UPREGULATION; ANIMAL; HEART MITOCHONDRION; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; HEART FAILURE; HUMANS; MICE; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NAD; OXIDATION-REDUCTION;

EID: 84981156632     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.116.022495     Document Type: Article

References (50)

1. Roth GA, Forouzanfar MH, Moran AE, Barber R, Nguyen G, Feigin VL, Naghavi M, Mensah GA, Murray CJ. Demographic and epidemiologic drivers of global cardiovascular mortality. N Engl J Med. 2015;372:1333-1341. doi: 10.1056/NEJMoa1406656.
2. Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, Das SR, de Ferranti S, Despres JP, Fullerton HJ, Howard VJ, Huffman MD, Isasi CR, Jimenez MC, Judd SE, Kissela BM, Lichtman JH, Lisabeth LD, Liu S, Mackey RH, Magid DJ, McGuire DK, Mohler ER, 3rd, Moy CS, Muntner P, Mussolino ME, Nasir K, Neumar RW, Nichol G, Palaniappan L, Pandey DK, Reeves MJ, Rodriguez CJ, Rosamond W, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Woo D, Yeh RW, Turner MB, American Heart Association statistics C and stroke statistics S. Heart disease and stroke statistics 2016 update: a report from the American Heart Association. Circulation. 2016;133:e38-e360.
3. Bayeva M, Gheorghiade M, Ardehali H. Mitochondria as a therapeutic target in heart failure. J Am Coll Cardiol. 2013;61:599-610. doi: 10.1016/j.jacc.2012.08.1021.
4. Rosca MG, Tandler B, Hoppel CL. Mitochondria in cardiac hypertrophy and heart failure. J Mol Cell Cardiol. 2013;55:31-41. doi: 10.1016/j.yjmcc.2012.09.002.
5. Wang W, Karamanlidis G, Tian R. Novel targets for mitochondrial medicine. Sci Transl Med. 2016;8:326rv3. doi: 10.1126/scitranslmed. aac7410.
6. 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. doi: 10.1038/nrm3841.
7. Cantó C, Menzies KJ, Auwerx J. NAD(+) metabolism and the control of energy homeostasis: a balancing act between Mitochondria and the nucleus. Cell Metab. 2015;22:31-53. doi: 10.1016/j. cmet.2015.05.023.
8. Lee CF, Tian R. Mitochondrion as a target for heart failure therapy-role of protein lysine acetylation. Circ J. 2015;79:1863-1870. doi: 10.1253/circj.CJ-15-0742.
9. Sauve AA, Wolberger C, Schramm VL, Boeke JD. The biochemistry of sirtuins. Annu Rev Biochem. 2006;75:435-465. doi: 10.1146/annurev.biochem.74.082803.133500.
10. Karamanlidis G, Lee CF, Garcia-Menendez L, Kolwicz SC Jr, Suthammarak W, Gong G, Sedensky MM, Morgan PG, Wang W, Tian R. Mitochondrial complex I deficiency increases protein acetylation and accelerates heart failure. Cell Metab. 2013;18:239-250. doi: 10.1016/j.cmet.2013.07.002.
11. Kolwicz SC Jr, Olson DP, Marney LC, Garcia-Menendez L, Synovec RE, Tian R. Cardiac-specific deletion of acetyl CoA carboxylase 2 prevents metabolic remodeling during pressure-overload hypertrophy. Circ Res. 2012;111:728-738. doi: 10.1161/CIRCRESAHA. 112.268128.
12. Boehm EA, Jones BE, Radda GK, Veech RL, Clarke K. Increased uncoupling proteins and decreased efficiency in palmitate-perfused hyperthyroid rat heart. Am J Physiol Heart Circ Physiol. 2001;280:H977-H983.
13. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem. 2002;74:5383-5392.
14. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003;75:4646-4658.
15. Elias JE, Gygi SP. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods. 2007;4:207-214. doi: 10.1038/nmeth1019.
16. Ma K, Vitek O, Nesvizhskii AI. A statistical model-building perspective to identification of MS/MS spectra with PeptideProphet. BMC Bioinformatics. 2012;13 Suppl 16:S1. doi: 10.1186/1471-2105-13-S16-S1.
17. Liu H, Sadygov RG, Yates JR 3rd. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem. 2004;76:4193-4201. doi: 10.1021/ac0498563.
18. Eng JK, Jahan TA, Hoopmann MR. Comet: an open-source MS/MS sequence database search tool. Proteomics. 2013;13:22-24. doi: 10.1002/pmic.201200439.
19. Siegel S and Castellan Jr. NJ. Nonparametric Statistics for the Behavioral Sciences. Second Edition ed: McGraw Hill; 2000.
20. 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. doi: 10.1161/CIRCRESAHA.109.203703.
21. Errami M, Galindo CL, Tassa AT, Dimaio JM, Hill JA, Garner HR. Doxycycline attenuates isoproterenol-and transverse aortic band ing-induced cardiac hypertrophy in mice. J Pharmacol Exp Ther. 2008;324:1196-1203. doi: 10.1124/jpet.107.133975.
22. Houtkooper RH, Cantó C, Wanders RJ, Auwerx J. The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocr Rev. 2010;31:194-223. doi: 10.1210/er.2009-0026.
23. LaNoue KF, Williamson JR. Interrelationships between malateaspartate shuttle and citric acid cycle in rat heart mitochondria. Metabolism. 1971;20:119-140.
24. Allard MF, Schönekess 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.
25. Nascimben L, Ingwall JS, Lorell BH, Pinz I, Schultz V, Tornheim K, Tian R. Mechanisms for increased glycolysis in the hypertrophied rat heart. Hypertension. 2004;44:662-667. doi: 10.1161/01. HYP.0000144292.69599.0c.
26. Wambolt RB, Lopaschuk GD, Brownsey RW, Allard MF. Dichloroacetate improves postischemic function of hypertrophied rat hearts. J Am Coll Cardiol. 2000;36:1378-1385.
27. Rupert BE, Segar JL, Schutte BC, Scholz TD. Metabolic adaptation of the hypertrophied heart: role of the malate/aspartate and alpha-glycerophosphate shuttles. J Mol Cell Cardiol. 2000;32:2287-2297. doi: 10.1006/jmcc.2000.1257.
28. 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. doi: 10.1152/ajpcell.00576.2006.
29. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature. 2005;434:658-662. doi: 10.1038/nature03434.
30. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T, Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature. 2005;434:652-658. doi: 10.1038/nature03317.
31. Giorgio V, von Stockum S, Antoniel M, Fabbro A, Fogolari F, Forte M, Glick GD, Petronilli V, Zoratti M, Szabó I, Lippe G, Bernardi P. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc Natl Acad Sci USA. 2013;110:5887-5892. doi: 10.1073/pnas.1217823110.
32. Chinopoulos C, Adam-Vizi V. Modulation of the mitochondrial permeability transition by cyclophilin D: moving closer to F(0)-F(1) ATP synthase? Mitochondrion. 2012;12:41-45. doi: 10.1016/j. mito.2011.04.007.
33. Schlatter D, Thoma R, Küng E, Stihle M, Müller F, Borroni E, Cesura A, Hennig M. Crystal engineering yields crystals of cyclophilin D diffracting to 1.7 A resolution. Acta Crystallogr D Biol Crystallogr. 2005;61(Pt 5):513-519. doi: 10.1107/S0907444905003070.
34. Rees DM, Leslie AG, Walker JE. The structure of the membrane extrinsic region of bovine ATP synthase. Proc Natl Acad Sci USA. 2009;106:21597-21601. doi: 10.1073/pnas.0910365106.
35. Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ. Patch-Dock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res. 2005;33(Web Server issue):W363-W367. doi: 10.1093/nar/gki481.
36. Hafner AV, Dai J, Gomes AP, Xiao CY, Palmeira CM, Rosenzweig A, Sinclair DA. 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. doi: 10.18632/aging.100252.
37. Bochaton T, Crola-Da-Silva C, Pillot B, Villedieu C, Ferreras L, Alam MR, Thibault H, Strina M, Gharib A, Ovize M, Baetz D. Inhibition of myocardial reperfusion injury by ischemic postconditioning requires sirtuin 3-mediated deacetylation of cyclophilin D. J Mol Cell Cardiol. 2015;84:61-69. doi: 10.1016/j.yjmcc.2015.03.017.
38. 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. doi: 10.1016/j.cmet.2011.08.014.
39. Cantó C, Houtkooper RH, Pirinen E, Youn DY, Oosterveer MH, Cen Y, Fernandez-Marcos PJ, Yamamoto H, Andreux PA, Cettour-Rose P, Gademann K, Rinsch C, Schoonjans K, Sauve AA, Auwerx J. The NAD(+) precursor nicotinamide riboside enhances oxidative metabolism and protects against high-fat diet-induced obesity. Cell Metab. 2012;15:838-847. doi: 10.1016/j.cmet.2012.04.022.
40. Gomes AP, Price NL, Ling AJ, Moslehi JJ, Montgomery MK, Rajman L, White JP, Teodoro JS, Wrann CD, Hubbard BP, Mercken EM, Palmeira CM, de Cabo R, Rolo AP, Turner N, Bell EL, Sinclair DA. Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell. 2013;155:1624-1638. doi: 10.1016/j.cell.2013.11.037.
41. Yang L, Vaitheesvaran B, Hartil K, Robinson AJ, Hoopmann MR, Eng JK, Kurland IJ, Bruce JE. The fasted/fed mouse metabolic acetylome: N6-acetylation differences suggest acetylation coordinates organ-specific fuel switching. J Proteome Res. 2011;10:4134-4149. doi: 10.1021/pr200313x.
42. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, Lombard DB, Grueter CA, Harris C, Biddinger S, Ilkayeva OR, Stevens RD, Li Y, Saha AK, Ruderman NB, Bain JR, Newgard CB, Farese RV Jr, Alt FW, Kahn CR, Verdin E. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature. 2010;464:121-125. doi: 10.1038/nature08778.
43. 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. doi: 10.1016/j.cmet.2010.11.015.
44. Shimazu T, Hirschey MD, Hua L, Dittenhafer-Reed KE, Schwer B, Lombard DB, Li Y, Bunkenborg J, Alt FW, Denu JM, Jacobson MP, Verdin E. SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab. 2010;12:654-661. doi: 10.1016/j.cmet.2010.11.003.
45. Horton JL, Martin OJ, Lai L, Riley NM, Richards AL, Vega RB, Leone TC, Pagliarini DJ, Muoio DM, Bedi KC, Jr., Margulies KB, Coon JJ and Kelly DP. Mitochondrial protein hyperacetylation in the failing heart. JCI Insight. 2016;2:e84897.
46. Chung HS, Wang SB, Venkatraman V, Murray CI, Van Eyk JE. Cysteine oxidative posttranslational modifications: emerging regulation in the cardiovascular system. Circ Res. 2013;112:382-392. doi: 10.1161/CIRCRESAHA.112.268680.
47. Murphy E, Kohr M, Menazza S, Nguyen T, Evangelista A, Sun J, Steenbergen C. Signaling by S-nitrosylation in the heart. J Mol Cell Cardiol. 2014;73:18-25. doi: 10.1016/j.yjmcc.2014.01.003.
48. Wells TN, Saxty BA. Redox control of catalysis in ATP-citrate lysate from rat liver. Eur J Biochem. 1992;204:249-255.
49. Alavian KN, Beutner G, Lazrove E, Sacchetti S, Park HA, Licznerski P, Li H, Nabili P, Hockensmith K, Graham M, Porter GA Jr, Jonas EA. An uncoupling channel within the c-subunit ring of the F1FO ATP synthase is the mitochondrial permeability transition pore. Proc Natl Acad Sci USA. 2014;111:10580-10585. doi: 10.1073/pnas.1401591111.
50. Bonora M, Bononi A, De Marchi E, Giorgi C, Lebiedzinska M, Marchi S, Patergnani S, Rimessi A, Suski JM, Wojtala A, Wieckowski MR, Kroemer G, Galluzzi L, Pinton P. Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition. Cell Cycle. 2013;12:674-683. doi: 10.4161/cc.23599.