Integrated Omic Analysis of a Guinea Pig Model of Heart Failure and Sudden Cardiac Death

Journal of Proteome Research

Volumn 15, Issue 9, 2016, Pages 3009-3028

  Brian Foster, D ^a   Liu, Ting ^a   Kammers, Kai ^b   O'Meally, Robert ^a   Yang, Ni ^a   Papanicolaou, Kyriakos N ^a   Conover Talbot, C ^a   Cole, Robert N ^a   O'Rourke, Brian ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

heart failure; hypertrophy; mass spectrometry; median sweep; metabolic bottleneck; metabolome; pathway analysis; proteome; proteomics; transcriptome

Indexed keywords

ACYL COENZYME A; ANTIOXIDANT; CARNITINE PALMITOYLTRANSFERASE I; CYCLIC NUCLEOTIDE; ION CHANNEL; PHOSPHOLAMBAN; RYANODINE RECEPTOR 2; UPSTREAM STIMULATORY FACTOR; FATTY ACID; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; DOWN REGULATION; FATTY ACID METABOLISM; GENE CONTROL; GUINEA PIG MODEL; HEART FAILURE; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE FIBROSIS; INTEGRATION; LIQUID CHROMATOGRAPHY; MASS FRAGMENTOGRAPHY; MASS SPECTROMETRY; METABOLITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SUDDEN CARDIAC DEATH; ANIMAL; CARDIOMEGALY; COMPLICATION; DISEASE COURSE; DISEASE MODEL; GUINEA PIG; HYPERTENSION; LIPID METABOLISM; METABOLISM; METABOLOME; METABOLOMICS; PROCEDURES; PROTEOMICS;

ANIMALS; CARDIOMEGALY; CITRIC ACID CYCLE; DEATH, SUDDEN, CARDIAC; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FATTY ACIDS; GUINEA PIGS; HEART FAILURE; HYPERTENSION; LIPID METABOLISM; METABOLOME; METABOLOMICS; PROTEOMICS; TRANSCRIPTOME;

EID: 84985994763     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.6b00149     Document Type: Article

References (77)

1. Go, A. S.; Mozaffarian, D.; Roger, V. L.; Benjamin, E. J.; Berry, J. D.; Blaha, M. J.; Dai, S.; Ford, E. S.; Fox, C. S.; Franco, S.; Fullerton, H. J.; Gillespie, C.; Hailpern, S. M.; Heit, J. A.; Howard, V. J.; Huffman, M. D.; Judd, S. E.; Kissela, B. M.; Kittner, S. J.; Lackland, D. T.; Lichtman, J. H.; Lisabeth, L. D.; Mackey, R. H.; Magid, D. J.; Marcus, G. M.; Marelli, A.; Matchar, D. B.; McGuire, D. K.; Mohler, E. R., 3rd; Moy, C. S.; Mussolino, M. E.; Neumar, R. W.; Nichol, G.; Pandey, D. K.; Paynter, N. P.; Reeves, M. J.; Sorlie, P. D.; Stein, J.; Towfighi, A.; Turan, T. N.; Virani, S. S.; Wong, N. D.; Woo, D.; Turner, M. B. Executive summary: heart disease and stroke statistics - 2014 update: a report from the American heart association Circulation 2014, 129 (3) 399-410 10.1161/01.cir.0000442015.53336.12
2. Heidenreich, P. A.; Albert, N. M.; Allen, L. A.; Bluemke, D. A.; Butler, J.; Fonarow, G. C.; Ikonomidis, J. S.; Khavjou, O.; Konstam, M. A.; Maddox, T. M.; Nichol, G.; Pham, M.; Pina, I. L.; Trogdon, J. G. Forecasting the impact of heart failure in the United States: a policy statement from the American Heart Association Circ.: Heart Failure 2013, 6 (3) 606-19 10.1161/HHF.0b013e318291329a
3. Cohn, J. N. Prognosis in congestive heart failure J. Card. Failure 1996, 2 (Suppl. 1) S225-9 10.1016/S1071-9164(96)80081-9
4. Cohn, J. N.; Archibald, D. G.; Ziesche, S.; Franciosa, J. A.; Harston, W. E.; Tristani, F. E.; Dunkman, W. B.; Jacobs, W.; Francis, G. S.; Flohr, K. H. et al. Effect of vasodilator therapy on mortality in chronic congestive heart failure. Results of a Veterans Administration Cooperative Study N. Engl. J. Med. 1986, 314 (24) 1547-52 10.1056/NEJM198606123142404
5. Liu, T.; Takimoto, E.; Dimaano, V. L.; DeMazumder, D.; Kettlewell, S.; Smith, G.; Sidor, A.; Abraham, T. P.; O'Rourke, B. Inhibiting mitochondrial Na+/Ca2+ exchange prevents sudden death in a Guinea pig model of heart failure Circ. Res. 2014, 115 (1) 44-54 10.1161/CIRCRESAHA.115.303062
6. Rosati, B.; Dong, M.; Cheng, L.; Liou, S. R.; Yan, Q.; Park, J. Y.; Shiang, E.; Sanguinetti, M.; Wang, H. S.; McKinnon, D. Evolution of ventricular myocyte electrophysiology Physiol. Genomics 2008, 35 (3) 262-72 10.1152/physiolgenomics.00159.2007
7. The Laboratory Rabbit, Guinea Pig, Hamster and Other Rodents; Suckow, M. A.; Stevens, K. A.; Wilson, R. P., Eds.; Academic Press: Waltham, MA, 2012.
8. Bers, D. Excitation-Contraction Coupling and Cardiac Contractile Force; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2001.
9. Kembro, J. M.; Aon, M. A.; Winslow, R. L.; O'Rourke, B.; Cortassa, S. Integrating mitochondrial energetics, redox and ROS metabolic networks: a two-compartment model Biophys. J. 2013, 104 (2) 332-343 10.1016/j.bpj.2012.11.3808
10. Zhou, L.; Aon, M. A.; Almas, T.; Cortassa, S.; Winslow, R. L.; O'Rourke, B. A reaction-diffusion model of ROS-Induced ROS release in a mitochondrial network PLoS Comput. Biol. 2010, 6 (1) e1000657 10.1371/journal.pcbi.1000657
11. Wei, A.-C.; Aon, M. A.; O'Rourke, B.; Winslow, R. L.; Cortassa, S. Mitochondrial energetics, pH regulation, and ion dynamics:a computational-experimental approach Biophys. J. 2011, 100 (12) 2894-2903 10.1016/j.bpj.2011.05.027
12. Liew, C. C.; Dzau, V. J. Molecular genetics and genomics of heart failure Nat. Rev. Genet. 2004, 5 (11) 811-25 10.1038/nrg1470
13. Margulies, K. B.; Bednarik, D. P.; Dries, D. L. Genomics, transcriptional profiling, and heart failure J. Am. Coll. Cardiol. 2009, 53 (19) 1752-9 10.1016/j.jacc.2008.12.064
14. Agnetti, G.; Husberg, C.; Van Eyk, J. E. Divide and conquer: the application of organelle proteomics to heart failure Circ. Res. 2011, 108 (4) 512-26 10.1161/CIRCRESAHA.110.226910
15. Franklin, S.; Chen, H.; Mitchell-Jordan, S.; Ren, S.; Wang, Y.; Vondriska, T. M. Quantitative analysis of the chromatin proteome in disease reveals remodeling principles and identifies high mobility group protein B2 as a regulator of hypertrophic growth Mol. Cell. Proteomics 2012, 11 (6) M111.014258 10.1074/mcp.M111.014258
16. Agnetti, G.; Kaludercic, N.; Kane, L. A.; Elliott, S. T.; Guo, Y.; Chakir, K.; Samantapudi, D.; Paolocci, N.; Tomaselli, G. F.; Kass, D. A.; Van Eyk, J. E. Modulation of mitochondrial proteome and improved mitochondrial function by biventricular pacing of dyssynchronous failing hearts Circ.: Cardiovasc. Genet. 2010, 3 (1) 78-87 10.1161/CIRCGENETICS.109.871236
17. Banfi, C.; Brioschi, M.; Wait, R.; Begum, S.; Gianazza, E.; Fratto, P.; Polvani, G.; Vitali, E.; Parolari, A.; Mussoni, L.; Tremoli, E. Proteomic analysis of membrane microdomains derived from both failing and non-failing human hearts Proteomics 2006, 6 (6) 1976-88 10.1002/pmic.200500278
18. Bugger, H.; Schwarzer, M.; Chen, D.; Schrepper, A.; Amorim, P. A.; Schoepe, M.; Nguyen, T. D.; Mohr, F. W.; Khalimonchuk, O.; Weimer, B. C.; Doenst, T. Proteomic remodelling of mitochondrial oxidative pathways in pressure overload-induced heart failure Cardiovasc. Res. 2010, 85 (2) 376-84 10.1093/cvr/cvp344
19. Baseler, W. A.; Dabkowski, E. R.; Williamson, C. L.; Croston, T. L.; Thapa, D.; Powell, M. J.; Razunguzwa, T. T.; Hollander, J. M. Proteomic alterations of distinct mitochondrial subpopulations in the type 1 diabetic heart: contribution of protein import dysfunction American journal of physiology. Regulatory, integrative and comparative physiology 2011, 300 (2) R186-200 10.1152/ajpregu.00423.2010
20. Jullig, M.; Hickey, A. J.; Chai, C. C.; Skea, G. L.; Middleditch, M. J.; Costa, S.; Choong, S. Y.; Philips, A. R.; Cooper, G. J. Is the failing heart out of fuel or a worn engine running rich? A study of mitochondria in old spontaneously hypertensive rats Proteomics 2008, 8 (12) 2556-72 10.1002/pmic.200700977
21. Monte, E.; Mouillesseaux, K.; Chen, H.; Kimball, T.; Ren, S.; Wang, Y.; Chen, J. N.; Vondriska, T. M.; Franklin, S. Systems proteomics of cardiac chromatin identifies nucleolin as a regulator of growth and cellular plasticity in cardiomyocytes American journal of physiology. Heart and circulatory physiology 2013, 305 (11) H1624-38 10.1152/ajpheart.00529.2013
22. Heinke, M. Y.; Wheeler, C. H.; Chang, D.; Einstein, R.; Drake-Holland, A.; Dunn, M. J.; dos Remedios, C. G. Protein changes observed in pacing-induced heart failure using two-dimensional electrophoresis Electrophoresis 1998, 19 (11) 2021-30 10.1002/elps.1150191122
23. Buscemi, N.; Doherty-Kirby, A.; Sussman, M. A.; Lajoie, G.; Van Eyk, J. E. Proteomic analysis of Rac1 transgenic mice displaying dilated cardiomyopathy reveals an increase in creatine kinase M-chain protein abundance Mol. Cell. Biochem. 2003, 251 (1-2) 145-51 10.1023/A:1025402520506
24. Chu, G.; Kerr, J. P.; Mitton, B.; Egnaczyk, G. F.; Vazquez, J. A.; Shen, M.; Kilby, G. W.; Stevenson, T. I.; Maggio, J. E.; Vockley, J.; Rapundalo, S. T.; Kranias, E. G. Proteomic analysis of hyperdynamic mouse hearts with enhanced sarcoplasmic reticulum calcium cycling FASEB J. 2004, 18 (14) 1725-7 10.1096/fj.04-2025fje
25. Sawicki, G.; Jugdutt, B. I. Detection of regional changes in protein levels in the in vivo canine model of acute heart failure following ischemia-reperfusion injury: functional proteomics studies Proteomics 2004, 4 (7) 2195-202 10.1002/pmic.200300746
26. Geiger, T.; Velic, A.; Macek, B.; Lundberg, E.; Kampf, C.; Nagaraj, N.; Uhlen, M.; Cox, J.; Mann, M. Initial Quantitative Proteomic Map of 28 Mouse Tissues Using the SILAC Mouse Mol. Cell. Proteomics 2013, 12 (6) 1709-1722 10.1074/mcp.M112.024919
27. Hammer, E.; Goritzka, M.; Ameling, S.; Darm, K.; Steil, L.; Klingel, K.; Trimpert, C.; Herda, L. R.; Dorr, M.; Kroemer, H. K.; Kandolf, R.; Staudt, A.; Felix, S. B.; Volker, U. Characterization of the human myocardial proteome in inflammatory dilated cardiomyopathy by label-free quantitative shotgun proteomics of heart biopsies J. Proteome Res. 2011, 10 (5) 2161-71 10.1021/pr1008042
28. Dai, D. F.; Hsieh, E. J.; Chen, T.; Menendez, L. G.; Basisty, N. B.; Tsai, L.; Beyer, R. P.; Crispin, D. A.; Shulman, N. J.; Szeto, H. H.; Tian, R.; MacCoss, M. J.; Rabinovitch, P. S. Global proteomics and pathway analysis of pressure-overload-induced heart failure and its attenuation by mitochondrial-targeted peptides Circ.: Heart Failure 2013, 6 (5) 1067-76 10.1161/CIRCHEARTFAILURE.113.000406
29. Gramolini, A. O.; Kislinger, T.; Alikhani-Koopaei, R.; Fong, V.; Thompson, N. J.; Isserlin, R.; Sharma, P.; Oudit, G. Y.; Trivieri, M. G.; Fagan, A.; Kannan, A.; Higgins, D. G.; Huedig, H.; Hess, G.; Arab, S.; Seidman, J. G.; Seidman, C. E.; Frey, B.; Perry, M.; Backx, P. H.; Liu, P. P.; MacLennan, D. H.; Emili, A. Comparative proteomics profiling of a phospholamban mutant mouse model of dilated cardiomyopathy reveals progressive intracellular stress responses Mol. Cell. Proteomics 2008, 7 (3) 519-33 10.1074/mcp.M700245-MCP200
30. Isserlin, R.; Merico, D.; Alikhani-Koupaei, R.; Gramolini, A.; Bader, G. D.; Emili, A. Pathway analysis of dilated cardiomyopathy using global proteomic profiling and enrichment maps Proteomics 2010, 10 (6) 1316-27 10.1002/pmic.200900412
31. Wittel, B.; Spann, J. F., Jr. Defective lipid metabolism in the failing heart J. Clin. Invest. 1968, 47 (8) 1787-94 10.1172/JCI105868
32. Bishop, S. P.; Altschuld, R. A. Increased glycolytic metabolism in cardiac hypertrophy and congestive failure Am. J. Physiol. 1970, 218 (1) 153-9
33. Taegtmeyer, H.; Overturf, M. L. Effects of moderate hypertension on cardiac function and metabolism in the rabbit Hypertension 1988, 11 (5) 416-26 10.1161/01.HYP.11.5.416
34. Christe, M. E.; Rodgers, R. L. Altered glucose and fatty acid oxidation in hearts of the spontaneously hypertensive rat J. Mol. Cell. Cardiol. 1994, 26 (10) 1371-5 10.1006/jmcc.1994.1155
35. 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 2002, 106 (5) 606-12 10.1161/01.CIR.0000023531.22727.C1
36. Irizarry, R. A.; Hobbs, B.; Collin, F.; Beazer-Barclay, Y. D.; Antonellis, K. J.; Scherf, U.; Speed, T. P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 2003, 4 (2) 249-264 10.1093/biostatistics/4.2.249
37. Kammers, K.; Cole, R. N.; Tiengwe, C.; Ruczinski, I. Detecting Significant Changes in Protein Abundance EuPa Open Proteomics 2015, 7, 11-19 10.1016/j.euprot.2015.02.002
38. Schwammle, V.; Leon, I. R.; Jensen, O. N. Assessment and improvement of statistical tools for comparative proteomics analysis of sparse data sets with few experimental replicates J. Proteome Res. 2013, 12 (9) 3874-83 10.1021/pr400045u
39. Storey, J. D. A direct approach to false discovery rates Journal of the Royal Statistical Society: Series B (Statistical Methodology) 2002, 64 (3) 479-498 10.1111/1467-9868.00346
40. Storey, J. D.; Tibshirani, R. Statistical significance for genomewide studies Proc. Natl. Acad. Sci. U. S. A. 2003, 100 (16) 9440-9445 10.1073/pnas.1530509100
41. Kramer, A.; Green, J.; Pollard, J., Jr.; Tugendreich, S. Causal analysis approaches in Ingenuity Pathway Analysis Bioinformatics 2014, 30 (4) 523-30 10.1093/bioinformatics/btt703
42. Herbrich, S. M.; Cole, R. N.; West, K. P., Jr.; Schulze, K.; Yager, J. D.; Groopman, J. D.; Christian, P.; Wu, L.; O'Meally, R. N.; May, D. H.; McIntosh, M. W.; Ruczinski, I. Statistical inference from multiple iTRAQ experiments without using common reference standards J. Proteome Res. 2013, 12 (2) 594-604 10.1021/pr300624g
43. Dias, P.; Terracciano, C. M. Hyperpolarization-activated cyclic nucleotide-gated channels and ventricular arrhythmias in heart failure: a novel target for therapy? J. Am. Heart Assoc. 2013, 2 (3) e000287 10.1161/JAHA.113.000287
44. Kuwahara, K.; Wang, Y.; McAnally, J.; Richardson, J. A.; Bassel-Duby, R.; Hill, J. A.; Olson, E. N. TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling J. Clin. Invest. 2006, 116 (12) 3114-3126 10.1172/JCI27702
45. Onohara, N.; Nishida, M.; Inoue, R.; Kobayashi, H.; Sumimoto, H.; Sato, Y.; Mori, Y.; Nagao, T.; Kurose, H. TRPC3 and TRPC6 are essential for angiotensin II-induced cardiac hypertrophy EMBO J. 2006, 25 (22) 5305-5316 10.1038/sj.emboj.7601417
46. Berkers, C. R.; Maddocks, O. D.; Cheung, E. C.; Mor, I.; Vousden, K. H. Metabolic regulation by p53 family members Cell Metab. 2013, 18 (5) 617-33 10.1016/j.cmet.2013.06.019
47. Izzo, A.; Manco, R.; Bonfiglio, F.; Cali, G.; De Cristofaro, T.; Patergnani, S.; Cicatiello, R.; Scrima, R.; Zannini, M.; Pinton, P.; Conti, A.; Nitsch, L. NRIP1/RIP140 siRNA-mediated attenuation counteracts mitochondrial dysfunction in Down syndrome Hum. Mol. Genet. 2014, 23 (16) 4406-19 10.1093/hmg/ddu157
48. Nautiyal, J.; Christian, M.; Parker, M. G. Distinct functions for RIP140 in development, inflammation, and metabolism Trends Endocrinol. Metab. 2013, 24 (9) 451-9 10.1016/j.tem.2013.05.001
49. Seth, A.; Steel, J. H.; Nichol, D.; Pocock, V.; Kumaran, M. K.; Fritah, A.; Mobberley, M.; Ryder, T. A.; Rowlerson, A.; Scott, J.; Poutanen, M.; White, R.; Parker, M. The transcriptional corepressor RIP140 regulates oxidative metabolism in skeletal muscle Cell Metab. 2007, 6 (3) 236-45 10.1016/j.cmet.2007.08.004
50. Shieh, P. B.; Hu, S. C.; Bobb, K.; Timmusk, T.; Ghosh, A. Identification of a signaling pathway involved in calcium regulation of BDNF expression Neuron 1998, 20 (4) 727-40 10.1016/S0896-6273(00)81011-9
51. Herzig, S.; Long, F.; Jhala, U. S.; Hedrick, S.; Quinn, R.; Bauer, A.; Rudolph, D.; Schutz, G.; Yoon, C.; Puigserver, P.; Spiegelman, B.; Montminy, M. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1 Nature 2001, 413 (6852) 179-83 10.1038/35093131
52. Yoon, J. C.; Puigserver, P.; Chen, G.; Donovan, J.; Wu, Z.; Rhee, J.; Adelmant, G.; Stafford, J.; Kahn, C. R.; Granner, D. K.; Newgard, C. B.; Spiegelman, B. M. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1 Nature 2001, 413 (6852) 131-8 10.1038/35093050
53. Xia, J.; Wishart, D. S. MSEA: a web-based tool to identify biologically meaningful patterns in quantitative metabolomic data Nucleic Acids Res. 2010, 38 (Web Server issue) W71-7 10.1093/nar/gkq329
54. Xia, J.; Wishart, D. S. MetPA: a web-based metabolomics tool for pathway analysis and visualization Bioinformatics 2010, 26 (18) 2342-4 10.1093/bioinformatics/btq418
55. Cheema-Dhadli, S.; Leznoff, C. C.; Halperin, M. L. Effect of 2-methylcitrate on citrate metabolism: implications for the management of patients with propionic acidemia and methylmalonic aciduria Pediatr. Res. 1975, 9 (12) 905-8 10.1203/00006450-197512000-00008
56. Cohn, J. N.; Archibald, D. G.; Ziesche, S.; Franciosa, J. A.; Harston, W. E.; Tristani, F. E.; Dunkman, W. B.; Jacobs, W.; Francis, G. S.; Flohr, K. H. et al. Effect of vasodilator therapy on mortality in chronic congestive heart failure. Results of a Veterans Administration Cooperative Study N. Engl. J. Med. 1986, 314 (24) 1547-52 10.1056/NEJM198606123142404
57. Braunwald, E. The war against heart failure: the Lancet lecture Lancet 2015, 385 (9970) 812-24 10.1016/S0140-6736(14)61889-4
58. Stengl, M. Experimental models of spontaneous ventricular arrhythmias and of sudden cardiac death Physiol Res. 2010, 59 (Suppl. 1) S25-31
59. Bers, D. M.; Bassani, J. W.; Bassani, R. A. Na-Ca exchange and Ca fluxes during contraction and relaxation in mammalian ventricular muscle Ann. N. Y. Acad. Sci. 1996, 779, 430-42 10.1111/j.1749-6632.1996.tb44818.x
60. Hofmann, F.; Fabritz, L.; Stieber, J.; Schmitt, J.; Kirchhof, P.; Ludwig, A.; Herrmann, S. Ventricular HCN channels decrease the repolarization reserve in the hypertrophic heart Cardiovasc. Res. 2012, 95 (3) 317-26 10.1093/cvr/cvs184
61. Kuwabara, Y.; Kuwahara, K.; Takano, M.; Kinoshita, H.; Arai, Y.; Yasuno, S.; Nakagawa, Y.; Igata, S.; Usami, S.; Minami, T.; Yamada, Y.; Nakao, K.; Yamada, C.; Shibata, J.; Nishikimi, T.; Ueshima, K.; Nakao, K. Increased expression of HCN channels in the ventricular myocardium contributes to enhanced arrhythmicity in mouse failing hearts J. Am. Heart Assoc. 2013, 2 (3) e000150 10.1161/JAHA.113.000150
62. Ceconi, C.; Freedman, S. B.; Tardif, J. C.; Hildebrandt, P.; McDonagh, T.; Gueret, P.; Parrinello, G.; Robertson, M.; Steg, P. G.; Tendera, M.; Ford, I.; Fox, K.; Ferrari, R. Effect of heart rate reduction by ivabradine on left ventricular remodeling in the echocardiographic substudy of BEAUTIFUL Int. J. Cardiol. 2011, 146 (3) 408-14 10.1016/j.ijcard.2010.10.125
63. Fox, K.; Ferrari, R.; Tendera, M.; Steg, P. G.; Ford, I. Rationale and design of a randomized, double-blind, placebo-controlled trial of ivabradine in patients with stable coronary artery disease and left ventricular systolic dysfunction: the morBidity-mortality EvAlUaTion of the I(f) inhibitor ivabradine in patients with coronary disease and left ventricULar dysfunction (BEAUTIFUL) study Am. Heart J. 2006, 152 (5) 860-6 10.1016/j.ahj.2006.01.013
64. U.S. Food and Drug Administration. FDA approves Corlanor to treat heart failure (April 15, 2015). http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm442978.htm (accessed Feb 18, 2016).
65. Liang, B.; Nissen, J. D.; Laursen, M.; Wang, X.; Skibsbye, L.; Hearing, M. C.; Andersen, M. N.; Rasmussen, H. B.; Wickman, K.; Grunnet, M.; Olesen, S. P.; Jespersen, T. G-protein-coupled inward rectifier potassium current contributes to ventricular repolarization Cardiovasc. Res. 2014, 101 (1) 175-84 10.1093/cvr/cvt240
66. Sansbury, B. E.; DeMartino, A. M.; Xie, Z.; Brooks, A. C.; Brainard, R. E.; Watson, L. J.; DeFilippis, A. P.; Cummins, T. D.; Harbeson, M. A.; Brittian, K. R.; Prabhu, S. D.; Bhatnagar, A.; Jones, S. P.; Hill, B. G. Metabolomic analysis of pressure-overloaded and infarcted mouse hearts Circ.: Heart Failure 2014, 7 (4) 634-42 10.1161/CIRCHEARTFAILURE.114.001151
67. Lai, L.; Leone, T. C.; Keller, M. P.; Martin, O. J.; Broman, A. T.; Nigro, J.; Kapoor, K.; Koves, T. R.; Stevens, R.; Ilkayeva, O. R.; Vega, R. B.; Attie, A. D.; Muoio, D. M.; Kelly, D. P. Energy metabolic reprogramming in the hypertrophied and early stage failing heart: a multisystems approach Circ.: Heart Failure 2014, 7 (6) 1022-31 10.1161/CIRCHEARTFAILURE.114.001469
68. Gupta, A.; Akki, A.; Wang, Y.; Leppo, M. K.; Chacko, V. P.; Foster, D. B.; Caceres, V.; Shi, S.; Kirk, J. A.; Su, J.; Lai, S.; Paolocci, N.; Steenbergen, C.; Gerstenblith, G.; Weiss, R. G. Creatine kinase-mediated improvement of function in failing mouse hearts provides causal evidence the failing heart is energy starved J. Clin. Invest. 2012, 122 (1) 291-302 10.1172/JCI57426
69. Finck, B. N.; Kelly, D. P. Peroxisome Proliferator-Activated Receptor I Coactivator-1 (PGC-1) Regulatory Cascade in Cardiac Physiology and Disease Circulation 2007, 115 (19) 2540-2548 10.1161/CIRCULATIONAHA.107.670588
70. Arany, Z.; Novikov, M.; Chin, S.; Ma, Y.; Rosenzweig, A.; Spiegelman, B. M. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-I coactivator 1α Proc. Natl. Acad. Sci. U. S. A. 2006, 103 (26) 10086-10091 10.1073/pnas.0603615103
71. Schilling, J. D. The Mitochondria in Diabetic Heart Failure: From Pathogenesis to Therapeutic Promise Antioxid. Redox Signaling 2015, 22 (17) 1515-1526 10.1089/ars.2015.6294
72. Ando, T.; Rasmussen, K.; Nyhan, W. L.; Hull, D. 3-hydroxypropionate: significance of -oxidation of propionate in patients with propionic acidemia and methylmalonic acidemia Proc. Natl. Acad. Sci. U. S. A. 1972, 69 (10) 2807-11 10.1073/pnas.69.10.2807
73. Ando, T.; Rasmussen, K.; Wright, J. M.; Nyhan, W. L. Isolation and identification of methylcitrate, a major metabolic product of propionate in patients with propionic acidemia J. Biol. Chem. 1972, 247 (7) 2200-4
74. Cowan, M. J.; Wara, D. W.; Packman, S.; Ammann, A. J.; Yoshino, M.; Sweetman, L.; Nyhan, W. Multiple biotin-dependent carboxylase deficiencies associated with defects in T-cell and B-cell immunity Lancet 1979, 314 (8134) 115-8 10.1016/S0140-6736(79)90002-3
75. Ampola, M. G.; Mahoney, M. J.; Nakamura, E.; Tanaka, K. Prenatal therapy of a patient with vitamin-B12-responsive methylmalonic acidemia N. Engl. J. Med. 1975, 293 (7) 313-7 10.1056/NEJM197508142930701
76. Edgar, R.; Domrachev, M.; Lash, A. E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Nucleic Acids Res. 2002, 30 (1) 207-210 10.1093/nar/30.1.207
77. Vizcaino, J. A.; Csordas, A.; Del-Toro, N.; Dianes, J. A.; Griss, J.; Lavidas, I.; Mayer, G.; Perez-Riverol, Y.; Reisinger, F.; Ternent, T.; Xu, Q. W.; Wang, R.; Hermjakob, H. 2016 update of the PRIDE database and its related tools Nucleic Acids Res. 2016, 44 (D1) D447-56 10.1093/nar/gkv1145