Metabolic remodeling in moderate synchronous versus dyssynchronous pacing-induced heart failure: Integrated metabolomics and proteomics study

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Shibayama, Junko ^a   Yuzyuk, Tatiana N ^a,b   Cox, James ^a,c   Makaju, Aman ^a   Miller, Mickey ^a   Lichter, Justin ^a,d   Li, Hui ^a   Leavy, Jane D ^a   Franklin, Sarah ^a   Zaitsev, Alexey V ^a,d  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b ARUP LABORATORIES   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d University of Utah   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARNITINE; CARNITINE PARMITOYLTRANSFERASE I; CREATINE; CREATINE KINASE; CREATINE PHOSPHATE; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR PARAMETERS; CITRIC ACID CYCLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME REGULATION; FEMALE; GAS CHROMATOGRAPHY; GLYCOLYSIS; HEART ATRIUM PACING; HEART FAILURE; HEART HEMODYNAMICS; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART VENTRICLE PACING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LEFT VENTRICULAR SYSTOLIC PRESSURE; MALE; METABOLOMICS; NONHUMAN; PROTEOMICS; TANDEM MASS SPECTROMETRY; UPREGULATION; ANIMAL; CARDIAC MUSCLE; DOG; HEART VENTRICLE FUNCTION; MASS FRAGMENTOGRAPHY; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; TIME FACTOR;

ANIMALIA;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CITRIC ACID CYCLE; CREATINE; CREATINE KINASE; DOGS; ENERGY METABOLISM; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GLYCOLYSIS; HEART FAILURE; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MYOCARDIUM; PROTEOMICS; TANDEM MASS SPECTROMETRY; TIME FACTORS; VENTRICULAR DYSFUNCTION;

EID: 84961287987     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118974     Document Type: Article

References (70)

1. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, et al. Heart disease and stroke statistics - 2010 update: a report from the American Heart Association. Circulation. 2010; 121: e46-e215. doi: 10.1161/CIRCULATIONAHA.109.192667 PMID: 20019324
2. Iuliano S, Fisher SG, Karasik PE, Fletcher RD, Singh SN. QRS duration and mortality in patients with congestive heart failure. Am Heart J. 2002; 143: 1085-1091. PMID: 12075267
3. Sachse FB, Torres NS, Savio-Galimberti E, Aiba T, Kass DA, Tomaselli GF, et al. Subcellular structures and function of myocytes impaired during heart failure are restored by cardiac resynchronization therapy. Circ Res. 2012; 110: 588-597. doi: 10.1161/CIRCRESAHA.111.257428 PMID: 22253411
4. Agnetti G, Kaludercic N, Kane LA, Elliott ST, Guo Y, Chakir K, et al. Modulation of mitochondrial proteome and improved mitochondrial function by biventricular pacing of dyssynchronous failing hearts. Circ Cardiovasc Genet. 2010; 3: 78-87. doi: 10.1161/CIRCGENETICS.109.871236 PMID: 20160199
5. Aiba T, Hesketh GG, Barth AS, Liu T, Daya S, Chakir K, et al. Electrophysiological consequences of dyssynchronous heart failure and its restoration by resynchronization therapy. Circulation. 2009; 119: 1220-1230. doi: 10.1161/CIRCULATIONAHA.108.794834 PMID: 19237662
6. Lichter JG, Carruth E, Mitchell C, Barth AS, Aiba T, Kass DA, et al. Remodeling of the sarcomeric cytoskeleton in cardiac ventricular myocytes during heart failure and after cardiac resynchronization therapy. Journal of Molecular and Cellular Cardiology. 2014; 72: 186-195. doi: 10.1016/j.yjmcc.2014.03.012 PMID: 24657727
7. Shen W, Asai K, Uechi M, Mathier MA, Shannon RP, Vatner SF, et al. Progressive loss of myocardial ATP due to a loss of total purines during the development of heart failure in dogs: a compensatory role for the parallel loss of creatine. Circulation. 1999; 100: 2113-2118. PMID: 10562269
8. Spragg DD, Leclercq C, Loghmani M, Faris OP, Tunin RS, DiSilvestre D, et al. Regional alterations in protein expression in the dyssynchronous failing heart. Circulation. 2003; 108: 929-932. PMID: 12925451
9. Gao Z, Barth AS, DiSilvestre D, Akar FG, Tian Y, Tanskanen A, et al. Key pathways associated with heart failure development revealed by gene networks correlated with cardiac remodeling. Physiol Genomics. 2008; 35: 222-230. doi: 10.1152/physiolgenomics.00100.2007 PMID: 18780759
10. Osorio JC, Stanley WC, Linke A, Castellari M, Diep QN, Panchal AR, et al. Impaired Myocardial Fatty Acid Oxidation and Reduced Protein Expression of Retinoid X Receptor-α in Pacing-Induced Heart Failure. Circulation. 2002; 106: 606-612. PMID: 12147544
11. Shibayama J, Taylor TG, Venable PW, Rhodes NL, Gil RB, Warren M, et al. Metabolic determinants of electrical failure in ex-vivo canine model of cardiac arrest: evidence for the protective role of inorganic pyrophosphate. PLoS One. 2013; 8: e57821. doi: 10.1371/journal.pone.0057821 PMID: 23520482
12. Shakoury-Elizeh M, Protchenko O, Berger A, Cox J, Gable K, Dunn TM, et al. Metabolic response to iron deficiency in Saccharomyces cerevisiae. J Biol Chem. 2010; 285:14823-33. doi: 10.1074/jbc.M109.091710 PMID: 20231268
13. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008; 26: 1367-1372. doi: 10.1038/nbt.1511 PMID: 19029910
14. Luber CA, Cox J, Lauterbach H, Fancke B, Selbach M, Tschopp J, et al. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity. 2010; 32: 279-289. doi: 10.1016/j.immuni.2010.01.013 PMID: 20171123
15. Xia J, Psychogios N, Young N, Wishart DS. MetaboAnalyst: A web server for metabolomic data analysis and interpretation. Nucleic Acids Res. 2009; 37: W652-660. doi: 10.1093/nar/gkp356 PMID: 19429898
16. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS. MetaboAnalyst 2.0 - a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 2012; 40: W127-133. doi: 10.1093/nar/gks374 PMID: 22553367
17. Chakir K, Depry C, Dimaano VL, Zhu WZ, Vanderheyden M, Bartunek J, et al. Galphas-biased beta2-adrenergic receptor signaling from restoring synchronous contraction in the failing heart. Sci Transl Med. 2011; 3: 100ra188.
18. Des Rosiers C, Labarthe F, Lloyd SG, Chatham JC. Cardiac anaplerosis in health and disease: food for thought. Cardiovasc Res. 2011; 90: 210-219. doi: 10.1093/cvr/cvr055 PMID: 21398307
19. Bugger H, Schwarzer M, Chen D, Schrepper A, Amorim PA, Schoepe M, et al. Proteomic remodelling of mitochondrial oxidative pathways in pressure overload-induced heart failure. Cardiovasc Res. 2010; 85: 376-384. doi: 10.1093/cvr/cvp344 PMID: 19843514
20. Gibala MJ, Young ME, Taegtmeyer H. Anaplerosis of the citric acid cycle: role in energy metabolism of heart and skeletal muscle. Acta Physiol Scand. 2000; 168: 657-665. PMID: 10759602
21. Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010; 90: 207-258. doi: 10.1152/physrev.00015.2009 PMID: 20086077
22. Weisiger RA. Cytosolic fatty acid binding proteins catalyze two distinct steps in intracellular transport of their ligands. Mol Cell Biochem. 2002; 239: 35-43. PMID: 12479566
23. Betz A, Chance B. Phase Relationship of Glycolytic Intermediates in Yeast Cells with Oscillatory Metabolic Control. Arch Biochem Biophys. 1965; 109: 585-594. PMID: 14320501
24. Richter PH, Ross J. Oscillations and efficiency in glycolysis. Biophys Chem. 1980; 12: 285-297. PMID: 6452914
25. Chakir K, Daya SK, Aiba T, Tunin RS, Dimaano VL, Abraham TP, et al. Mechanisms of Enhanced β-Adrenergic Reserve From Cardiac Resynchronization Therapy. Circulation. 2009; 119: 1231-1240. doi: 10.1161/CIRCULATIONAHA.108.774752 PMID: 19237665
26. Ingwall JS. Energy metabolism in heart failure and remodelling. Cardiovasc Res. 2009; 81: 412-419. doi: 10.1093/cvr/cvn301 PMID: 18987051
27. 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. PMID: 9337189
28. Montgomery C, Hamilton N, Ianuzzo CD. Energy status of the rapidly paced canine myocardium in congestive heart failure. J Appl Physiol. 1992; 73: 2363-2367. PMID: 1490944
29. Cha YM, Dzeja PP, Redfield MM, Shen WK, Terzic A. Bioenergetic protection of failing atrial and ventricular myocardium by vasopeptidase inhibitor omapatrilat. Am J Physiol Heart Circ Physiol. 2006; 290: H1686-1692. PMID: 16339841
30. Lei B, Lionetti V, Young ME, Chandler MP, d'Agostino C, Kang E, et al. Paradoxical downregulation of the glucose oxidation pathway despite enhanced flux in severe heart failure. Journal of Molecular and Cellular Cardiology. 2004; 36: 567-576. PMID: 15081316
31. 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: 2837-2842. PMID: 8941110
32. Razeghi P, Young ME, Alcorn JL, Moravec CS, Frazier OH, Taegtmeyer H. Metabolic gene expression in fetal and failing human heart. Circulation. 2001; 104: 2923-2931. PMID: 11739307
33. Ardehali H, Sabbah HN, Burke MA, Sarma S, Liu PP, Cleland JG, et al. Targeting myocardial substrate metabolism in heart failure: potential for new therapies. Eur J Heart Fail. 2012; 14: 120-129. doi: 10.1093/eurjhf/hfr173 PMID: 22253453
34. Lionetti V, Stanley WC, Recchia FA. Modulating fatty acid oxidation in heart failure. Cardiovasc Res. 2011; 90: 202-209. doi: 10.1093/cvr/cvr038 PMID: 21289012
35. Southworth R, Davey KA, Warley A, Garlick PB. A reevaluation of the roles of hexokinase I and II in the heart. Am J Physiol Heart Circ Physiol. 2007; 292: H378-386. PMID: 16951044
36. Calmettes G, John SA, Weiss JN, Ribalet B. Hexokinase-mitochondrial interactions regulate glucose metabolism differentially in adult and neonatal cardiac myocytes. J Gen Physiol. 2013; 142: 425-436. doi: 10.1085/jgp.201310968 PMID: 24081983
37. Kodde IF, van der Stok J, Smolenski RT, de Jong JW. Metabolic and genetic regulation of cardiac energy substrate preference. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 2007; 146: 26-39.
38. Fueger PT, Shearer J, Krueger TM, Posey KA, Bracy DP, Heikkinen S, et al. Hexokinase II protein content is a determinant of exercise endurance capacity in the mouse. J Physiol. 2005; 566: 533-541. PMID: 15878951
39. Neglia D, De Caterina A, Marraccini P, Natali A, Ciardetti M, Vecoli C, et al. Impaired myocardial metabolic reserve and substrate selection flexibility during stress in patients with idiopathic dilated cardiomyopathy. Am J Physiol Heart Circ Physiol. 2007; 293: H3270-3278. PMID: 17921325
40. Williams RE, Kass DA, Kawagoe Y, Pak P, Tunin RS, Shah R, et al. Endomyocardial gene expression during development of pacing tachycardia- induced heart failure in the dog. Circulation Research. 1994; 75: 615-623. PMID: 7923607
41. Armstrong PW, Stopps TP, Ford SE, de Bold AJ. Rapid ventricular pacing in the dog: pathophysiologic studies of heart failure. Circulation. 1986; 74: 1075-1084. PMID: 2945673
42. Wilson JR, Douglas P, Hickey WF, Lanoce V, Ferraro N, Muhammad A, et al. Experimental congestive heart failure produced by rapid ventricular pacing in the dog: cardiac effects. Circulation 1987; 75: 857-867. PMID: 3829344
43. Jóhannsson E, Lunde PK, Heddle C, Sjaastad I, Thomas MJ, Bergersen L, et al. Upregulation of the Cardiac Monocarboxylate Transporter MCT1 in a Rat Model of Congestive Heart Failure. Circulation. 2001; 104: 729-734. PMID: 11489783
44. Yazaki Y, Isobe M, Takahashi W, Kitabayashi H, Nishiyama O, Sekiguchi M, et al. Assessment of myocardial fatty acid metabolic abnormalities in patients with idiopathic dilated cardiomyopathy using 123I BMIPP SPECT: correlation with clinicopathological findings and clinical course. Heart 1999; 81: 153-159. PMID: 9922350
45. Martin MA, Gomez MA, Guillen F, Bornstein B, Campos Y, Rubio JC, et al. Myocardial carnitine and carnitine palmitoyltransferase deficiencies in patients with severe heart failure. Biochim Biophys Acta. 2000; 1502: 330-336. PMID: 11068176
46. Chandler MP, Kerner J, Huang H, Vazquez E, Reszko A, Martini WZ, 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. PMID: 15191896
47. Morgan EE, Chandler MP, Young ME, McElfresh TA, Kung TA, Rennison JH, et al. Dissociation between gene and protein expression of metabolic enzymes in a rodent model of heart failure. Eur J Heart Fail. 2006; 8: 687-693. PMID: 16513421
48. Pieske B, Maier LS, Piacentino V 3rd, Weisser J, Hasenfuss G, Houser S, et al. Rate dependence of [Na+]i and contractility in nonfailing and failing human myocardium. Circulation. 2002; 106: 447-453. PMID: 12135944
49. Grube M, Ameling S, Noutsias M, Kock K, Triebel I, Bonitz K, et al. Selective regulation of cardiac organic cation transporter novel type 2 (OCTN2) in dilated cardiomyopathy. Am J Pathol. 2011; 178: 2547-2559. doi: 10.1016/j.ajpath.2011.02.020 PMID: 21641380
50. El-Aroussy W, Rizk A, Mayhoub G, Aleem SA, El-Tobgy S, Mokhtar MS. Plasma carnitine levels as a marker of impaired left ventricular functions. Mol Cell Biochem. 2000; 213: 37-41. PMID: 11129956
51. Ueland T, Svardal A, Oie E, Askevold ET, Nymoen SH, Bjorndal B, et al. Disturbed carnitine regulation in chronic heart failure - increased plasma levels of palmitoyl-carnitine are associated with poor prognosis. Int J Cardiol. 2013; 167: 1892-1899. doi: 10.1016/j.ijcard.2012.04.150 PMID: 22622056
52. Marin-Garcia J, Goldenthal MJ, Moe GW. Abnormal cardiac and skeletal muscle mitochondrial function in pacing-induced cardiac failure. Cardiovasc Res. 2001; 52: 103-110. PMID: 11557238
53. Hammer E, Goritzka M, Ameling S, Darm K, Steil L, Klingel K, et al. Characterization of the Human Myocardial Proteome in Inflammatory Dilated Cardiomyopathy by Label-free Quantitative Shotgun Proteomics of Heart Biopsies. J Proteome Res. 2011; 10: 2161-2171. doi: 10.1021/pr1008042 PMID: 21417265
54. Birner C, Dietl A, Deutzmann R, Schröder J, Schmid P, Jungbauer C, et al. Proteomic Profiling Implies Mitochondrial Dysfunction in Tachycardia-Induced Heart Failure. Journal of Cardiac Failure. 2012; 18: 660-673. doi: 10.1016/j.cardfail.2012.06.418 PMID: 22858083
55. Cieniewski-Bernard C, Mulder P, Henry J-P, Drobecq H, Dubois E, Pottiez Gnl, et al. Proteomic Analysis of Left Ventricular Remodeling in an Experimental Model of Heart Failure. J Proteome Res. 2008; 7: 5004-5016. doi: 10.1021/pr800409u PMID: 18922030
56. Ingwall JS, Weiss RG. Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ Res. 2004; 95: 135-145. PMID: 15271865
57. Ingwall JS. On the hypothesis that the failing heart is energy starved: lessons learned from the metabolism of ATP and creatine. Curr Hypertens Rep. 2006; 8: 457-464. PMID: 17087856
58. Ventura-Clapier R, Garnier A, Veksler V, Joubert F. Bioenergetics of the failing heart. Biochim Biophys Acta. 2011; 1813: 1360-1372. doi: 10.1016/j.bbamcr.2010.09.006 PMID: 20869993
59. Doenst T, Pytel G, Schrepper A, Amorim P, Farber G, Shingu Y, et al. Decreased rates of substrate oxidation ex vivo predict the onset of heart failure and contractile dysfunction in rats with pressure overload. Cardiovasc Res. 2010; 86: 461-470. doi: 10.1093/cvr/cvp414 PMID: 20035032
60. Garnier A, Fortin D, Delomenie C, Momken I, Veksler V, Ventura-Clapier R. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. J Physiol. 2003; 551: 491-501. PMID: 12824444
61. Oka S, Alcendor R, Zhai P, Park JY, Shao D, Cho J, et al. PPARalpha-Sirt1 complex mediates cardiac hypertrophy and failure through suppression of the ERR transcriptional pathway. Cell Metab. 2011; 14: 598-611. doi: 10.1016/j.cmet.2011.10.001 PMID: 22055503
62. Karbowska J, Kochan Z, Smolenski RT. Peroxisome proliferator-activated receptor alpha is downregulated in the failing human heart. Cell Mol Biol Lett. 2003; 8: 49-53. PMID: 12655356
63. Karamanlidis G, Nascimben L, Couper GS, Shekar PS, del Monte F, Tian R. Defective DNA replication impairs mitochondrial biogenesis in human failing hearts. Circ Res. 2010; 106: 1541-1548. doi: 10.1161/CIRCRESAHA.109.212753 PMID: 20339121
64. Sihag S, Cresci S, Li AY, Sucharov CC, Lehman JJ. PGC-1alpha and ERRalpha target gene downregulation is a signature of the failing human heart. J Mol Cell Cardiol. 2009; 46: 201-212. doi: 10.1016/j.yjmcc.2008.10.025 PMID: 19061896
65. Barth AS, Kumordzie A, Frangakis C, Margulies KB, Cappola TP, Tomaselli GF. Reciprocal transcriptional regulation of metabolic and signaling pathways correlates with disease severity in heart failure. Circ Cardiovasc Genet. 2011; 4: 475-483. doi: 10.1161/CIRCGENETICS.110.957571 PMID: 21828333
66. Cordero-Reyes AM, Gupte AA, Youker KA, Loebe M, Hsueh WA, Torre-Amione G, et al. Freshly isolated mitochondria from failing human hearts exhibit preserved respiratory function. J Mol Cell Cardiol. 2014; 68: 98-105. doi: 10.1016/j.yjmcc.2013.12.029 PMID: 24412531
67. Schupp M, Kintscher U, Fielitz J, Thomas J, Pregla R, Hetzer R, et al. (2006) Cardiac PPARalpha expression in patients with dilated cardiomyopathy. Eur J Heart Fail. 2006; 8: 290-294. PMID: 16307905
68. Garcia-Rua V, Otero MF, Lear PV, Rodriguez-Penas D, Feijoo-Bandin S, Noguera-Moreno T, et al. Increased expression of fatty-acid and calcium metabolism genes in failing human heart. PLoS One 2012; 7: e37505. doi: 10.1371/journal.pone.0037505 PMID: 22701570
69. Pak PH, Nuss HB, Tunin RS, Kaab S, Tomaselli GF, Marban E, et al. Repolarization abnormalities, arrhythmia and sudden death in canine tachycardia-induced cardiomyopathy. J Am Coll Cardiol. 1997; 30: 576-584. PMID: 9247535
70. Wang TJ, Ngo D, Psychogios N, Dejam A, Larson MG, Vasan RS, et al. 2-Aminoadipic acid is a biomarker for diabetes risk. J Clin Invest. 2013; 123: 4309-4317. doi: 10.1172/JCI64801 PMID: 24091325