Early structural and metabolic cardiac remodelling in response to inducible adipose triglyceride lipase ablation

Cardiovascular Research

Volumn 99, Issue 3, 2013, Pages 442-451

  Kienesberger, Petra C ^a,g   Pulinilkunnil, Thomas ^a,g   Nagendran, Jeevan ^a   Young, Martin E ^b   Bogner Strauss, Juliane G ^c   Hackl, Hubert ^d   Khadour, Rammy ^a   Heydari, Emma ^a   Haemmerle, Guenter ^e   Zechner, Rudolf ^e   Kershaw, Erin E ^f   Dyck, Jason R B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b and Clinical Center   (United States)

^c GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^e UNIVERSITY OF GRAZ   (Austria)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^g DALHOUSIE UNIVERSITY   (Canada)

Author keywords

ATGL; Cardiomyopathy; Lipid metabolism; Lipid signalling; Remodelling

Indexed keywords

ADIPOSE TRIGLYCERIDE LIPASE; FATTY ACID; MITOCHONDRIAL ENZYME; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; DESNUTRIN PROTEIN, MOUSE;

ADULT; ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARDIAC REMODELLING; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ELECTRON MICROSCOPY; ENERGY METABOLISM; ENZYME DEFICIENCY; EX VIVO STUDY; FEMALE; GENE EXPRESSION; GENE TARGETING; GLUCOSE OXIDATION; HEART DISEASE; HEART FUNCTION; HEART MUSCLE METABOLISM; HYPERTROPHIC CARDIOMYOPATHY; IN VIVO STUDY; LIPID METABOLISM; MALE; MICROARRAY ANALYSIS; MOUSE; MYOCARDIAL STEATOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; SIGNAL TRANSDUCTION; STEATOSIS; TRANSTHORACIC ECHOCARDIOGRAPHY; UPREGULATION; ANIMAL; ATGL; C57BL MOUSE; CARDIOMYOPATHY; DISEASE MODEL; GENETICS; HEART MITOCHONDRION; HEART MUSCLE CELL; KNOCKOUT MOUSE; LIPID SIGNALLING; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; PATHOPHYSIOLOGY; REMODELLING; DEFICIENCY;

ATGL; CARDIOMYOPATHY; LIPID METABOLISM; LIPID SIGNALLING; REMODELLING;

ANIMALS; CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; FATTY ACIDS; LIPASE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; OXIDATION-REDUCTION; PPAR ALPHA; SIGNAL TRANSDUCTION;

EID: 84894455464     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt124     Document Type: Article

References (43)

1. Banke NH, Wende AR, Leone TC, O'Donnell JM, Abel ED, Kelly DP et al. Preferential oxidation of triacylglyceride-derived fatty acids in heart is augmented by the nuclear receptor PPARalpha. Circ Res 2010;107:233-241.
2. Kienesberger PC, Pulinilkunnil T, Nagendran J, Dyck JR. Myocardial triacylglycerol metabolism. J Mol Cell Cardiol 2013;55:101-110.
3. McGavock JM, Lingvay I, Zib I, Tillery T, Salas N, Unger R et al. Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 2007;116: 1170-1175.
4. McGavock JM, Victor RG, Unger RH, Szczepaniak LS. Adiposity of the heart, revisited. Ann Intern Med 2006;144:517-524.
5. Marfella R, Di Filippo C, Portoghese M, Barbieri M, Ferraraccio F, SiniscalchiMet al. Myocardial lipid accumulation in patients with pressure-overloaded heart and metabolic syndrome. J Lipid Res 2009;50:2314-2323.
6. Khan RS, Drosatos K, Goldberg IJ. Creating and curing fatty hearts. Curr Opin Clin Nutr Metab Care 2010;13:145-149.
7. Sharma S, Adrogue JV, Golfman L, Uray I, Lemm J, Youker K et al. Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. Faseb J 2004;18:1692-1700.
8. Christoffersen C, Bollano E, Lindegaard ML, Bartels ED, Goetze JP, Andersen CB et al. Cardiac lipid accumulation associated with diastolic dysfunction in obese mice. Endocrinology 2003;144:3483-3490.
9. Korosoglou G, Humpert PM, Ahrens J, Oikonomou D, OsmanNF, GitsioudisGet al. Left ventricular diastolic function in type 2 diabetes mellitus is associated with myocardial triglyceride content but not with impaired myocardial perfusion reserve. J Magn Reson Imaging 2012;35:804-811.
10. Goldberg IJ, TrentCM, Schulze PC. Lipid metabolism and toxicity in the heart. Cell Metab 2012;15:805-812.
11. McGavockJ, Szczepaniak LS, Ayers CR, Abdullah SM, See R, GoreMOet al. The effects of rosiglitazone on myocardial triglyceride content in patients with type 2 diabetes: a randomised, placebo-controlled trial. Diab Vasc Dis Res 2012;9:131-137.
12. Son NH, Yu S, Tuinei J, Arai K, Hamai H, Homma S et al. PPARgamma-induced cardiolipotoxicity in mice is ameliorated by PPARalpha deficiency despite increases in fatty acid oxidation. J Clin Invest 2010;120:3443-3454.
13. Chokshi A, Drosatos K, Cheema FH, Ji R, Khawaja T, Yu S et al. Ventricular assist device implantation corrects myocardial lipotoxicity, reverses insulin resistance, and normalizes cardiac metabolism in patients with advanced heart failure. Circulation 2012; 125:2844-2853.
14. Liu L, Shi X, Bharadwaj KG, Ikeda S, Yamashita H, Yagyu H et al. DGAT1 expression increases heart triglyceride content but ameliorates lipotoxicity. J Biol Chem 2009;284: 36312-36323.
15. Liu L, Yu S, Khan RS, Homma S, Schulze PC, Blaner WS et al. Diacylglycerol acyl transferase 1 overexpression detoxifies cardiac lipids in PPARgamma transgenic mice. J Lipid Res 2012;53:1482-1492.
16. Haemmerle G, Lass A, Zimmermann R, Gorkiewicz G, Meyer C, Rozman J et al. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 2006;312:734-737.
17. Hirano K, Ikeda Y, Zaima N, Sakata Y, Matsumiya G. Triglyceride deposit cardiomyovasculopathy. N Engl J Med 2008;359:2396-2398.
18. Schweiger M, Lass A, Zimmermann R, Eichmann TO, Zechner R. Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI-58/ABHD5. Am J Physiol Endocrinol Metab 2009;297:E289-E296.
19. Reilich P, Horvath R, Krause S, Schramm N, TurnbullDM, TrenellMet al. The phenotypic spectrum of neutral lipid storage myopathy due to mutations in the PNPLA2 gene. J Neurol 2011;258:1987-1997.
20. van deWeijerT, Havekes B, Bilet L, Hoeks J, Sparks L, BosmaMet al. Effects of bezafibrate treatment in a patient and a carrier with mutations in the PNPLA2 gene, causing neutral lipid storage disease with myopathy. Circ Res 2013;112:e51-e54.
21. Fischer J, Lefevre C, Morava E, Mussini JM, Laforet P, Negre-Salvayre A et al. The gene encoding adipose triglyceride lipase (PNPLA2) is mutated in neutral lipid storage disease with myopathy. Nat Genet 2007;39:28-30.
22. Utz W, Engeli S, Haufe S, Kast P, Hermsdorf M, Wiesner S et al. Myocardial steatosis, cardiac remodelling and fitness in insulin-sensitive and insulin-resistant obese women. Heart 2011;97:1585-1589.
23. Rijzewijk LJ, van der Meer RW, Smit JW, Diamant M, Bax JJ, Hammer S et al. Myocardial steatosis is an independent predictor of diastolic dysfunction in type 2 diabetes mellitus. J Am Coll Cardiol 2008;52:1793-1799.
24. NgAC, Delgado V, Bertini M, van der MeerRW, Rijzewijk LJ, Hooi EweS et al. Myocardial steatosis and biventricular strain and strain rate imaging in patients with type 2 diabetes mellitus. Circulation 2010;122:2538-2544.
25. Szczepaniak LS, Victor RG, Orci L, Unger RH. Forgotten but not gone: the rediscovery of fatty heart, the most common unrecognized disease in America. Circ Res 2007;101: 759-767.
26. Szczepaniak LS, Dobbins RL, Metzger GJ, Sartoni-D'Ambrosia G, Arbique D, VongpatanasinWet al. Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magn Reson Med 2003;49:417-423.
27. van der Meer RW, Rijzewijk LJ, Diamant M, Hammer S, Schar M, Bax JJ et al. The ageing male heart: myocardial triglyceride content as independent predictor of diastolic function. Eur Heart J 2008;29:1516-1522.
28. Haemmerle G, Moustafa T, Woelkart G, Buttner S, Schmidt A, van de Weijer T et al. ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-alpha and PGC-1. Nat Med 2011;17:1076-1085.
29. Kienesberger PC, Lee D, Pulinilkunnil T, Brenner DS, Cai L, Magnes C et al. Adipose triglyceride lipase deficiency causes tissue-specific changes in insulin signaling. J Biol Chem 2009;284:30218-30229.
30. Huang TT, Naeemuddin M, Elchuri S, Yamaguchi M, Kozy HM, Carlson EJ et al. Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Hum Mol Genet 2006;15:1187-1194.
31. Kienesberger PC, Pulinilkunnil T, Sung MM, Nagendran J, Haemmerle G, Kershaw EE et al. Myocardial ATGL overexpression decreases the reliance on fatty acid oxidation and protects against pressureoverload-induced cardiac dysfunction.Mol Cell Biol 2012;32:740-750.
32. O'Connell TD, Rodrigo MC, Simpson PC. Isolation and culture of adult mouse cardiac myocytes. Methods Mol Biol 2007;357:271-296.
33. Boudina S, Sena S, O'Neill BT, Tathireddy P, Young ME, Abel ED. Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 2005;112:2686-2695.
34. Tasseva G, Bai HD, Davidescu M, Haromy A, Michelakis E, Vance JE. Phosphatidylethanolamine deficiency in Mammalian mitochondria impairs oxidative phosphorylation and alters mitochondrial morphology. J Biol Chem 2013;288:4158-4173.
35. Tsai JY, Kienesberger PC, PulinilkunnilT, SailorsMH, Durgan DJ, Villegas-MontoyaCet al. Direct regulation of myocardial triglyceride metabolism by the cardiomyocyte circadian clock. J Biol Chem 2010;285:2918-2929.
36. Pinent M, Hackl H, Burkard TR, Prokesch A, Papak C, ScheidelerMet al. Differential transcriptional modulation of biological processes in adipocyte triglyceride lipase and hormone-sensitive lipase-deficient mice. Genomics 2008;92:26-32.
37. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate:APractical and Powerful Approach to Multiple Testing. J R Statist Soc B 1995;57:289-300.
38. Pulinilkunnil T, Kienesberger PC, Nagendran J, Waller TJ, Young ME, Kershaw EE et al. Myocardial adipose triglyceride lipase overexpression protects diabetic mice from the development of lipotoxic cardiomyopathy. Diabetes 2013;62:1464-177.
39. Bashyam MD, Savithri GR, Kumar MS, Narasimhan C, Nallari P. Molecular genetics of familial hypertrophic cardiomyopathy (FHC). J Hum Genet 2003;48:55-64.
40. Sorokina N, O'Donnell JM, McKinney RD, Pound KM, Woldegiorgis G, LaNoue KF et al. Recruitment of compensatory pathways to sustain oxidative flux with reduced carnitine palmitoyltransferase I activity characterizes inefficiency in energy metabolism in hypertrophied hearts. Circulation 2007;115:2033-2041.
41. Ueno M, Suzuki J, ZenimaruY, Takahashi S, KoizumiT, Noriki S et al. Cardiac overexpression of hormone-sensitive lipase inhibits myocardial steatosis and fibrosis in streptozotocin diabetic mice. Am J Physiol Endocrinol Metab 2008;294:E1109-E1118.
42. Suzuki J, Shen WJ, Nelson BD, Patel S, Veerkamp JH, Selwood SP et al. Absence of cardiac lipid accumulation in transgenic mice with heart-specific HSL overexpression. Am J Physiol Endocrinol Metab 2001;281:E857-E866.
43. Saddik M, Lopaschuk GD. Myocardial triglyceride turnover and contribution to energy substrate utilization in isolated working rat hearts. J Biol Chem 1991;266:8162-8170.