Prolonged QT interval and lipid alterations beyond β-oxidation in very long-chain acyl-CoA dehydrogenase null mouse hearts

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 301, Issue 3, 2011, Pages

  Gélinas, Roselle ^a,b   Thompson Legault, Julie ^a,b   Bouchard, Bertrand ^b   Daneault, Caroline ^b   Mansour, Asmaa ^b   Gillis, Marc Antoine ^b   Charron, Guy ^b   Gavino, Victor ^a   Labarthe, François ^c   des Rosiers, Christine ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MONTREAL HEART INSTITUTE   (Canada)

^c UNIVERSITY HOSPITAL OF TOURS   (France)

Author keywords

Docosahexaenoic acid; Isolated working mouse heart perfusion; Metabolic fluxes; Triglycerides

Indexed keywords

ADRENALIN; CARBON 13; DOCOSAHEXAENOIC ACID; FISH OIL; LIPID; LONG CHAIN ACYL COENZYME A DEHYDROGENASE; MEMBRANE PHOSPHOLIPID; PALMITIC ACID; SATURATED FATTY ACID; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; DISORDERS OF LIPID AND LIPOPROTEIN METABOLISM; ELECTROCARDIOGRAM; ENERGY YIELD; ENZYME SUBSTRATE; EX VIVO STUDY; FATTY ACID OXIDATION; GENE EXPRESSION; HEART MUSCLE CONTRACTILITY; IN VIVO STUDY; LIPID DIET; LIPIDOMICS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; QT PROLONGATION; TELEMETRY;

ACYL-COA DEHYDROGENASE, LONG-CHAIN; AGE FACTORS; AGING; ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; ELECTROCARDIOGRAPHY, AMBULATORY; FISH OILS; HEART CONDUCTION SYSTEM; LIPID METABOLISM; LIVER; LONG QT SYNDROME; MALE; METABOLISM, INBORN ERRORS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIAL DISEASES; MUSCULAR DISEASES; MYOCARDIAL CONTRACTION; MYOCARDIUM; OXIDATION-REDUCTION; PALMITIC ACID; PERFUSION; TELEMETRY; TRIGLYCERIDES;

EID: 80052331171     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01275.2010     Document Type: Article

References (63)

1. Algra A, Tijssen JG, Roelandt JR, Pool J, Lubsen J. QTc prolongation measured by standard 12-lead electrocardiography is an independent risk factor for sudden death due to cardiac arrest. Circulation 83: 1888-1894, 1991.
2. Aoyama T, Uchida Y, Kelley RI, Marble M, Hofman K, Tonsgard JH, Rhead WJ, Hashimoto T. A novel disease with deficiency of mitochondrial very-long-chain acyl-CoA dehydrogenase. Biochem Biophys Res Commun 191: 1369-1372, 1993.
3. Barcelo-Coblijn G, Murphy EJ. Alpha-linolenic acid and its conversion to longer chain n-3 fatty acids: benefits for human health and a role in maintaining tissue n-3 fatty acid levels. Prog Lipid Res 48: 355-374, 2009.
4. Bertrand C, Largilliere C, Zabot MT, Mathieu M, Vianey-Saban C. Very long chain acyl-CoA dehydrogenase deficiency: identification of a new inborn error of mitochondrial fatty acid oxidation in fibroblasts. Biochim Biophys Acta 1180: 327-329, 1993.
5. Billman GE, Kang JX, Leaf A. Prevention of ischemia-induced cardiac sudden death by n-3 polyunsaturated fatty acids in dogs. Lipids 32: 1161-1168, 1997.
6. Bonnet D, Martin D, Pascale DL, Villain E, Jouvet P, Rabier D, Brivet M, Saudubray JM. Arrhythmias and conduction defects as presenting symptoms of fatty acid oxidation disorders in children. Circulation 100: 2248-2253, 1999.
7. Brindley DN, Kok BP, Kienesberger PC, Lehner R, Dyck JR. Shedding light on the enigma of myocardial lipotoxicity: the involvement of known and putative regulators of fatty acid storage and mobilization. Am J Physiol Endocrinol Metab 298: E897-E908, 2010.
8. Brouillette J, Grandy SA, Jolicoeur P, Fiset C. Cardiac repolarization is prolonged in CD4C/HIV transgenic mice. J Mol Cell Cardiol 43: 159-167, 2007.
9. Chegary M, Brinke H, Ruiter JP, Wijburg FA, Stoll MS, Minkler PE, van eeghel M W, Schulz H, Hoppel CL, Wanders RJ, Houten SM. Mitochondrial long chain fatty acid beta-oxidation in man and mouse. Biochim Biophys Acta 1791: 806-815, 2009.
10. Cox KB, Hamm DA, Millington DS, Matern D, Vockley J, Rinaldo P, Pinkert CA, Rhead WJ, Lindsey JR, Wood PA. Gestational, pathologic and biochemical differences between very long-chain acyl-CoA dehydrogenase deficiency and long-chain acyl-CoA dehydrogenase deficiency in the mouse. Hum Mol Genet 10: 2069-2077, 2001.
11. Das UN. Essential fatty acids: biochemistry, physiology and pathology. Biotechnol J 1: 420-439, 2006.
12. Drouin A, Gendron ME, Thorin E, Gillis MA, Mahlberg-Gaudin F, Tardif JC. Chronic heart rate reduction by ivabradine prevents endothelial dysfunction in dyslipidaemic mice. Br J Pharmacol 154: 749-757, 2008.
13. Ensenauer R, He M, Willard JM, Goetzman ES, Corydon TJ, Vandahl BB, Mohsen AW, Isaya G, Vockley J. Human acyl-CoA dehydrogenase-9 plays a novel role in the mitochondrial beta-oxidation of unsaturated fatty acids. J Biol Chem 280: 32309-32316, 2005.
14. Exil VJ, Gardner CD, Rottman JN, Sims H, Bartelds B, Khuchua Z, Sindhal R, Ni G, Strauss AW. Abnormal mitochondrial bioenergetics and heart rate dysfunction in mice lacking very-long-chain acyl-CoA dehydrogenase. Am J Physiol Heart Circ Physiol 290: H1289-H1297, 2006.
15. Exil VJ, Roberts RL, Sims H, McLaughlin JE, Malkin RA, Gardner CD, Ni G, Rottman JN, Strauss AW. Very-long-chain acyl-coenzyme a dehydrogenase deficiency in mice. Circ Res 93: 448-455, 2003.
16. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509, 1957.
17. Fukazawa K, Gologorsky E, Manmohansingh V, Nishida S, Vigoda MM, Pretto EA Jr. Is the immediate reversal of diastolic dysfunction of cirrhotic cardiomyopathy after liver transplantation a sign of the metabolic etiology? Liver Transpl 15: 1417-1419, 2009.
18. Gelinas R, Labarthe F, Bouchard B, Mc Duff J, Charron G, Young ME, Des Rosiers C. Alterations in carbohydrate metabolism and its regulation in PPARα null mouse hearts. Am J Physiol Heart Circ Physiol 294: H1571-H1580, 2008.
19. Gillingham M, Van Calcar S, Ney D, Wolff J, Harding C. Dietary management of long-chain 3-hydroxyacyl-CoA dehydrogenase deficiency (LCHADD). A case report and survey. J Inherit Metab Dis 22: 123-131, 1999.
20. Goetzman ES, Tian L, Wood PA. Differential induction of genes in liver and brown adipose tissue regulated by peroxisome proliferator-activated receptor-alpha during fasting and cold exposure in acyl-CoA dehydrogenase-deficient mice. Mol Genet Metab 84: 39-47, 2005.
21. Gregersen N, Andresen BS, Corydon MJ, Corydon TJ, Olsen RK, Bolund L, Bross P. Mutation analysis in mitochondrial fatty acid oxidation defects: exemplified by acyl-CoA dehydrogenase deficiencies, with special focus on genotype-phenotype relationship. Hum Mutat 18: 169-189, 2001.
22. Holm C. Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 31: 1120-1124, 2003.
23. Igarashi M, Ma K, Chang L, Bell JM, Rapoport SI. Rat heart cannot synthesize docosahexaenoic acid from circulating alpha-linolenic acid because it lacks elongase-2. J Lipid Res 49: 1735-1745, 2008.
24. Iozzo P. Metabolic toxicity of the heart: insights from molecular imaging. Nutr Metab Cardiovasc Dis 20: 147-156, 2010.
25. Izai K, Uchida Y, Orii T, Yamamoto S, Hashimoto T. Novel fatty acid beta-oxidation enzymes in rat liver mitochondria. I. Purification and properties of very-long-chain acyl-coenzyme A dehydrogenase. J Biol Chem 267: 1027-1033, 1992.
26. Jeron A, Mitchell GF, Zhou J, Murata M, London B, Buckett P, Wiviott SD, Koren G. Inducible polymorphic ventricular tachyarrhythmias in a transgenic mouse model with a long Q-T phenotype. Am J Physiol Heart Circ Physiol 278: H1891-H1898, 2000.
27. Jude S, Martel E, Vincent F, Besson P, Couet C, Ogilvie GK, Pinault M, De CC, Bougnoux P, Richard S, Champeroux P, Crozatier B, Le Guennec JY. Dietary long-chain n-3 fatty acids modify blood and cardiac phospholipids and reduce protein kinase-C-delta and protein kinase-Cepsilon translocation. Br J Nutr 98: 1143-1151, 2007.
28. Khairallah M, Labarthe F, Bouchard B, Danialou G, Petrof BJ, Des Rosiers C. Profiling substrate fluxes in the isolated working mouse heart using 13C-labeled substrates: focusing on the origin and fate of pyruvate and citrate carbons. Am J Physiol Heart Circ Physiol 286: H1461-H1470, 2004.
29. Khairallah RJ, Khairallah M, Gelinas R, Bouchard B, Young ME, Allen BG, Lopaschuk GD, Deschepper CF, Des Rosiers C. Cyclic GMP signaling in cardiomyocytes modulates fatty acid trafficking and prevents triglyceride accumulation. J Mol Cell Cardiol 45: 230-239, 2008.
30. Kluge S, Kuhnelt P, Block A, Merkel M, Gocht A, Lukacs Z, Kohlschutter A, Kreymann G. A young woman with persistent hypoglycemia, rhabdomyolysis, and coma: recognizing fatty acid oxidation defects in adults. Crit Care Med 31: 1273-1276, 2003.
31. Kovsan J, Bashan N, Greenberg A, Rudich A. Potential role of autophagy in modulation of lipid metabolism. Am J Physiol Endocrinol Metab 298: E1-E7, 2010.
32. Kris-Etherton PM, Harris WS, Appel LJ. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Arterioscler Thromb Vasc Biol 23: e20-e30, 2003.
33. Lepage G, Roy CC. Direct transesterification of all classes of lipids in a one-step reaction. J Lipid Res 27: 114-120, 1986.
34. Liebig M, Schymik I, Mueller M, Wendel U, Mayatepek E, Ruiter J, Strauss AW, Wanders RJ, Spiekerkoetter U. Neonatal screening for very long-chain acyl-coA dehydrogenase deficiency: enzymatic and molecular evaluation of neonates with elevated C14:1-carnitine levels. Pediatrics 118: 1065-1069, 2006.
35. London B, Albert C, Anderson ME, Giles WR, Van Wagoner DR, Balk E, Billman GE, Chung M, Lands W, Leaf A, McAnulty J, Martens JR, Costello RB, Lathrop DA. Omega-3 fatty acids and cardiac arrhythmias: prior studies and recommendations for future research: a report from the National Heart, Lung, and Blood Institute and Office of Dietary Supplements Omega-3 Fatty Acids and their Role in Cardiac Arrhythmogenesis Workshop. Circulation 116: e320-e335, 2007.
36. Lund AM, Dixon MA, Vreken P, Leonard JV, Morris AA. Plasma and erythrocyte fatty acid concentrations in long-chain 3-hydroxyacyl-CoA dehydrogenase deficiency. J Inherit Metab Dis 26: 410-412, 2003.
37. Mathur A, Sims HF, Gopalakrishnan D, Gibson B, Rinaldo P, Vockley J, Hug G, Strauss AW. Molecular heterogeneity in very-long-chain acyl-CoA dehydrogenase deficiency causing pediatric cardiomyopathy and sudden death. Circulation 99: 1337-1343, 1999.
38. Mitchell GF, Jeron A, Koren G. Measurement of heart rate and Q-T interval in the conscious mouse. Am J Physiol Heart Circ Physiol 274: H747-H751, 1998.
39. Moller S, Dumcke CW, Krag A. The heart and the liver. Expert Rev Gastroenterol Hepatol 3: 51-64, 2009.
40. Mozaffarian D, Prineas RJ, Stein PK, Siscovick DS. Dietary fish and n-3 fatty acid intake and cardiac electrocardiographic parameters in humans. J Am Coll Cardiol 48: 478-484, 2006.
41. Nair SS, Leitch J, Garg ML. Suppression of inositol phosphate release by cardiac myocytes isolated from fish oil-fed pigs. Mol Cell Biochem 215: 57-64, 2000.
42. Nair SS, Leitch J, Garg ML. N-3 polyunsaturated fatty acid supplementation alters inositol phosphate metabolism and protein kinase C activity in adult porcine cardiac myocytes. J Nutr Biochem 12: 7-13, 2001.
43. Nouws J, Nijtmans L, Houten SM, van den Brand M, Huynen M, Venselaar H, Hoefs S, Gloerich J, Kronick J, Hutchin T, Willems P, Rodenburg R, Wanders R, van den Heuvel L, Smeitink J, Vogel RO. Acyl-CoA dehydrogenase 9 is required for the biogenesis of oxidative phosphorylation complex I. Cell Metab 12: 283-294, 2010.
44. Rapoport SI, Igarashi M, Gao F. Quantitative contributions of diet and liver synthesis to docosahexaenoic acid homeostasis. Prostaglandins Leukot Essent Fatty Acids 82: 273-276, 2010.
45. Rousseau-Ralliard D, Moreau D, Guilland JC, Raederstorff D, Grynberg A. Docosahexaenoic acid, but not eicosapentaenoic acid, lowers ambulatory blood pressure and shortens interval QT in spontaneously hypertensive rats in vivo. Prostaglandins Leukot Essent Fatty Acids 80: 269-277, 2009.
46. Ruiz J, Antequera T, Andres AI, Petron M, Muriel E. Improvement of a solid phase extraction method for analysis of lipid fractions in muscle foods. Analytica Chimica Acta 520: 201-205, 2004.
47. Saudubray JM, Martin D, de Lonlay P, Touati G, Poggi-Travert F, Bonnet D, Jouvet P, Boutron M, Slama A, Vianey-Saban C, Bonnefont JP, Rabier D, Kamoun P, Brivet M. Recognition and management of fatty acid oxidation defects: a series of 107 patients. J Inherit Metab Dis 22: 488-502, 1999.
48. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ. Autophagy regulates lipid metabolism. Nature 458: 1131-1135, 2009.
49. Singh R, Xiang Y, Wang Y, Baikati K, Cuervo AM, Luu YK, Tang Y, Pessin JE, Schwartz GJ, Czaja MJ. Autophagy regulates adipose mass and differentiation in mice. J Clin Invest 119: 3329-3339, 2009.
50. Souri M, Aoyama T, Hoganson G, Hashimoto T. Very-long-chain acyl-CoA dehydrogenase subunit assembles to the dimer form on mitochondrial inner membrane. FEBS Lett 426: 187-190, 1998.
51. Spiekerkoetter U, Lindner M, Santer R, Grotzke M, Baumgartner MR, Boehles H, Das A, Haase C, Hennermann JB, Karall D, de Klerk H, Knerr I, Koch HG, Plecko B, Roschinger W, Schwab KO, Scheible D, Wijburg FA, Zschocke J, Mayatepek E, Wendel U. Treatment recommendations in long-chain fatty acid oxidation defects: consensus from a workshop. J Inherit Metab Dis 32: 498-505, 2009.
52. Spiekerkoetter U, Sun B, Zytkovicz T, Wanders R, Strauss AW, Wendel U. MS/MS-based newborn and family screening detects asymptomatic patients with very-long-chain acyl-CoA dehydrogenase deficiency. J Pediatr 143: 335-342, 2003.
53. Spiekerkoetter U, Tokunaga C, Wendel U, Mayatepek E, Exil V, Duran M, Wijburg FA, Wanders RJ, Strauss AW. Changes in blood carnitine and acylcarnitine profiles of very long-chain acyl-CoA dehydrogenase-deficient mice subjected to stress. Eur J Clin Invest 34: 191-196, 2004.
54. Spiekerkoetter U, Tokunaga C, Wendel U, Mayatepek E, Iilst L, Vaz FM, van Viies N, Overmars H, Duran M, Wijburg FA, Wanders RJ, Strauss AW. Tissue carnitine homeostasis in very-long-chain acyl-CoA dehydrogenase-deficient mice. Pediatr Res 57: 760-764, 2005.
55. Stillwell W, Wassall SR. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Phys Lipids 126: 1-27, 2003.
56. ter Veld F, Primassin S, Hoffmann L, Mayatepek E, Spiekerkoetter U. Corresponding increase in long-chain acyl-CoA and acylcarnitine after exercise in muscle from VLCAD mice. J Lipid Res 50: 1556-1562, 2009.
57. Vianey-Saban C, Divry P, Brivet M, Nada M, Zabot MT, Mathieu M, Roe C. Mitochondrial very-long-chain acyl-coenzyme A dehydrogenase deficiency: clinical characteristics and diagnostic considerations in 30 patients. Clin Chim Acta 269: 43-62, 1998.
58. Vincent G, Bouchard B, Khairallah M, Des Rosiers C. Differential modulation of citrate synthesis and release by fatty acids in perfused working rat hearts. Am J Physiol Heart Circ Physiol 286: H257-H266, 2004.
59. Watkins SM, Lin TY, Davis RM, Ching JR, DePeters EJ, Halpern GM, Walzem RL, German JB. Unique phospholipid metabolism in mouse heart in response to dietary docosahexaenoic or alpha-linolenic acids. Lipids 36: 247-254, 2001.
60. 2+ handling in very-long-chain acyl-CoA dehydrogenase null mice. Am J Physiol Heart Circ Physiol 292: H2202-H2211, 2007.
61. Wong F. Cirrhotic cardiomyopathy. Hepatol Int 3: 294-304, 2009.
62. Yamaguchi S, Indo Y, Coates PM, Hashimoto T, Tanaka K. Identification of very-long-chain acyl-CoA dehydrogenase deficiency in three patients previously diagnosed with long-chain acyl-CoA dehydrogenase deficiency. Pediatr Res 34: 111-113, 1993.
63. Zhang D, Christianson J, Liu ZX, Tian L, Choi CS, Neschen S, Dong J, Wood PA, Shulman GI. Resistance to high-fat diet-induced obesity and insulin resistance in mice with very long-chain acyl-CoA dehydrogenase deficiency. Cell Metab 11: 402-411, 2010.