Western diet changes cardiac acyl-CoA composition in obese rats: A potential role for hepatic lipogenesis

Journal of Lipid Research

Volumn 51, Issue 6, 2010, Pages 1380-1393

  Harmancey, Romain ^a   Wilson, Christopher R ^a   Wright, Nathan R ^a   Taegtmeyer, Heinrich ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Dyslipidemia; Fatty acid; Heart failure; Lipotoxicity; Metabolic syndrome

Indexed keywords

ACYL COENZYME A; ACYL COENZYME A DESATURASE; CERAMIDE; DIACYLGLYCEROL; LIPID PEROXIDE; SATURATED FATTY ACID; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE FLUIDITY; CONTROLLED STUDY; FLUORESCENCE POLARIZATION; HEART FAILURE; HEART MUSCLE CONTRACTILITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID COMPOSITION; LIPID DIET; LIPID PEROXIDATION; LIPOGENESIS; MALE; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ACYL COENZYME A; ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL MEMBRANE; DIET; DIETARY CARBOHYDRATES; DIETARY FATS; FATTY ACIDS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEART; LIPID METABOLISM; LIPOGENESIS; LIVER; MALE; MUSCLE CONTRACTION; MYOCARDIUM; OBESITY; RATS; STEAROYL-COA DESATURASE;

EID: 77952688942     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M001230     Document Type: Article

References (54)

1. Kenchaiah, S., J. C. Evans, D. Levy, P. W. Wilson, E. J. Benjamin, M. G. Larson, W. B. Kannel, and R. Vasan. 2002. Obesity and the risk of heart failure. N. Engl. J. Med. 347: 305-313.
2. Smith, W. M. 1985. Epidemiology of congestive heart failure. Am. J. Cardiol. 55: 3A-8A.
3. Harmancey, R., C. R. Wilson, and H. Taegtmeyer. 2008. Adaptation and maladaptation of the heart in obesity. Hypertension. 52: 181-187.
4. Taegtmeyer, H., P. McNulty, and M. E. Young. 2002. Adaptation and maladaptation of the heart in diabetes: part I: general concepts. Circulation. 105: 1727-1733. (Pubitemid 34298619)
5. McGavock, J. M., I. Lingvay, I. Zib, T. Tillery, N. Salas, R. Unger, B. D. Levine, P. Raskin, R. G. Victor, and L. S. Szczepaniak. 2007. Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation. 116: 1170-1175.
6. Sharma, S., J. V. Adrogue, L. Golfman, I. Uray, J. Lemm, K. Youker, G. P. Noon, O. H. Frazier, and H. Taegtmeyer. 2004. Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. FASEB J. 18: 1692-1700. (Pubitemid 39463708)
7. Rijzewijk, L. J., R. W. van der Meer, J. W. Smit, M. Diamant, J. J. Bax, S. Hammer, J. A. Romijn, A. de Roos, and H. J. Lamb. 2008. Myocardial steatosis is an independent predictor of diastolic dysfunction in type 2 diabetes mellitus. J. Am. Coll. Cardiol. 52: 1793-1799.
8. Hsueh, W., E. D. Abel, J. L. Breslow, N. Maeda, R. C. Davis, E. A. Fisher, H. Dansky, D. A. McClain, R. McIndoe, M. K. Wassef, et al. 2007. Recipes for creating animal models of diabetic cardiovascular disease. Circ. Res. 100: 1415-1427. (Pubitemid 46834754)
9. Chiu, H. C., A. Kovacs, R. M. Blanton, X. Han, M. Courtois, C. J. Weinheimer, K. A. Yamada, S. Brunet, H. Xu, J. M. Nerbonne, et al. 2005. Transgenic expression of fatty acid transport protein 1 in the heart causes lipotoxic cardiomyopathy. Circ. Res. 96: 225-233.
10. Yagyu, H., G. Chen, M. Yokoyama, K. Hirata, A. Augustus, Y. Kako, T. Seo, Y. Hu, E. P. Lutz, M. Merkel, et al. 2003. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J. Clin. Invest. 111: 419-426. (Pubitemid 36182219)
11. Haemmerle, G., A. Lass, R. Zimmermann, G. Gorkiewicz, C. Meyer, J. Rozman, G. Heldmaier, R. Maier, C. Theussl, S. Eder, et al. 2006. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science. 312: 734-737.
12. Chiu, H. C., A. Kovacs, D. A. Ford, F. F. Hsu, R. Garcia, P. Herrero, J. E. Saffitz, and J. E. Schaffer. 2001. A novel mouse model of lipotoxic cardiomyopathy. J. Clin. Invest. 107: 813-822. (Pubitemid 32274034)
13. Finck, B. N., X. Han, M. Courtois, F. Aimond, J. M. Nerbonne, A. Kovacs, R. W. Gross, and D. P. Kelly. 2003. A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc. Natl. Acad. Sci. USA. 100: 1226-1231.
14. Finck, B. N., J. J. Lehman, T. C. Leone, M. J. Welch, M. J. Bennett, A. Kovacs, X. Han, R. W. Gross, R. Kozak, G. D. Lopaschuk, et al. 2002. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J. Clin. Invest. 109: 121-130.
15. Bonnard, C., A. Durand, S. Peyrol, E. Chanseaume, M. A. Chauvin, B. Morio, H. Vidal, and J. Rieusset. 2008. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J. Clin. Invest. 118: 789-800. (Pubitemid 351206566)
16. Boudina, S., S. Sena, H. Theobald, X. Sheng, J. J. Wright, X. X. Hu, S. Aziz, J. I. Johnson, H. Bugger, V. G. Zaha, et al. 2007. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes. 56: 2457-2466. (Pubitemid 47523253)
17. Borradaile, N. M., X. Han, J. D. Harp, S. E. Gale, D. S. Ory, and J. E. Schaffer. 2006. Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J. Lipid Res. 47: 2726-2737. (Pubitemid 44936086)
18. Summers, S. A. 2006. Ceramides in insulin resistance and lipotoxicity. Prog. Lipid Res. 45: 42-72.
19. Morino, K., K. F. Petersen, and G. I. Shulman. 2006. Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes. 55 ( Suppl 2): S9-S15. (Pubitemid 44927027)
20. Summers, S. A., and D. H. Nelson. 2005. A role for sphingolipids in producing the common features of type 2 diabetes, metabolic syndrome X, and Cushing's syndrome. Diabetes. 54: 591-602.
21. Aguila, M. B., and C. A. Mandarim-de-Lacerda. 2003. Heart and blood pressure adaptations in Wistar rats fed with different high-fat diets for 18 months. Nutrition. 19: 347-352.
22. Carroll, J. F., W. J. Zenebe, and T. B. Strange. 2006. Cardiovascular function in a rat model of diet-induced obesity. Hypertension. 48: 65-72. (Pubitemid 44297526)
23. Okere, I. C., M. P. Chandler, T. A. McElfresh, J. H. Rennison, T. A. Kung, B. D. Hoit, P. Ernsberger, M. E. Young, and W. C. Stanley. 2007. Carnitine palmitoyl transferase-I inhibition is not associated with cardiac hypertrophy in rats fed a high-fat diet. Clin. Exp. Pharmacol. Physiol. 34: 113-119.
24. Okere, I. C., M. P. Chandler, T. A. McElfresh, J. H. Rennison, V. Sharov, H. N. Sabbah, K. Y. Tserng, B. D. Hoit, P. Ernsberger, M. E. Young, et al. 2006. Differential effects of saturated and unsaturated fatty acid diets on cardiomyocyte apoptosis, adipose distribution, and serum leptin. Am. J. Physiol. Heart Circ. Physiol. 291: H38-H44.
25. Park, S. Y., Y. R. Cho, H. J. Kim, T. Higashimori, C. Danton, M. K. Lee, A. Dey, B. Rothermel, Y. B. Kim, A. Kalinowski, et al. 2005. Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes. 54: 3530-3540.
26. Relling, D. P., L. B. Esberg, C. X. Fang, W. T. Johnson, E. J. Murphy, E. C. Carlson, J. T. Saari, and J. Ren. 2006. High-fat diet-induced juvenile obesity leads to cardiomyocyte dysfunction and upregulation of Foxo3a transcription factor independent of lipotoxicity and apoptosis. J. Hypertens. 24: 549-561.
27. Faergeman, N. J., and J. Knudsen. 1997. Role of long-chain fatty acyl-CoA esters in the regulation of metabolism and in cell signalling. Biochem. J. 323: 1-12.
28. Schroeder, F., A. D. Petrescu, H. Huang, B. P. Atshaves, A. L. McIntosh, G. G. Martin, H. A. Hostetler, A. Vespa, D. Landrock, K. K. Landrock, et al. 2008. Role of fatty acid binding proteins and long chain fatty acids in modulating nuclear receptors and gene transcription. Lipids. 43: 1-17. (Pubitemid 351206956)
29. Wilson, C. R., M. K. Tran, K. L. Salazar, M. E. Young, and H. Taegtmeyer. 2007. Western diet, but not high fat diet, causes derangements of fatty acid metabolism and contractile dysfunction in the heart of Wistar rats. Biochem. J. 406: 457-467.
30. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
31. Previati, M., L. Bertolaso, M. Tramarin, V. Bertagnolo, and S. Capitani. 1996. Low nanogram range quantitation of diglycerides and ceramide by high-performance liquid chromatography. Anal. Biochem. 233: 108-114. (Pubitemid 26036368)
32. Mangino, M. J., J. Zografakis, M. K. Murphy, and C. B. Anderson. 1992. Improved and simplified tissue extraction method for quantitating long-chain acyl-coenzyme A thioesters with picomolar detection using high-performance liquid chromatography. J. Chromatogr. B. 577: 157-162.
33. Ohkawa, H., N. Ohishi, and K. Yagi. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95: 351-358. (Pubitemid 9194347)
34. Walaas, O., and E. Walaas. 1950. Effect of epinephrine on rat diaphragm. J. Biol. Chem. 187: 769-776.
35. Douce, R., C. A. Mannella, and W. D. Bonner, Jr. 1973. The external NADH dehydrogenases of intact plant mitochondria. Biochim. Biophys. Acta. 292: 105-116.
36. Miyazaki, M., F. E. Gomez, and J. M. Ntambi. 2002. Lack of stearoyl-CoA desaturase-1 function induces a palmitoyl-CoA Delta6 desaturase and represses the stearoyl-CoA desaturase-3 gene in the preputial glands of the mouse. J. Lipid Res. 43: 2146-2154. (Pubitemid 35471083)
37. Talamo, B. R., and K. Bloch. 1969. A new assay for fatty acid desaturation. Anal. Biochem. 29: 300-304.
38. Moon, Y. A., N. A. Shah, S. Mohapatra, J. A. Warrington, and J. D. Horton. 2001. Identification of a mammalian long chain fatty acyl elongase regulated by sterol regulatory element-binding proteins. J. Biol. Chem. 276: 45358-45366. (Pubitemid 37391332)
39. Wang, Y., D. Botolin, B. Christian, J. Busik, J. Xu, and D. B. Jump. 2005. Tissue-specific, nutritional, and developmental regulation of rat fatty acid elongases. J. Lipid Res. 46: 706-715. (Pubitemid 43073280)
40. Park, T. S., Y. Hu, H. L. Noh, K. Drosatos, K. Okajima, J. Buchanan, J. Tuinei, S. Homma, X. C. Jiang, E. D. Abel, et al. 2008. Ceramide is a cardiotoxin in lipotoxic cardiomyopathy. J. Lipid Res. 49: 2101-2112.
41. Aarsland, A., and R. R. Wolfe. 1998. Hepatic secretion of VLDL fatty acids during stimulated lipogenesis in men. J. Lipid Res. 39: 1280-1286. (Pubitemid 28270092)
42. Sul, H. S., and S. Smith. 2008. Fatty acid synthesis in eukaryotes. In Biochemistry of Lipids, Lipoproteins and Membranes. 5th ed. D. E. Vance and J. E. Vance, editors. Elsevier, Amsterdam, The Netherlands. 155-190.
43. Jeffcoat, R. 2007. Obesity - a perspective based on the biochemical interrelationship of lipids and carbohydrates. Med. Hypotheses. 68: 1159-1171. (Pubitemid 46274024)
44. Schwarz, J. M., P. Linfoot, D. Dare, and K. Aghajanian. 2003. Hepatic de novo lipogenesis in normoinsulinemic and hyperinsulinemic subjects consuming high-fat, low-carbohydrate and low-fat, high-carbohydrate isoenergetic diets. Am. J. Clin. Nutr. 77: 43-50.
45. Stanhope, K. L., J. M. Schwarz, N. L. Keim, S. C. Griffen, A. A. Bremer, J. L. Graham, B. Hatcher, C. L. Cox, A. Dyachenko, W. Zhang, et al. 2009. Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J. Clin. Invest. 119: 1322-1334.
46. Miyazaki, M., and J. M. Ntambi. 2008. Fatty acid desaturation and chain elongation in mammals. In Biochemistry of Lipids, Lipoproteins and Membranes. 5th ed. D. E. Vance and J. E. Vance, editors. Elsevier, Amsterdam, The Netherlands. 191-211.
47. Wang, Y., D. Botolin, J. Xu, B. Christian, E. Mitchell, B. Jayaprakasam, M. G. Nair, J. M. Peters, J. V. Busik, L. K. Olson, et al. 2006. Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity. J. Lipid Res. 47: 2028-2041. (Pubitemid 44401991)
48. Listenberger, L. L., X. Han, S. E. Lewis, S. Cases, R. V. Farese, Jr., D. S. Ory, and J. E. Schaffer. 2003. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. USA. 100: 3077-3082.
49. Diakogiannaki, E., H. J. Welters, and N. G. Morgan. 2008. Differential regulation of the endoplasmic reticulum stress response in pancreatic beta-cells exposed to long-chain saturated and monounsaturated fatty acids. J. Endocrinol. 197: 553-563. (Pubitemid 351803959)
50. Cao, H., K. Gerhold, J. R. Mayers, M. M. Wiest, S. M. Watkins, and G. S. Hotamisligil. 2008. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell. 134: 933-944.
51. Dowhan, W., M. Bogdanov, and E. Mileykovskaya. 2008. Functional roles of lipids in membranes. In Biochemistry of Lipids, Lipoproteins and Membranes. 5th ed. D. E. Vance and J. E. Vance, editors. Elsevier, Amsterdam, The Netherlands. 1-37.
52. Odiet, J. A., and J. Y. Wei. 1996. Heart failure and the aging myocardium: possible role of cardiac mitochondria. Heart Fail. Rev. 1: 139-149.
53. Chavez, J. A., and S. A. Summers. 2010. Lipid oversupply, selective insulin resistance, and lipotoxicity: molecular mechanisms. Biochim. Biophys. Acta. 1801: 252-265.
54. Marfella, R., C. Di Filippo, M. Portoghese, M. Barbieri, F. Ferraraccio, M. Siniscalchi, F. Cacciapuoti, F. Rossi, M. D'Amico, and G. Paolisso. 2009. Myocardial lipid accumulation in patients with pressure-overloaded heart and metabolic syndrome. J. Lipid Res. 50: 2314-2323.