Docosahexaenoic Acid Supplementation Does Not Improve Western Diet-Induced Cardiomyopathy in Rats

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Jeckel, Kimberly M ^a   Veeramachaneni, D N Rao ^a   Chicco, Adam J ^a   Chapman, Phillip L ^b   Mulligan, Christopher M ^a   Hegarty, Jennifer R ^c   Pagliassotti, Michael J ^a   Ferguson, Lindsay A ^d   Bouma, Gerrit J ^a   Frye, Melinda A ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b CO 80523jessicawitt colostateedunatetenhundfeld colostateeduzachking colostateeduhttp: amplabcolostateedu   (United States)

^c Engineering Research Center and Hydraulics Laboratory   (United States)

^d CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; COLLAGEN; DOCOSAHEXAENOIC ACID; DOCOSAPENTAENOIC ACID; FATTY ACID; ICOSAPENTAENOIC ACID; LEPTIN; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CARDIOMYOPATHY; CARDIOVASCULAR PARAMETERS; CELL ULTRASTRUCTURE; CELL VACUOLE; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DIET; DIET SUPPLEMENTATION; DIETARY INTAKE; ELECTROCARDIOGRAPHY; FATTY ACID BLOOD LEVEL; HEART LEFT VENTRICLE HYPERTROPHY; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART RATE; HYPERTENSION; INSULIN RESISTANCE; LIPID COMPOSITION; MACRONUTRIENT; MALE; MUSCLE ATROPHY; NONHUMAN; ORGAN WEIGHT; PROTEIN BLOOD LEVEL; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; RAT; STRAIN DIFFERENCE; SYSTOLIC BLOOD PRESSURE; TRANSMISSION ELECTRON MICROSCOPY; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN DIET;

ADIPONECTIN; ANIMALS; BLOTTING, WESTERN; CARDIOMYOPATHIES; DIET; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; ECHOCARDIOGRAPHY; FATTY ACIDS; LEPTIN; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRIGLYCERIDES;

RATTUS; RATTUS NORVEGICUS; RODENTIA;

EID: 84871548392     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051994     Document Type: Article

References (77)

1. Kenchaiah S, Evans JC, Levy D, Wilson PW, Benjamin EJ, et al. (2002) Obesity and the risk of heart failure. N Engl J Med 347: 305-313.
2. Kortelainen ML, Porvari K, (2011) Extreme obesity and associated cardiovascular disease verified at autopsy: time trends over 3 decades. Am J Forensic Med Pathol 32: 372-377.
3. Park J, Kim SH, Cho GY, Baik I, Kim NH, et al. (2011) Obesity phenotype and cardiovascular changes. J Hypertens 29: 1765-1772.
4. Lind L, Siegbahn A, Ingelsson E, Sundstrom J, Arnlov J, (2011) A detailed cardiovascular characterization of obesity without the metabolic syndrome. Arterioscler Thromb Vasc Biol 31: e27-34.
5. Wong CY, O'Moore-Sullivan T, Leano R, Byrne N, Beller E, et al. (2004) Alterations of left ventricular myocardial characteristics associated with obesity. Circulation 110: 3081-3087.
6. Tumuklu MM, Etikan I, Kisacik B, Kayikcioglu M, (2007) Effect of obesity on left ventricular structure and myocardial systolic function: assessment by tissue Doppler imaging and strain/strain rate imaging. Echocardiography 24: 802-809.
7. Rider OJ, Petersen SE, Francis JM, Ali MK, Hudsmith LE, et al. (2011) Ventricular hypertrophy and cavity dilatation in relation to body mass index in women with uncomplicated obesity. Heart 97: 203-208.
8. Amad KH, Brennan JC, Alexander JK, (1965) The cardiac pathology of chronic exogenous obesity. Circulation 32: 740-745.
9. Drazner MH, Rame JE, Marino EK, Gottdiener JS, Kitzman DW, et al. (2004) Increased left ventricular mass is a risk factor for the development of a depressed left ventricular ejection fraction within five years: the Cardiovascular Health Study. J Am Coll Cardiol 43: 2207-2215.
10. Kardys I, Deckers JW, Stricker BH, Vletter WB, Hofman A, et al. (2008) Echocardiographic parameters and all-cause mortality: the Rotterdam Study. Int J Cardiol 133: 198-204.
11. Levy D, Garrison RJ, Savage DD, Kannel WB, Castelli WP, (1990) Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med 322: 1561-1566.
12. Gardin JM, McClelland R, Kitzman D, Lima JA, Bommer W, et al. (2001) M-mode echocardiographic predictors of six- to seven-year incidence of coronary heart disease, stroke, congestive heart failure, and mortality in an elderly cohort (the Cardiovascular Health Study). Am J Cardiol 87: 1051-1057.
13. Duda MK, O'Shea KM, Tintinu A, Xu W, Khairallah RJ, et al. (2008) Fish oil, but not flaxseed oil, decreases inflammation and prevents pressure overload-induced cardiac dysfunction. Cardiovasc Res 81: 319-327.
14. Fang Y, Favre J, Vercauteren M, Laillet B, Remy-Jouet I, et al. (2011) Reduced cardiac remodelling and prevention of glutathione deficiency after omega-3 supplementation in chronic heart failure. Fundam Clin Pharmacol 25: 323-332.
15. Halade GV, Williams PJ, Lindsey ML, Fernandes G, (2011) Fish oil decreases inflammation and reduces cardiac remodeling in rosiglitazone treated aging mice. Pharmacol Res 63: 300-307.
16. Poudyal H, Panchal SK, Waanders J, Ward L, Brown L, (2011) Lipid redistribution by alpha-linolenic acid-rich chia seed inhibits stearoyl-CoA desaturase-1 and induces cardiac and hepatic protection in diet-induced obese rats. J Nutr Biochem 23: 153-162.
17. Jeckel KM, Miller KE, Chicco AJ, Chapman PL, Mulligan CM, et al. (2011) The role of dietary fatty acids in predicting myocardial structure in fat-fed rats. Lipids Health Dis 10: 92.
18. Schemmel R, Mickelsen O, Gill JL, (1970) Dietary obesity in rats: body weight and body fat accretion in seven strains of rats. J Nutr 100: 1041-1048.
19. West DB, Waguespack J, McCollister S, (1995) Dietary obesity in the mouse: interaction of strain with diet composition. Am J Physiol 268: R658-665.
20. Galan X, Llobera M, Ramirez I, (1994) Lipoprotein lipase and hepatic lipase in Wistar and Sprague-Dawley rat tissues. Differences in the effects of gender and fasting. Lipids 29: 333-336.
21. Esmaillzadeh A, Kimiagar M, Mehrabi Y, Azadbakht L, Hu FB, et al. (2007) Dietary patterns, insulin resistance, and prevalence of the metabolic syndrome in women. Am J Clin Nutr 85: 910-918.
22. Murtaugh MA, Herrick JS, Sweeney C, Baumgartner KB, Guiliano AR, et al. (2007) Diet composition and risk of overweight and obesity in women living in the southwestern United States. J Am Diet Assoc 107: 1311-1321.
23. Poudyal H, Campbell F, Brown L, (2010) Olive leaf extract attenuates cardiac, hepatic, and metabolic changes in high carbohydrate-, high fat-fed rats. J Nutr 140: 946-953.
24. Arterburn LM, Boswell KD, Koskelo E, Kassner SL, Kelly C, et al. (2000) A combined subchronic (90-day) toxicity and neurotoxicity study of a single-cell source of docosahexaenoic acid triglyceride (DHASCO oil). Food Chem Toxicol 38: 35-49.
25. Sergiel JP, Martine L, Raederstorff D, Grynberg A, Demaison L, (1998) Individual effects of dietary EPA and DHA on the functioning of the isolated working rat heart. Can J Physiol Pharmacol 76: 728-736.
26. Ayalew-Pervanchon A, Rousseau D, Moreau D, Assayag P, Weill P, et al. (2007) Long-term effect of dietary {alpha}-linolenic acid or decosahexaenoic acid on incorporation of decosahexaenoic acid in membranes and its influence on rat heart in vivo. Am J Physiol Heart Circ Physiol 293: H2296-2304.
27. Iyer A, Brown L, (2009) Fermented wheat germ extract (Avemar) in the treatment of cardiac remodeling and metabolic symptoms in rats. Evid Based Complement Alternat Med 2011: 1-10.
28. Higashino H, Simeonova K, Lambev I, Markov M, Suzuki A, (1995) Proper measurement of blood pressure and heart rate in SHRSP and WKY by an indirect volume-oscillometric method. Clin Exp Pharmacol Physiol (Suppl 22) pp. S292-293.
29. Kuwahara M, Sugano S, Yayou K, Tsubone H, Kobayashi H, (1991) Evaluation of a new tail-cuff method for blood pressure measurements in rats with special reference to the effects of ambient temperature. Jikken Dobutsu 40: 331-336.
30. Foppa M, Duncan BB, Rohde LE, (2005) Echocardiography-based left ventricular mass estimation. How should we define hypertrophy? Cardiovasc Ultrasound 3: 17.
31. Switzer BR, Summer GK, (1971) Improved method for hydroxyproline analysis in tissue hydrolyzates. Anal Biochem 39: 487-491.
32. Matyash V, Liebisch G, Kurzchalia TV, Shevchenko A, Schwudke D, (2008) Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. J Lipid Res 49: 1137-1146.
33. Kris-Etherton PM, Harris WS, Appel LJ, (2003) Omega-3 fatty acids and cardiovascular disease: new recommendations from the American Heart Association. Arterioscler Thromb Vasc Biol 23: 151-152.
34. Loh MY, Flatt WP, Martin RJ, Hausman DB, (1998) Dietary fat type and level influence adiposity development in obese but not lean Zucker rats. Proc Soc Exp Biol Med 218: 38-44.
35. McManus DD, Lyass A, Ingelsson E, Massaro JM, Meigs JB, et al. (2011) Relations of Circulating Resistin and Adiponectin and Cardiac Structure and Function: The Framingham Offspring Study. Obesity (Silver Spring) doi:10.1038/oby.2011.32.
36. Amin RH, Mathews ST, Alli A, Leff T, (2010) Endogenously produced adiponectin protects cardiomyocytes from hypertrophy by a PPARgamma-dependent autocrine mechanism. Am J Physiol Heart Circ Physiol 299: H690-698.
37. Essick EE, Ouchi N, Wilson RM, Ohashi K, Ghobrial J, et al. (2011) Adiponectin mediates cardioprotection in oxidative stress-induced cardiac myocyte remodeling. Am J Physiol Heart Circ Physiol 301: H984-993.
38. Guo Z, Qin Z, Zhang R, Li J, Yin Y, (2012) Effect of rosiglitazone on the expression of cardiac adiponectin receptors and NADPH oxidase in type 2 diabetic rats. Eur J Pharmacol 685: 116-125.
39. Mullen KL, Smith AC, Junkin KA, Dyck DJ, (2007) Globular adiponectin resistance develops independently of impaired insulin-stimulated glucose transport in soleus muscle from high-fat-fed rats. Am J Physiol Endocrinol Metab 293: E83-90.
40. Yi W, Sun Y, Gao E, Wei X, Lau WB, et al. (2011) Reduced cardioprotective action of adiponectin in high-fat diet-induced type II diabetic mice and its underlying mechanisms. Antioxid Redox Signal 15: 1779-1788.
41. Fujita M, Momose A, Ohtomo T, Nishinosono A, Tanonaka K, et al. (2011) Upregulation of fatty acyl-CoA thioesterases in the heart and skeletal muscle of rats fed a high-fat diet. Biol Pharm Bull 34: 87-91.
42. Rustan AC, Christiansen EN, Drevon CA, (1992) Serum lipids, hepatic glycerolipid metabolism and peroxisomal fatty acid oxidation in rats fed omega-3 and omega-6 fatty acids. Biochem J 283 (Pt 2) (): 333-339.
43. O'Shea KM, Chess DJ, Khairallah RJ, Hecker PA, Lei B, et al. (2010) Omega-3 polyunsaturated fatty acids prevent pressure overload-induced ventricular dilation and decrease in mitochondrial enzymes despite no change in adiponectin. Lipids Health Dis 9: 95.
44. Okere IC, Young ME, McElfresh TA, Chess DJ, Sharov VG, et al. (2006) Low carbohydrate/high-fat diet attenuates cardiac hypertrophy, remodeling, and altered gene expression in hypertension. Hypertension 48: 1116-1123.
45. McLennan PL, Abeywardena MY, Dallimore JA, Raederstorff D, (2011) Dietary fish oil preserves cardiac function in the hypertrophied rat heart. Br J Nutr doi:10.1017/S0007114511005915.
46. Glenn DJ, Wang F, Nishimoto M, Cruz MC, Uchida Y, et al. (2011) A murine model of isolated cardiac steatosis leads to cardiomyopathy. Hypertension 57: 216-222.
47. Riquelme CA, Magida JA, Harrison BC, Wall CE, Marr TG, et al. (2011) Fatty acids identified in the Burmese python promote beneficial cardiac growth. Science 334: 528-531.
48. Bordoni A, Astolfi A, Morandi L, Pession A, Danesi F, et al. (2007) N-3 PUFAs modulate global gene expression profile in cultured rat cardiomyocytes. Implications in cardiac hypertrophy and heart failure. FEBS Lett 581: 923-929.
49. Okere IC, Chandler MP, McElfresh TA, Rennison JH, Sharov V, 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: H38-44.
50. Turdi S, Kandadi MR, Zhao J, Huff AF, Du M, et al. (2011) Deficiency in AMP-activated protein kinase exaggerates high fat diet-induced cardiac hypertrophy and contractile dysfunction. J Mol Cell Cardiol 50: 712-722.
51. Powell BD, Redfield MM, Bybee KA, Freeman WK, Rihal CS, (2006) Association of obesity with left ventricular remodeling and diastolic dysfunction in patients without coronary artery disease. Am J Cardiol 98: 116-120.
52. Berkalp B, Cesur V, Corapcioglu D, Erol C, Baskal N, (1995) Obesity and left ventricular diastolic dysfunction. Int J Cardiol 52: 23-26.
53. Perona JS, Ruiz-Gutierrez V, (2005) Triacylglycerol molecular species are depleted to different extents in the myocardium of spontaneously hypertensive rats fed two oleic acid-rich oils. Am J Hypertens 18: 72-80.
54. Jalili T, Manning J, Kim S, (2003) Increased translocation of cardiac protein kinase C beta2 accompanies mild cardiac hypertrophy in rats fed saturated fat. J Nutr 133: 358-361.
55. Jude S, Martel E, Vincent F, Besson P, Couet C, et al. (2007) Dietary long-chain n-3 fatty acids modify blood and cardiac phospholipids and reduce protein kinase-C-delta and protein kinase-C-epsilon translocation. Br J Nutr 98: 1143-1151.
56. Akki A, Seymour AM, (2009) Western diet impairs metabolic remodelling and contractile efficiency in cardiac hypertrophy. Cardiovasc Res 81: 610-617.
57. Chicco AJ, Sparagna GC, McCune SA, Johnson CA, Murphy RC, et al. (2008) Linoleate-rich high-fat diet decreases mortality in hypertensive heart failure rats compared with lard and low-fat diets. Hypertension 52: 549-555.
58. Slee EL, McLennan PL, Owen AJ, Theiss ML, (2010) Low dietary fish-oil threshold for myocardial membrane n-3 PUFA enrichment independent of n-6 PUFA intake in rats. J Lipid Res 51: 1841-1848.
59. Lien EL, (2009) Toxicology and safety of DHA. Prostaglandins Leukot Essent Fatty Acids 81: 125-132.
60. Storlien LH, Jenkins AB, Chisholm DJ, Pascoe WS, Khouri S, et al. (1991) Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid. Diabetes 40: 280-289.
61. Oliveira Junior SA, Dal Pai-Silva M, Martinez PF, Lima-Leopoldo AP, Campos DH, et al. (2010) Diet-induced obesity causes metabolic, endocrine and cardiac alterations in spontaneously hypertensive rats. Med Sci Monit 16: BR367-373.
62. Qin YW, Ye P, He JQ, Sheng L, Wang LY, et al. (2010) Simvastatin inhibited cardiac hypertrophy and fibrosis in apolipoprotein E-deficient mice fed a "Western-style diet" by increasing PPAR alpha and gamma expression and reducing TC, MMP-9, and Cat S levels. Acta Pharmacol Sin 31: 1350-1358.
63. Gruber C, Kohlstedt K, Loot AE, Fleming I, Kummer W, et al. (2011) Stereological characterization of left ventricular cardiomyocytes, capillaries, and innervation in the nondiabetic, obese mouse. Cardiovasc Pathol doi:10.1016/j.carpath.2011.11.003.
64. Schaub MC, Hefti MA, Harder BA, Eppenberger HM, (1997) Various hypertrophic stimuli induce distinct phenotypes in cardiomyocytes. J Mol Med 75: 901-920.
65. Kong SW, Bodyak N, Yue P, Liu Z, Brown J, et al. (2005) Genetic expression profiles during physiological and pathological cardiac hypertrophy and heart failure in rats. Physiol Genomics 21: 34-42.
66. Xu FP, Chen MS, Wang YZ, Yi Q, Lin SB, et al. (2004) Leptin induces hypertrophy via endothelin-1-reactive oxygen species pathway in cultured neonatal rat cardiomyocytes. Circulation 110: 1269-1275.
67. Szczepaniak LS, Dobbins RL, Metzger GJ, Sartoni-D'Ambrosia G, Arbique D, et al. (2003) Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magn Reson Med 49: 417-423.
68. Sharma S, Adrogue JV, Golfman L, Uray I, Lemm J, et al. (2004) Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. FASEB J 18: 1692-1700.
69. Bartels ED, Nielsen JM, Bisgaard LS, Goetze JP, Nielsen LB, (2010) Decreased expression of natriuretic peptides associated with lipid accumulation in cardiac ventricle of obese mice. Endocrinology 151: 5218-5225.
70. Ouwens DM, Boer C, Fodor M, de Galan P, Heine RJ, et al. (2005) Cardiac dysfunction induced by high-fat diet is associated with altered myocardial insulin signalling in rats. Diabetologia 48: 1229-1237.
71. Ge F, Hu C, Hyodo E, Arai K, Zhou S, et al. (2012) Cardiomyocyte triglyceride accumulation and reduced ventricular function in mice with obesity reflect increased long chain fatty acid uptake and de novo fatty acid synthesis. J Obes doi:10.1155/2012/205648.
72. Wilson CR, Tran MK, Salazar KL, Young ME, Taegtmeyer H, (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.
73. Li Y, Cheng L, Qin Q, Liu J, Lo WK, et al. (2009) High-fat feeding in cardiomyocyte-restricted PPARdelta knockout mice leads to cardiac overexpression of lipid metabolic genes but fails to rescue cardiac phenotypes. J Mol Cell Cardiol 47: 536-543.
74. Dong F, Li Q, Sreejayan N, Nunn JM, Ren J, (2007) Metallothionein prevents high-fat diet induced cardiac contractile dysfunction: role of peroxisome proliferator activated receptor gamma coactivator 1alpha and mitochondrial biogenesis. Diabetes 56: 2201-2212.
75. Pulakat L, DeMarco VG, Ardhanari S, Chockalingam A, Gul R, et al. (2011) Adaptive mechanisms to compensate for overnutrition-induced cardiovascular abnormalities. Am J Physiol Regul Integr Comp Physiol 301: R885-895.
76. du Toit EF, Nabben M, Lochner A, (2005) A potential role for angiotensin II in obesity induced cardiac hypertrophy and ischaemic/reperfusion injury. Basic Res Cardiol 100: 346-354.
77. Oliveira SA Jr, Okoshi K, Lima-Leopoldo AP, Leopoldo AS, Campos DH, et al. (2009) Nutritional and cardiovascular profiles of normotensive and hypertensive rats kept on a high fat diet. Arq Bras Cardiol 93: 526-533.