Dietary saturated fat and docosahexaenoic acid differentially effect cardiac mitochondrial phospholipid fatty acyl composition and ca2+ uptake, without altering permeability transition or left ventricular function

Physiological Reports

Volumn 1, Issue 1, 2013, Pages

  O'connell, Kelly A ^a   Dabkowski, Erinne R ^a   Galvao, Tatiana de Fatima ^a,b   Xu, Wenhong ^a   Daneault, Caroline ^c   des Rosiers, Christine ^c   Stanley, William C ^a,d  

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

^b HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

^c MONTREAL HEART INSTITUTE   (Canada)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cardiovascular; Mitochondria n3 polyunsaturated fatty acids; Nutrition; Phospholipid; Saturated fatty acids

Indexed keywords

ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; DOCOSAPENTAENOIC ACID; FATTY ACID; ICOSAPENTAENOIC ACID; LINOLEIC ACID; MITOCHONDRIAL PROTEIN; MONOUNSATURATED FATTY ACID; OLEIC ACID; PALMITIC ACID; PALMITOYLCARNITINE; POLYUNSATURATED FATTY ACID; STEARIC ACID; TRIACYLGLYCEROL; VACCENIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CALCIUM TRANSPORT; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENZYMATIC ASSAY; FAT INTAKE; FLUORESCENCE; FLUORESCENCE POLARIZATION; HEART LEFT VENTRICLE FUNCTION; HEART VOLUME; MALE; MASS FRAGMENTOGRAPHY; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION SWELLING; NONHUMAN; RAT; RESPIRATION CONTROL; TRANSESTERIFICATION;

EID: 85009104988     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.1002/phy2.9     Document Type: Article

References (36)

1. Asemu, G., K. A. O’Connell, J. W. Cox, E. R. Dabkowski, W. Xu, R. F. Ribeiro Jr., et al. 2013. Enhanced resistance to permeability transition in interfibrillar cardiac mitochondria in dogs: effects of aging and long-term aldosterone infusion. Am. J. Physiol. Heart Circ. Physiol. 304: H514–H528.
2. Astrup, A., J. Dyerberg, P. Elwood, K. Hermansen, F. B. Hu, M. U. Jakobsen, et al. 2011. The role of reducing intakes of saturated fat in the prevention of cardiovascular disease: where does the evidence stand in 2010? Am. J. Clin. Nutr. 93: 684–688.
3. Berthiaume, J. M., M. S. Bray, T. A. McElfresh, X. Chen, S. Azam, M. E. Young, et al. 2010. The myocardial contractile response to physiological stress improves with high saturated fat feeding in heart failure. Am. J. Physiol. Heart Circ. Physiol. 299: H410–H421.
4. Brand, M. D., and D. G. Nicholls. 2011. Assessing mitochondrial dysfunction in cells. Biochem. J. 435: 297–312.
5. Brochot, A., M. Guinot, D. Auchere, J. P. Macaire, P. Weill, A. Grynberg, et al. 2009. Effects of alpha-linolenic acid vs. docosahexaenoic acid supply on the distribution of fatty acids among the rat cardiac subcellular membranes after a short-or long-term dietary exposure. Nutr. Metab. (Lond.) 6: 14.
6. Chess, D. J., R. J. Khairallah, K. M. O’shea, W. Xu, and W. C. Stanley. 2009. A high-fat diet increases adiposity but maintains mitochondrial oxidative enzymes without affecting development of heart failure with pressure overload. Am. J. Physiol. Heart Circ. Physiol. 297: H1585–H1593.
7. Duda, M. K., K. M. O’shea, B. Lei, B. R. Barrows, A. M. Azimzadeh, T. E. McElfresh, et al. 2008. Low-carbohydrate/high-fat diet attenuates pressure overload-induced ventricular remodeling and dysfunction. J. Card. Fail. 14: 327–335.
8. Duda, M. K., K. M. O’shea, A. Tintinu, W. Xu, R. J. Khairallah, B. R. Barrows, et al. 2009. Fish oil, but not flaxseed oil, decreases inflammation and prevents pressure overload-induced cardiac dysfunction. Cardiovasc. Res. 81: 319–327.
9. Galvao, T. F., B. H. Brown, P. A. Hecker, K. A. O’Connell, K. M. O’shea, H. N. Sabbah, et al. 2012. High intake of saturated fat, but not polyunsaturated fat, improves survival in heart failure despite persistent mitochondrial defects. Cardiovasc. Res. 93: 24–32.
10. Galvao, T. F., R. J. Khairallah, E. R. Dabkowski, B. H. Brown, P. A. Hecker, K. A. O’Connell, et al. 2013. Marine n3 polyunsaturated fatty acids enhance resistance to mitochondrial permeability transition in heart failure, but do not improve survival. Am. J. Physiol. Heart Circ. Physiol. 73: H12–H21.
11. Gelinas, R., J. Thompson-Legault, B. Bouchard, C. Daneault, A. Mansour, M. A. Gillis, et al. 2011. Prolonged QT interval and lipid alterations beyond {beta}-oxidation in very long-chain acyl-CoA dehydrogenase null mouse hearts. Am. J. Physiol. Heart Circ. Physiol. 301: H813–H823.
12. Heather, L. C., C. A. Carr, D. J. Stuckey, S. Pope, K. J. Morten, E. E. Carter, et al. 2010. Critical role of complex III in the early metabolic changes following myocardial infarction. Cardiovasc. Res. 85: 127–136.
13. Hofer, T., S. Servais, A. Y. Seo, E. Marzetti, A. Hiona, S. J. Upadhyay, et al. 2009. Bioenergetics and permeability transition pore opening in heart subsarcolemmal and interfibrillar mitochondria: effects of aging and lifelong calorie restriction. Mech. Ageing Dev. 130: 297–307.
14. Kasumov, T., E. R. Dabkowski, K. C. Shekar, L. Li, R. F. Ribeiro Jr., K. Walsh, et al. 2013. Assessment of cardiac proteome dynamics with heavy water: slower protein synthesis rates in interfibrillar than subsarcolemmal mitochondria. Am. J. Physiol. Heart Circ. Physiol. 304: H1201–H1214.
15. 2+-induced mitochondria permeability transition in normal and hypertrophied myocardium. J. Pharmacol. Exp. Ther. 335: 155–162.
16. Khairallah, R. J., G. C. Sparagna, N. Khanna, K. M. O’shea, P. A. Hecker, T. Kristian, et al. 2010b. Dietary supplementation with docosahexaenoic acid, but not eicosapentaenoic acid, dramatically alters cardiac mitochondrial phospholipid fatty acid composition and prevents permeability transition. Biochim. Biophys. Acta 1797: 1555–1562.
17. Khairallah, R. J., J. Kim, K. M. O’Shea, K. A. O’Connell, B. H. Brown, T. Galvao. 2012, et al. Improved mitochondrial function with diet-induced increase in either docosahexaenoic acid or arachidonic acid in membrane phospholipids. PLoS ONE 7: e34402.
18. 2+-induced mitochondrial permeability transition. J. Pharmacol. Exp. Ther. 321: 707–715.
19. McCormack, J. G., A. P. Halestrap, and R. M. Denton. 1990. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev. 70: 391–425.
20. Moon, S. H., C. M. Jenkins, X. Liu, S. Guan, D. J. Mancuso, and R. W. Gross. 2012. Activation of mitochondrial calcium-independent phospholipase A2gamma (iPLA2gamma) by divalent cations mediating arachidonate release and production of downstream eicosanoids. J. Biol. Chem. 287: 14880–14895.
21. Okere, I. C., D. J. Chess, T. A. McElfresh, J. Johnson, J. Rennison, P. Ernsberger, et al. 2005. High-fat diet prevents cardiac hypertrophy and improves contractile function in the hypertensive DAHL salt-sensitive rat. Clin. Exp. Pharmacol. Physiol. 32: 825–831.
22. Okere, I. C., M. E. Young, T. A. McElfresh, D. J. Chess, V. G. Sharov, H. N. Sabbah, et al. 2006. Low carbohydrate/ high-fat diet attenuates cardiac hypertrophy, remodeling, and altered gene expression in hypertension. Hypertension 48: 1116–1123.
23. 2+-induced permeability transition. J. Mol. Cell. Cardiol. 47: 819–827.
24. Palmer, J. W., B. Tandler, and C. L. Hoppel. 1977. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J. Biol. Chem. 252: 8731–8739.
25. Palmer, J. W., B. Tandler, and C. L. Hoppel. 1985. Biochemical differences between subsarcolemmal and interfibrillar mitochondria from rat cardiac muscle: effects of procedural manipulations. Arch. Biochem. Biophys. 236: 691–702.
26. Palmer, J. W., B. Tandler, and C. L. Hoppel. 1986. Heterogeneous response of subsarcolemmal heart mitochondria to calcium. Am. J. Physiol. 250: H741–H748.
27. Papanicolaou, K. N., G. A. Ngoh, E. R. Dabkowski, K. A. O’Connell, R. F. Ribeiro, W. C. Stanley, et al. 2012. Cardiomyocyte deletion of mitofusin-1 leads to mitochondrial fragmentation and improves tolerance to ROS-induced mitochondrial dysfunction and cell death. Am. J. Physiol. Heart Circ. Physiol. 302: H167–H179.
28. 2+ activation of PDH. Am. J. Physiol. 276: H149–H158
29. Rennison, J. H., T. A. McElfresh, I. C. Okere, E. J. Vazquez, H. V. Patel, A. B. Foster, et al. 2007. High-fat diet postinfarction enhances mitochondrial function and does not exacerbate left ventricular dysfunction. Am. J. Physiol. Heart Circ. Physiol. 292: H1498–H1506.
30. Rennison, J. H., T. A. McElfresh, I. C. Okere, H. V. Patel, A. B. Foster, K. K. Patel, et al. 2008. Enhanced acyl-CoA dehydrogenase activity is associated with improved mitochondrial and contractile function in heart failure. Cardiovasc. Res. 79: 331–340.
31. Riva, A., B. Tandler, F. Loffredo, E. Vazquez, and C. Hoppel. 2005. Structural differences in two biochemically defined populations of cardiac mitochondria. Am. J. Physiol. Heart Circ. Physiol. 289: H868–H872.
32. Shah, K. B., M. K. Duda, K. M. O’shea, G. C. Sparagna, D. J. Chess, R. J. Khairallah, et al. 2009. The cardioprotective effects of fish oil during pressure overload are blocked by high fat intake: role of cardiac phospholipid remodeling. Hypertension 54: 605–611.
33. Sharma, N., I. C. Okere, M. K. Duda, J. Johnson, C. L. Yuan, M. P. Chandler, et al. 2007. High fructose diet increases mortality in hypertensive rats compared to a complex carbohydrate or high fat diet. Am. J. Hypertens. 20: 403–409.
34. Sharma, N., I. C. Okere, B. R. Barrows, B. Lei, M. K. Duda, C. L. Yuan, et al. 2008. High-sugar diets increase cardiac dysfunction and mortality in hypertension compared to low-carbohydrate or high-starch diets. J. Hypertens. 26: 1402–1410.
35. Stanley, W. C., E. R. Dabkowski, R. F. Ribeiro Jr., and K. A. O’Connell. 2012. Dietary fat and heart failure: moving from lipotoxicity to lipoprotection. Circ. Res. 110: 764–776.
36. Zhou, L., M. E. Cabrera, H. Huang, C. L. Yuan, D. K. Monika, N. Sharma, et al. 2007. Parallel activation of mitochondrial oxidative metabolism with increased cardiac energy expenditure is not dependent on fatty acid oxidation in pigs. J. Physiol. 579: 811–821.