Cardiomyocyte-specific ablation of CD36 improves post-ischemic functional recovery

Journal of Molecular and Cellular Cardiology

Volumn 63, Issue , 2013, Pages 180-188

  Nagendran, Jeevan ^a   Pulinilkunnil, Thomas ^a   Kienesberger, Petra C ^a   Sung, Miranda M ^a   Fung, David ^a   Febbraio, Maria ^a   Dyck, Jason R B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Efficiency; Ischemia and reperfusion; Lipids; Metabolism

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD36 ANTIGEN; CRE RECOMBINASE; FATTY ACID; GENOMIC DNA; GLUCOSE; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; EX VIVO STUDY; EXON; FATTY ACID OXIDATION; FEMALE; GLUCOSE OXIDATION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PERFUSION; HEART WORK; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; TRIACYLGLYCEROL BLOOD LEVEL;

EFFICIENCY; ISCHEMIA AND REPERFUSION; LIPIDS; METABOLISM;

ANIMALS; ANTIGENS, CD36; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; FATTY ACIDS; GENE ORDER; GENE TARGETING; HOMOLOGOUS RECOMBINATION; MALE; MICE; MICE, KNOCKOUT; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC;

EID: 84884760130     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.07.020     Document Type: Article

References (46)

1. Frank A., Bonney M., Bonney S., Weitzel L., Koeppen M., Eckle T. Myocardial ischemia reperfusion injury: from basic science to clinical bedside. Semin Cardiothorac Vasc Anesth 2012, 16:123-132.
2. Jaswal J.S., Keung W., Wang W., Ussher J.R., Lopaschuk G.D. Targeting fatty acid and carbohydrate oxidation-a novel therapeutic intervention in the ischemic and failing heart. Biochim Biophys Acta 1813, 2011:1333-1350.
3. Heather L.C., Cole M.A., Lygate C.A., Evans R.D., Stuckey D.J., Murray A.J., et al. Fatty acid transporter levels and palmitate oxidation rate correlate with ejection fraction in the infarcted rat heart. Cardiovasc Res 2006, 72:430-437.
4. Lopaschuk G.D., Ussher J.R., Folmes C.D., Jaswal J.S., Stanley W.C. Myocardial fatty acid metabolism in health and disease. Physiol Rev 2010, 90:207-258.
5. Lopaschuk G.D., Barr R., Thomas P.D., Dyck J.R. Beneficial effects of trimetazidine in ex vivo working ischemic hearts are due to a stimulation of glucose oxidation secondary to inhibition of long-chain 3-ketoacyl coenzyme a thiolase. Circ Res 2003, 93:e33-e37.
6. Fragasso G., Salerno A., Lattuada G., Cuko A., Calori G., Scollo A., et al. Effect of partial inhibition of fatty acid oxidation by trimetazidine on whole body energy metabolism in patients with chronic heart failure. Heart 2011, 97:1495-1500.
7. McCormack J.G., Barr R.L., Wolff A.A., Lopaschuk G.D. Ranolazine stimulates glucose oxidation in normoxic, ischemic, and reperfused ischemic rat hearts. Circulation 1996, 93:135-142.
8. McCormack J.G., Stanley W.C., Wolff A.A. Ranolazine: a novel metabolic modulator for the treatment of angina. Gen Pharmacol 1998, 30:639-645.
9. Sabbah H.N., Chandler M.P., Mishima T., Suzuki G., Chaudhry P., Nass O., et al. Ranolazine, a partial fatty acid oxidation (pFOX) inhibitor, improves left ventricular function in dogs with chronic heart failure. J Card Fail 2002, 8:416-422.
10. Chandler M.P., Stanley W.C., Morita H., Suzuki G., Roth B.A., Blackburn B., et al. Short-term treatment with ranolazine improves mechanical efficiency in dogs with chronic heart failure. Circ Res 2002, 91:278-280.
11. Fragasso G., Piatti Md P.M., Monti L., Palloshi A., Setola E., Puccetti P., et al. Short- and long-term beneficial effects of trimetazidine in patients with diabetes and ischemic cardiomyopathy. Am Heart J 2003, 146:E18.
12. Sossalla S., Wagner S., Rasenack E.C., Ruff H., Weber S.L., Schondube F.A., et al. Ranolazine improves diastolic dysfunction in isolated myocardium from failing human hearts-role of late sodium current and intracellular ion accumulation. J Mol Cell Cardiol 2008, 45:32-43.
13. Macinnes A., Fairman D.A., Binding P., Rhodes J., Wyatt M.J., Phelan A., et al. The antianginal agent trimetazidine does not exert its functional benefit via inhibition of mitochondrial long-chain 3-ketoacyl coenzyme A thiolase. Circ Res 2003, 93:e26-e32.
14. Hale S.L., Shryock J.C., Belardinelli L., Sweeney M., Kloner R.A. Late sodium current inhibition as a new cardioprotective approach. J Mol Cell Cardiol 2008, 44:954-967.
15. Rowe G.C., Jiang A., Arany Z. PGC-1 coactivators in cardiac development and disease. Circ Res 2010, 107:825-838.
16. Cheng L., Ding G., Qin Q., Huang Y., Lewis W., He N., et al. Cardiomyocyte-restricted peroxisome proliferator-activated receptor-delta deletion perturbs myocardial fatty acid oxidation and leads to cardiomyopathy. Nat Med 2004, 10:1245-1250.
17. Febbraio M., Abumrad N.A., Hajjar D.P., Sharma K., Cheng W., Pearce S.F., et al. A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J Biol Chem 1999, 274:19055-19062.
18. Brinkmann J.F., Abumrad N.A., Ibrahimi A., Van Der Vusse G.J., Glatz J.F. New insights into long-chain fatty acid uptake by heart muscle: a crucial role for fatty acid translocase/CD36. Biochem J 2002, 367:561-570.
19. Ibrahimi A., Bonen A., Blinn W.D., Hajri T., Li X., Zhong K., et al. Muscle-specific overexpression of FAT/CD36 enhances fatty acid oxidation by contracting muscle, reduces plasma triglycerides and fatty acids, and increases plasma glucose and insulin. J Biol Chem 1999, 274:26761-26766.
20. Webb T., Whittington J., Holland A.J., Soni S., Boer H., Clarke D., et al. CD36 expression and its relationship with obesity in blood cells from people with and without Prader-Willi syndrome. Clin Genet 2006, 69:26-32.
21. Kuang M., Febbraio M., Wagg C., Lopaschuk G.D., Dyck J.R. Fatty acid translocase/CD36 deficiency does not energetically or functionally compromise hearts before or after ischemia. Circulation 2004, 109:1550-1557.
22. Irie H., Krukenkamp I.B., Brinkmann J.F., Gaudette G.R., Saltman A.E., Jou W., et al. Myocardial recovery from ischemia is impaired in CD36-null mice and restored by myocyte CD36 expression or medium-chain fatty acids. Proc Natl Acad Sci U S A 2003, 100:6819-6824.
23. Silverstein R.L., Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2009, 2:re3.
24. Glatz J.F., Luiken J.J., Bonen A. Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev 2010, 90:367-441.
25. Bessi V.L., Labbe S.M., Huynh D.N., Menard L., Jossart C., Febbraio M., et al. EP 80317, a selective CD36 ligand, shows cardioprotective effects against post-ischaemic myocardial damage in mice. Cardiovasc Res 2012, 96:99-108.
26. Kienesberger P.C., Pulinilkunnil T., Sung M.M., Nagendran J., Haemmerle G., Kershaw E.E., et al. Myocardial ATGL overexpression decreases the reliance on fatty acid oxidation and protects against pressure overload-induced cardiac dysfunction. Mol Cell Biol 2012, 32:740-745.
27. Sung M.M., Koonen D.P., Soltys C.L., Jacobs R.L., Febbraio M., Dyck J.R. Increased CD36 expression in middle-aged mice contributes to obesity-related cardiac hypertrophy in the absence of cardiac dysfunction. J Mol Med (Berl) 2011, 89:459-466.
28. Imahashi K., Mraiche F., Steenbergen C., Murphy E., Fliegel L. Overexpression of the Na+/H+exchanger and ischemia-reperfusion injury in the myocardium. Am J Physiol Heart Circ Physiol 2007, 292:H2237-H2247.
29. Pulinilkunnil T., Kienesberger P.C., Nagendran J., Waller T.J., Young M.E., Kershaw E.E., et al. Myocardial adipose triglyceride lipase overexpression protects diabetic mice from the development of lipotoxic cardiomyopathy. Diabetes 2013, 62(5):1464-1477.
30. Bodart V., Febbraio M., Demers A., Mcnicoll N., Pohankova P., Perreault A., et al. CD36 mediates the cardiovascular action of growth hormone-releasing peptides in the heart. Circ Res 2002, 90:844-849.
31. Gimeno R.E., Ortegon A.M., Patel S., Punreddy S., Ge P., Sun Y., et al. Characterization of a heart-specific fatty acid transport protein. J Biol Chem 2003, 278:16039-16044.
32. Ellis J.M., Mentock S.M., Depetrillo M.A., Koves T.R., Sen S., Watkins S.M., et al. Mouse cardiac acyl coenzyme a synthetase 1 deficiency impairs fatty acid oxidation and induces cardiac hypertrophy. Mol Cell Biol 2011, 31:1252-1256.
33. Randle P.J., Garland P.B., Hales C.N., Newsholme E.A. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1963, 1:785-789.
34. Randle P.J., Garland P.B., Newsholme E.A., Hales C.N. The glucose fatty acid cycle in obesity and maturity onset diabetes mellitus. Ann N Y Acad Sci 1965, 131:324-333.
35. Angin Y., Steinbusch L.K., Simons P.J., Greulich S., Hoebers N.T., Douma K., et al. CD36 inhibition prevents lipid accumulation and contractile dysfunction in rat cardiomyocytes. Biochem J 2012, 448:43-45.
36. Koonen D.P., Febbraio M., Bonnet S., Nagendran J., Young M.E., Michelakis E.D., et al. CD36 expression contributes to age-induced cardiomyopathy in mice. Circulation 2007, 116:2139-2147.
37. Ussher J.R., Wang W., Gandhi M., Keung W., Samokhvalov V., Oka T., et al. Stimulation of glucose oxidation protects against acute myocardial infarction and reperfusion injury. Cardiovasc Res 2012, 94:359-366.
38. Dyck J.R., Cheng J.F., Stanley W.C., Barr R., Chandler M.P., Brown S., et al. Malonyl coenzyme a decarboxylase inhibition protects the ischemic heart by inhibiting fatty acid oxidation and stimulating glucose oxidation. Circ Res 2004, 94:e78-e84.
39. Sung M.M., Soltys C.L., Masson G., Boisvenue J.J., Dyck J.R. Improved cardiac metabolism and activation of the RISK pathway contributes to improved post-ischemic recovery in calorie restricted mice. J Mol Med (Berl) 2011, 89:291-302.
40. Liu Q., Docherty J.C., Rendell J.C., Clanachan A.S., Lopaschuk G.D. High levels of fatty acids delay the recovery of intracellular pH and cardiac efficiency in post-ischemic hearts by inhibiting glucose oxidation. J Am Coll Cardiol 2002, 39:718-725.
41. Liu B., Clanachan A.S., Schulz R., Lopaschuk G.D. Cardiac efficiency is improved after ischemia by altering both the source and fate of protons. Circ Res 1996, 79:940-948.
42. Azizi Y., Faghihi M., Imani A., Roghani M., Nazari A. Post-infarct treatment with [Pyr1]-apelin-13 reduces myocardial damage through reduction of oxidative injury and nitric oxide enhancement in the rat model of myocardial infarction. Peptides 2013, 46:76-82.
43. Yang J., Sambandam N., Han X., Gross R.W., Courtois M., Kovacs A., et al. CD36 deficiency rescues lipotoxic cardiomyopathy. Circ Res 2007, 100:1208-1217.
44. Dyck J.R., Hopkins T.A., Bonnet S., Michelakis E.D., Young M.E., Watanabe M., et al. Absence of malonyl coenzyme A decarboxylase in mice increases cardiac glucose oxidation and protects the heart from ischemic injury. Circulation 2006, 114:1721-1728.
45. Zhou L., Huang H., McElfresh T.A., Prosdocimo D.A., Stanley W.C. Impact of anaerobic glycolysis and oxidative substrate selection on contractile function and mechanical efficiency during moderate severity ischemia. Am J Physiol Heart Circ Physiol 2008, 295:H939-H945.
46. Folmes C.D., Sowah D., Clanachan A.S., Lopaschuk G.D. High rates of residual fatty acid oxidation during mild ischemia decrease cardiac work and efficiency. J Mol Cell Cardiol 2009, 47:142-148.