In obese Zucker rats, lipids accumulate in the heart despite normal mitochondrial content, morphology and long-chain fatty acid oxidation

Journal of Physiology

Volumn 589, Issue 1, 2011, Pages 169-180

  Holloway, Graham P ^a   Snook, Laelie A ^a   Harris, Robert J ^a   Glatz, Jan F C ^b   Luiken, Joost J F P ^b   Bonen, Arend ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; CARNITINE PALMITOYLTRANSFERASE I; CD36 ANTIGEN; CITRATE SYNTHASE; FAT DROPLET; FATTY ACID BINDING PROTEIN; LIPID; LONG CHAIN FATTY ACID; MULTIENZYME COMPLEX; PALMITIC ACID; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; BIOCHEMISTRY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ESTERIFICATION; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; FEMALE; HEART FAILURE; HEART MITOCHONDRION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE; ISOLATED HEART; LIPID STORAGE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; TRANSMISSION ELECTRON MICROSCOPY;

3-HYDROXYACYL COA DEHYDROGENASES; ANIMALS; ANTIGENS, CD36; BIOLOGICAL TRANSPORT; CARNITINE O-PALMITOYLTRANSFERASE; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ESTERIFICATION; FATTY ACID-BINDING PROTEINS; FATTY ACIDS; FEMALE; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, HEART; MYOCARDIUM; OBESITY; OXIDATION-REDUCTION; PALMITIC ACID; RATS; RATS, ZUCKER; SARCOLEMMA; TRIGLYCERIDES;

EID: 78650318083     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.198663     Document Type: Article

References (49)

1. Belke DD, Larsen TS, Gibbs EM and Severson DL (2000). Altered metabolism causes cardiac dysfunction in perfused hearts from diabetic (db/db) mice. Am J Physiol Endocrinol Metab 279, E1104-E1113.
2. Bergmeyer HU (1974). Methods of Enzymatic Analysis, vol. 4. Verlag Chemie Weinheim, New York.
3. Bonen A, Luiken JJ, Liu S, Dyck DJ, Kiens B, Kristiansen S, Turcotte LP, Van Der Vusse GJ and Glatz JF (1998). Palmitate transport and fatty acid transporters in red and white muscles. Am J Physiol Endocrinol Metab 275, E471-E478.
4. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, Vidal H and Rieusset J (2008). Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118, 789-800.
5. Bugger H, Boudina S, Hu XX, Tuinei J, Zaha VG, Theobald HA, Yun UJ, McQueen AP, Wayment B, Litwin SE and Abel ED (2008). Type 1 diabetic akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3. Diabetes 57, 2924-2932.
6. Bugger H, Chen D, Riehle C, Soto J, Theobald HA, Hu XX, Ganesan B, Weimer BC and Abel ED (2009). Tissue-specific remodeling of the mitochondrial proteome in type 1 diabetic akita mice. Diabetes 58, 1986-1997.
7. Chabowski A, Gorski J, Luiken JJ, Glatz JF and Bonen A (2007). Evidence for concerted action of FAT/CD36 and FABPpm to increase fatty acid transport across the plasma membrane. Prostaglandins Leukot Essent Fatty Acids 77, 345-353.
8. Chandler MP, Chavez PN, McElfresh TA, Huang H, Harmon CS and Stanley WC (2003). Partial inhibition of fatty acid oxidation increases regional contractile power and efficiency during demand-induced ischemia. Cardiovasc Res 59, 143-151.
9. Chen Q, Moghaddas S, Hoppel CL and Lesnefsky EJ (2008). Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. Am J Physiol Cell Physiol 294, C460-C466.
10. Cogswell AM, Stevens RJ and Hood DA (1993). Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264, C383-C389.
11. Coort SL, Hasselbaink DM, Koonen DP, Willems J, Coumans WA, Chabowski A, Van Der Vusse GJ, Bonen A, Glatz JF and Luiken JJ (2004). Enhanced sarcolemmal FAT/CD36 content and triacylglycerol storage in cardiac myocytes from obese zucker rats. Diabetes 53, 1655-1663.
12. Dabkowski ER, Williamson CL, Bukowski VC, Chapman RS, Leonard SS, Peer CJ, Callery PS and Hollander JM (2009). Diabetic cardiomyopathy-associated dysfunction in spatially distinct mitochondrial subpopulations. Am J Physiol Heart Circ Physiol 296, H359-H369.
13. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
14. Ferreira R, Vitorino R, Alves RM, Appell HJ, Powers SK, Duarte JA and Amado F (2010). Subsarcolemmal and intermyofibrillar mitochondria proteome differences disclose functional specializations in skeletal muscle. Proteomics 10, 3142-3154.
15. Fischer Y, Rose H and Kammermeier H (1991). Highly insulin-responsive isolated rat heart muscle cells yielded by a modified isolation method. Life Sci 49, 1679-1688.
16. Glatz JF, Jacobs AE and Veerkamp JH (1984). Fatty acid oxidation in human and rat heart. Comparison of cell-free and cellular systems. Biochim Biophys Acta 794, 454-465.
17. Hancock CR, Han DH, Chen M, Terada S, Yasuda T, Wright DC and Holloszy JO (2008). High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci U S A 105, 7815-7820.
18. Holloway GP, Benton C, Mullen KL, Yoshida Y, Snook LA, Han XX, Glatz JF, Luiken JJ, Lally J, Dyck DJ and Bonen A (2009). In obese rat muscle transport of palmitate is increased and is channeled to triacylglycerol storage despite an increase in mitochondrial palmitate oxidation. Am J Physiol Endocrinol Metab 296, E738-E747.
19. Holloway GP, Gurd BJ, Snook LA, Lally J and Bonen A (2010). Compensatory increases in nuclear PGC1a protein are primarily associated with subsarcolemmal mitochondrial adaptations in ZDF rats. Diabetes 59, 819-828.
20. Hoppel CL, Moghaddas S and Lesnefsky EJ (2002). Interfibrillar cardiac mitochondrial comples III defects in the aging rat heart. Biogerontology 3, 41-44.
21. Hoppeler H (1986). Exercise-induced ultrastructural changes in skeletal muscle. Int J Sports Med 7, 187-204.
22. Jain SS, Chabowski A, Snook LA, Schwenk RW, Glatz JF, Luiken JJ and Bonen A (2009). Additive effects of insulin and muscle contraction on fatty acid transport and fatty acid transporters, FAT/CD36, FABPpm, FATP1, 4 and 6. FEBS Lett 583, 2294-2300.
23. Kelley DE, He J, Menshikova EV and Ritov VB (2002). Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51, 2944-2950.
24. Koonen DP, Benton CR, Arumugam Y, Tandon NN, Calles-Escandon J, Glatz JF, Luiken JJ and Bonen A (2004). Different mechanisms can alter fatty acid transport when muscle contractile activity is chronically altered. Am J Physiol Endocrinol Metab 286, E1042-E1049.
25. Koonen DP, Coumans WA, Arumugam Y, Bonen A, Glatz JF and Luiken JJ (2002). Giant membrane vesicles as a model to study cellular substrate uptake dissected from metabolism. Mol Cell Biochem 239, 121-130.
26. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD and Muoio DM (2008). Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7, 45-56.
27. Kraegen EW, Cooney GJ and Turner N (2008). Muscle insulin resistance: a case of fat overconsumption, not mitochondrial dysfunction. Proc Natl Acad Sci U S A 105, 7627-7628.
28. Lesnefsky EJ, Slabe TJ, Stoll MS, Minkler PE and Hoppel CL (2001). Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am J Physiol Heart Circ Physiol 280, H2770-H2778.
29. Luiken JJ, Arumugam Y, Dyck DJ, Bell RC, Pelsers MM, Turcotte LP, Tandon NN, Glatz JF and Bonen A (2001). Increased rates of fatty acid uptake and plasmalemmal fatty acid transporters in obese Zucker rats. J Biol Chem 276, 40567-40573.
30. Luiken JJ, Coort SL, Willems J, Coumans WA, Bonen A, Van Der Vusse GJ and Glatz JF (2003). Contraction-induced fatty acid translocase/CD36 translocation in rat cardiac myocytes is mediated through AMP-activated protein kinase signaling. Diabetes 52, 1627-1634.
31. Luiken JJ, Koonen DP, Willems J, Zorzano A, Becker C, Fischer Y, Tandon NN, Van Der Vusse GJ, Bonen A and Glatz JF (2002). Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes 51, 3113-3119.
32. Luiken JJ, Niessen HE, Coort SL, Hoebers N, Coumans WA, Schwenk RW, Bonen A and Glatz JF (2009). Etomoxir-induced partial carnitine palmitoyltransferase-I (CPT-I) inhibition in vivo does not alter cardiac long-chain fatty acid uptake and oxidation rates. Biochem J 419, 447-455.
33. Luiken JJ, Schaap FG, van Nieuwenhoven FA, Van Der Vusse GJ, Bonen A and Glatz JF (1999). Cellular fatty acid transport in heart and skeletal muscle as facilitated by proteins. Lipids 34, S169-S175.
34. Luiken JJ, van Nieuwenhoven FA, America G, Van Der Vusse GJ and Glatz JF (1997). Uptake and metabolism of palmitate by isolated cardiac myocytes from adult rats: involvement of sarcolemmal proteins. J Lipid Res 38, 745-758.
35. McGarry JD, Mills SE, Long CS and Foster DW (1983). Observations on the affinity for carnitine, and malonyl-CoA sensitivity, of carnitine palmitoyltransferase I in animal and human tissues. Demonstration of the presence of malonyl-CoA in non-hepatic tissues of the rat. Biochem J 214, 21-28.
36. Marchand I, Tarnopolsky M, Adamo KB, Bourgeois JM, Chorneyko K and Graham TE (2007). Quantitative assessment of human muscle glycogen granules size and number in subcellular locations during recovery from prolonged exercise. J Physiol 580, 617-628.
37. Marfella R, Di Filippo C, Portoghese M, Barbieri M, Ferraraccio F, Siniscalchi M, Cacciapuoti F, Rossi F, D'Amico M and Paolisso G (2009). Myocardial lipid accumulation in patients with pressure-overloaded heart and metabolic syndrome. J Lipid Res 50, 2314-2323.
38. Mazumder PK, O'Neill BT, Roberts MW, Buchanan J, Yun UJ, Cooksey RC, Boudina S and Abel ED (2004). Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes 53, 2366-2374.
39. Neitzel AS, Carley AN and Severson DL (2003). Chylomicron and palmitate metabolism by perfused hearts from diabetic mice. Am J Physiol Endocrinol Metab 284, E357-E365.
40. Palmer JW, Tandler B and Hoppel CL (1985). Biochemical differences between subsarcolemmal and interfibrillar mitochondria from rat cardiac muscle: effects of procedural manipulations. Arch Biochem Biophys 236, 691-702.
41. Sharma S, Adrogue JV, Golfman L, Uray I, Lemm J, Youker K, Noon GP, Frazier OH and Taegtmeyer H (2004). Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. FASEB J 18, 1692-1700.
42. Srere PA (1969). Citrate synthase. In Methods in Enzymology. Academid, New York.
43. Stanley WC, Recchia FA and Lopaschuk GD (2005). Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 85, 1093-1129.
44. Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC and Hamadeh MJ (2007). Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. Am J Physiol Regul Integr Comp Physiol 292, R1271-R1278.
45. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS and Cooney GJ (2007). Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56, 2085-2092.
46. Ussher JR, Koves TR, Jaswal JS, Zhang L, Ilkayeva O, Dyck JR, Muoio DM and Lopaschuk GD (2009). Insulin-stimulated cardiac glucose oxidation is increased in high-fat diet-induced obese mice lacking malonyl CoA decarboxylase. Diabetes 58, 1766-1775.
47. Van Der Meer RW, Rijzewijk LJ, de Jong HW, Lamb HJ, Lubberink M, Romijn JA, Bax JJ, de Roos A, Kamp O, Paulus WJ, Heine RJ, Lammertsma AA, Smit JW and Diamant M (2009). Pioglitazone improves cardiac function and alters myocardial substrate metabolism without affecting cardiac triglyceride accumulation and high-energy phosphate metabolism in patients with well-controlled type 2 diabetes mellitus. Circulation 119, 2069-2077.
48. Wang P, Lloyd SG, Zeng H, Bonen A and Chatham JC (2005). Impact of altered substrate utilization on cardiac function in isolated hearts from Zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol 288, H2102-H2110.
49. Wisneski JA, Gertz EW, Neese RA and Mayr M (1987). Myocardial metabolism of free fatty acids. Studies with 14C-labeled substrates in humans. J Clin Invest 79, 359-366.