Enhancement of muscle mitochondrial oxidative capacity and alterations in insulin action are lipid species dependent: Potent tissue-specific effects of medium-chain fatty acids

Diabetes

Volumn 58, Issue 11, 2009, Pages 2547-2554

  Turner, Nigel ^a,b   Hariharan, Krit ^a   TidAng, Jennifer ^a   Frangioudakis, Georgia ^a   Beale, Susan M ^a   Wright, Lauren E ^a   Zeng, Xiao Yi ^a   Leslie, Simon J ^a   Li, Jing Ya ^a,c   Kraegen, Edward W ^a,b   Cooney, Gregory J ^a,b   Ye, Ji Ming ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; GLUCOSE; INSULIN; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GLUCOSE TOLERANCE; INSULIN RESISTANCE; LIPID METABOLISM; LIPOGENESIS; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RAT;

ADIPOSE TISSUE; ANIMALS; BODY COMPOSITION; BODY WEIGHT; DIET, FAT-RESTRICTED; DIETARY FATS; ENERGY METABOLISM; FATTY ACIDS; FATTY ACIDS, NONESTERIFIED; GLUCOSE; INSULIN; INSULIN RESISTANCE; MICE; MICE, INBRED C57BL; MITOCHONDRIA, MUSCLE; ORGAN SIZE; OXIDATION-REDUCTION; RATS; RATS, WISTAR; TRIGLYCERIDES;

EID: 70350539537     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0784     Document Type: Article

References (48)

1. Savage DB, Petersen KF, Shulman GI. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 2007;87:507-520
2. Kraegen EW, Cooney GJ. Free fatty acids and skeletal muscle insulin resistance. Curr Opin Lipidol 2008;19:235-241
3. Turner N, Heilbronn LK. Is mitochondrial dysfunction a cause of insulin resistance? Trends Endocrinol Metab 2008;19:324-330
4. Storlien LH, Jenkins AB, Chisholm DJ, Pascoe WS, Khouri S, Kraegen EW. 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 1991;40:280-289
5. Park SY, Cho YR, Kim HJ, Higashimori T, Danton C, Lee MK, Dey A, Rothermel B, Kim YB, Kalinowski A, Russell KS, Kim JK. Unraveling the temporal pattern of diet-induced insulin resistance in individual organs and cardiac dysfunction in C57BL/6 mice. Diabetes 2005;54:3530-3540
6. Oakes ND, Cooney GJ, Camilleri S, Chisholm DJ, Kraegen EW. Mechanisms of liver and muscle insulin resistance induced by chronic high-fat feeding. Diabetes 1997;46:1768-1774 (Pubitemid 27456409)
7. Dobbins RL, Szczepaniak LS, Bentley B, Esser V, Myhill J, McGarry JD. Prolonged inhibition of muscle carnitine palmitoyltransferase-1 promotes intramyocellular lipid accumulation and insulin resistance in rats. Diabetes 2001;50:123-130 (Pubitemid 32047990)
8. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS, Cooney GJ. 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 2007;56:2085-2092 (Pubitemid 47195821)
9. Hancock CR, Han DH, Chen M, Terada S, Yasuda T, Wright DC, Holloszy JO. High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci U S A 2008;105:7815-7820 (Pubitemid 351872721)
10. Bruce CR, Hoy AJ, Turner N, Watt MJ, Allen TL, Carpenter K, Cooney GJ, Febbraio MA, Kraegen EW. Overexpression of carnitine palmitoyltransferase- 1 in skeletal muscle is sufficient to enhance fatty acid oxidation and improve high-fat diet-induced insulin resistance. Diabetes 2009;58:550-558
11. Buettner R, Parhofer KG, Woenckhaus M, Wrede CE, Kunz-Schughart LA, Scholmerich J, Bollheimer LC. Defining high-fat-diet rat models: metabolic and molecular effects of different fat types. J Mol Endocrinol 2006;36:485-501 (Pubitemid 43904942)
12. St-Onge MP. Dietary fats, teas, dairy, and nuts: potential functional foods for weight control? Am J Clin Nutr 2005;81:7-15
13. Papamandjaris AA, MacDougall DE, Jones PJ. Medium chain fatty acid metabolism and energy expenditure: obesity treatment implications. Life Sci 1998;62:1203-1215
14. St-Onge MP, Bourque C, Jones PJ, Ross R, Parsons WE. Medium-versus long-chain triglycerides for 27 days increases fat oxidation and energy expenditure without resulting in changes in body composition in overweight women. Int J Obes Relat Metab Disord 2003;27:95-102
15. St-Onge MP, Ross R, Parsons WD, Jones PJ. Medium-chain triglycerides increase energy expenditure and decrease adiposity in overweight men. Obes Res 2003;11:395-402 (Pubitemid 41151627)
16. Baba N, Bracco EF, Hashim SA. Enhanced thermogenesis and diminished deposition of fat in response to overfeeding with diet containing medium chain triglyceride. Am J Clin Nutr 1982;35:678-682
17. Shinohara H, Ogawa A, Kasai M, Aoyama T. Effect of randomly interesterified triacylglycerols containing medium- and long-chain fatty acids on energy expenditure and hepatic fatty acid metabolism in rats. Biosci Biotechnol Biochem 2005;69:1811-1818
18. Han J, Hamilton JA, Kirkland JL, Corkey BE, Guo W. Medium-chain oil reduces fat mass and down-regulates expression of adipogenic genes in rats. Obes Res 2003;11:734-744 (Pubitemid 41151599)
19. Takeuchi H, Noguchi O, Sekine S, Kobayashi A, Aoyama T. Lower weight gain and higher expression and blood levels of adiponectin in rats fed medium-chain TAG compared with long-chain TAG. Lipids 2006;41:207-212
20. Eckel RH, Hanson AS, Chen AY, Berman JN, Yost TJ, Brass EP. Dietary substitution of medium-chain triglycerides improves insulin-mediated glucose metabolism in NIDDM subjects. Diabetes 1992;41:641-647
21. Han JR, Deng B, Sun J, Chen CG, Corkey BE, Kirkland JL, Ma J, Guo W. Effects of dietary medium-chain triglyceride on weight loss and insulin sensitivity in a group of moderately overweight free-living type 2 diabetic Chinese subjects. Metabolism 2007;56:985-991
22. Ye JM, Iglesias MA, Watson DG, Ellis B, Wood L, Jensen PB, Sorensen RV, Larsen PJ, Cooney GJ, Wassermann K, Kraegen EW. PPARalpha/gamma ragaglitazar eliminates fatty liver and enhances insulin action in fat-fed rats in the absence of hepatomegaly. Am J Physiol Endocrinol Metab 2003;284:E531-E540 (Pubitemid 36237541)
23. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 1957;226:497-509
24. Lepage G, Roy CC. Direct transesterification of all classes of lipids in a one-step reaction. J Lipid Res 1986;27:114-120 (Pubitemid 16045295)
25. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP. The effect of insulin on the disposal of intravenous glucose: results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 1981;30:1000-1007
26. Levak-Frank S, Radner H, Walsh A, Stollberger R, Knipping G, Hoefler G, Sattler W, Weinstock PH, Breslow JL, Zechner R. Muscle-specific overexpression of lipoprotein lipase causes a severe myopathy characterized by proliferation of mitochondria and peroxisomes in transgenic mice. J Clin Invest 1995;96:976-986
27. Garcia-Roves P, Huss JM, Han DH, Hancock CR, Iglesias-Gutierrez E, Chen M, Holloszy JO. Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle. Proc Natl Acad Sci U S A 2007;104:10709-10713
28. Hegarty BD, Cooney GJ, Kraegen EW, Furler SM. Increased efficiency of fatty acid uptake contributes to lipid accumulation in skeletal muscle of high-fat-fed insulin-resistant rats. Diabetes 2002;51:1477-1484
29. Evans RM, Barish GD, Wang YX. PPARs and the complex journey to obesity. Nat Med 2004;10:355-361
30. Forman BM, Chen J, Evans RM. Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc Natl Acad Sci U S A 1997;94:4312-4317
31. Xu HE, Lambert MH, Montana VG, Parks DJ, Blanchard SG, Brown PJ, Sternbach DD, Lehmann JM, Wisely GB, Willson TM, Kliewer SA, Milburn MV. Molecular recognition of fatty acids by peroxisome proliferator-activated receptors. Mol Cell 1999;3:397-403
32. Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, Puigserver P. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 2007;26:1913-1923 (Pubitemid 46624046)
33. Guillot E, Vaugelade P, Lemarchal P, Rerat A. Intestinal absorption and liver uptake of medium-chain fatty acids in non-anaesthetized pigs. Br J Nutr 1993;69:431-442 (Pubitemid 23105481)
34. Friedman MI, Ramirez I, Bowden CR, Tordoff MG. Fuel partitioning and food intake: role for mitochondrial fatty acid transport. Am J Physiol 1990;258:R216-R221
35. Franck N, Stenkula KG, Ost A, Lindstrom T, Stralfors P, Nystrom FH. Insulin-induced GLUT4 translocation to the plasma membrane is blunted in large compared with small primary fat cells isolated from the same individual. Diabetologia 2007;50:1716-1722 (Pubitemid 47036658)
36. Salans LB, Dougherty JW. The effect of insulin upon glucose metabolism by adipose cells of different size: influence of cell lipid and protein content, age, and nutritional state. J Clin Invest 1971;50:1399-1410
37. Geliebter A, Torbay N, Bracco EF, Hashim SA, Van Itallie TB. Overfeeding with medium-chain triglyceride diet results in diminished deposition of fat. Am J Clin Nutr 1983;37:1-4 (Pubitemid 13155490)
38. Dias VC, Fung E, Snyder FF, Carter RJ, Parsons HG. Effects of medium-chain triglyceride feeding on energy balance in adult humans. Metabolism 1990;39:887-891 (Pubitemid 20293931)
39. Chanez M, Bois-Joyeux B, Arnaud MJ, Peret J. Metabolic effects in rats of a diet with a moderate level of medium-chain triglycerides. J Nutr 1991;121:585-594
40. Geelen MJ, Schoots WJ, Bijleveld C, Beynen AC. Dietary medium-chain fatty acids raise and (n-3) polyunsaturated fatty acids lower hepatic triacylglycerol synthesis in rats. J Nutr 1995;125:2449-2456
41. Lieber CS, DeCarli LM, Leo MA, Mak KM, Ponomarenko A, Ren C, Wang X. Beneficial effects versus toxicity of medium-chain triacylglycerols in rats with NASH. J Hepatol 2008;48:318-326
42. Baldermann H, Wicklmayr M, Rett K, Banholzer P, Dietze G, Mehnert H. Changes of hepatic morphology during parenteral nutrition with lipid emulsions containing LCT or MCT/LCT quantified by ultrasound. JPEN J Parenter Enteral Nutr 1991;15:601-603
43. Nosaka N, Kasai M, Nakamura M, Takahashi I, Itakura M, Takeuchi H, Aoyama T, Tsuji H, Okazaki M, Kondo K. Effects of dietary medium-chain triacylglycerols on serum lipoproteins and biochemical parameters in healthy men. Biosci Biotechnol Biochem 2002;66:1713-1718 (Pubitemid 39246830)
44. Hill JO, Peters JC, Swift LL, Yang D, Sharp T, Abumrad N, Greene HL. Changes in blood lipids during six days of overfeeding with medium or long chain triglycerides. J Lipid Res 1990;31:407-416
45. Swift LL, Hill JO, Peters JC, Greene HL. Plasma lipids and lipoproteins during 6 d of maintenance feeding with long-chain, medium-chain, and mixed-chain triglycerides. Am J Clin Nutr 1992;56:881-886
46. Tsuji H, Kasai M, Takeuchi H, Nakamura M, Okazaki M, Kondo K. Dietary medium-chain triacylglycerols suppress accumulation of body fat in a double-blind, controlled trial in healthy men and women. J Nutr 2001;131:2853-2859 (Pubitemid 33063114)
47. St-Onge MP, Bosarge A. Weight-loss diet that includes consumption of medium-chain triacylglycerol oil leads to a greater rate of weight and fat mass loss than does olive oil. Am J Clin Nutr 2008;87:621-626
48. Natali A, Ferrannini E. Effects of metformin and thiazolidinediones on suppression of hepatic glucose production and stimulation of glucose uptake in type 2 diabetes: a systematic review. Diabetologia 2006;49:434-441 (Pubitemid 43277865)