Lipid partitioning, incomplete fatty acid oxidation, and insulin signal transduction in primary human muscle cells: Effects of severe obesity, fatty acid incubation, and fatty acid translocase/CD36 overexpression

Journal of Clinical Endocrinology and Metabolism

Volumn 95, Issue 7, 2010, Pages 3400-3410

  Bell, Jill A ^a   Reed, Melissa A ^b   Consitt, Leslie A ^b   Martin, Ola J ^c   Haynie, Kimberly R ^d   Hulver, Matthew W ^d   Muoio, Deborah M ^c   Dohm, G Lynis ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; FATTY ACID TRANSPORTER; INSULIN; FATTY ACID;

ADULT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ESTERIFICATION; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LEAN BODY WEIGHT; LIPID ANALYSIS; LIPID METABOLISM; LIPID STORAGE; MUSCLE CELL; OBESITY; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION; ANALYSIS OF VARIANCE; GENETICS; INSULIN RESISTANCE; METABOLISM; MORBID OBESITY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADULT; ANALYSIS OF VARIANCE; ANTIGENS, CD36; BLOTTING, WESTERN; CELLS, CULTURED; FATTY ACID TRANSPORT PROTEINS; FATTY ACIDS; FEMALE; HUMANS; INSULIN; INSULIN RESISTANCE; MUSCLE FIBERS, SKELETAL; OBESITY, MORBID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 77954905826     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2009-1596     Document Type: Article

References (39)

1. Nielsen S, Guo Z, Johnson CM, Hensrud DD, Jensen MD 2004 Splanchnic lipolysis in human obesity [see comment]. J Clin Invest 113:1582-1588
2. Vice E, Privette JD, Hickner RC, Barakat HA 2005 Ketone body metabolism in lean and obese women. Metabolism 54:1542-1545 (Pubitemid 41527027)
3. Goodpaster BH, Theriault R, Watkins SC, Kelley DE 2000 Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 49:467-472 (Pubitemid 30196572)
4. Kelley DE, Goodpaster B, Wing RR, Simoneau JA 1999 Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 277:E1130-E1141 (Pubitemid 30046009)
5. Mandarino LJ, Consoli A, Jain A, Kelley DE 1996 Interaction of carbohydrate and fat fuels in human skeletal muscle: impact of obesity and NIDDM. Am J Physiol 270:E463-E470 (Pubitemid 126756376)
6. Boden G, Lebed B, Schatz M, Homko C, Lemieux S 2001 Effects of acute changes of plasma free fatty acids on intramyocellular fat content and insulin resistance in healthy subjects. Diabetes 50:1612-1617 (Pubitemid 33639602)
7. Cooney GJ, Thompson AL, Furler SM, Ye J, Kraegen EW 2002 Muscle long-chain acyl CoA esters and insulin resistance. Ann NY Acad Sci 967:196-207 (Pubitemid 34721906)
8. Kelley DE, Goodpaster BH 2001 Skeletal muscle triglyceride. An aspect of regional adiposity and insulin resistance. Diabetes Care 24:933-941
9. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, Storlien LH 1997 Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46:983-988 (Pubitemid 27220998)
10. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM 2008 Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7:45-56
11. Luiken JJ, Arumugam Y, Dyck DJ, Bell RC, Pelsers MM, Turcotte LP, Tandon NN, Glatz JF, Bonen A 2001 Increased rates of fatty acid uptake and plasmalemmal fatty acid transporters in obese Zucker rats. J Biol Chem 276:40567-40573 (Pubitemid 37373196)
12. Bonen A, Parolin ML, Steinberg GR, Calles-Escandon J, Tandon NN, Glatz JF, Luiken JJ, Heigenhauser GJ, Dyck DJ 2004 Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36. FASEB J 18:1144-1146 (Pubitemid 39561551)
13. García-Martínez C, Marotta M, Moore-Carrasco R, Guitart M, Camps M, Busquets S, Montell E, Gómez-Foix AM 2005 Impact on fatty acid metabolism and differential localization of FATP1 and FAT/CD36 proteins delivered in cultured human muscle cells. Am J Physiol Cell Physiol 288:C1264-C1272
14. Ibrahimi A, Bonen A, Blinn WD, Hajri T, Li X, Zhong K, Cameron R, Abumrad NA 1999 Muscle-specific over-expression 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 274:26761-26766 (Pubitemid 129520192)
15. Coburn CT, Knapp Jr FF, Febbraio M, Beets AL, Silverstein RL, Abumrad NA 2000 Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J Biol Chem 275:32523-32529
16. Febbraio M, Abumrad NA, Hajjar DP, Sharma K, Cheng W, Pearce SF, Silverstein RL 1999 A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J BiolChem 274:19055-19062 (Pubitemid 129519326)
17. Goudriaan JR, Dahlmans VE, Teusink B, Ouwens DM, Febbraio M, Maassen JA, Romijn JA, Havekes LM, Voshol PJ 2003 CD36 deficiency increases insulin sensitivity in muscle, but induces insulin resistance in the liver in mice. J Lipid Res 44:2270-2277 (Pubitemid 38082485)
18. McGarry JD 2002 Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51:7-18
19. Perseghin G, Petersen K, Shulman GI 2003 Cellular mechanism of insulin resistance: potential links with inflammation. Int J Obes Relat Metab Disord 27(Suppl 3):S6-S11 (Pubitemid 38019180)
20. Muoio DM, Way JM, Tanner CJ, Winegar DA, Kliewer SA, Houmard JA, Kraus WE, Dohm GL 2002 Peroxisome proliferator-activated receptor-α regulates fatty acid utilization in primary human skeletal muscle cells. Diabetes 51:901-909
21. Evans WJ, Phinney SD, Young VR 1982 Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc 14:101-102
22. Kim JY, Koves TR, Yu GS, Gulick T, Cortright RN, Dohm GL, Muoio DM 2002 Evidence of a malonyl-CoA-insensitive carnitine palmitoyltransferase I activity in red skeletal muscle. Am J Physiol Endocrinol Metab 282:E1014-E1022 (Pubitemid 34654714)
23. Hulver MW, Berggren JR, Carper MJ, Miyazaki M, Ntambi JM, Hoffman EP, Thyfault JP, Stevens R, Dohm GL, Houmard JA, Muoio DM 2005 Elevated stearoyl-CoA desaturase-1 expression in skeletal muscle contributes to abnormal fatty acid partitioning in obese humans. Cell Metab 2:251-261
24. Kim JY, Hickner RC, Cortright RL, Dohm GL, Houmard JA 2000 Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab 279:E1039-E1044
25. Hulver MW, Berggren JR, Cortright RN, Dudek RW, Thompson RP, Pories WJ, MacDonald KG, Cline GW, Shulman GI, Dohm GL, Houmard JA 2003 Skeletal muscle lipid metabolism with obesity. Am J Physiol Endocrinol Metab 284:E741-E747
26. Gomez-Foix AM, Coats WS, Baque S, Alam T, Gerard RD, Newgard CB 1992 Adenovirus-mediated transfer of the muscle glycogen phosphorylase gene into hepatocytes confers altered regulation of glycogen metabolism. J Biol Chem 267:25129-25134
27. Koves TR, Li P, An J, Akimoto T, Slentz D, Ilkayeva O, Dohm GL, Yan Z, Newgard CB, Muoio DM 2005 Peroxisome proliferator-activated receptor-γ co-activator 1α-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J Biol Chem 280:33588-33598
28. Cortright RN, Azevedo Jr JL, Zhou Q, Sinha M, Pories WJ, Itani SI, Dohm GL 2000 Protein kinase C modulates insulin action in human skeletal muscle. Am J Physiol Endocrinol Metab 278:E553-E562
29. Thyfault JP, Kraus RM, Hickner RC, Howell AW, Wolfe RR, Dohm GL 2004 Impaired plasma fatty acid oxidation in extremely obese women. Am J Physiol Endocrinol Metab 287:E1076-E1081
30. Laybutt DR, Schmitz-Peiffer C, Saha AK, Ruderman NB, Biden TJ, Kraegen EW 1999 Muscle lipid accumulation and protein kinase C activation in the insulin-resistant chronically glucose-infused rat. Am J Physiol 277:E1070-E1076
31. Ellis BA, Poynten A, Lowy AJ, Furler SM, Chisholm DJ, Kraegen EW, Cooney GJ 2000 Long-chain acyl-CoA esters as indicators of lipid metabolism and insulin sensitivity in rat and human muscle. Am J Physiol Endocrinol Metab 279:E554-E560
32. Krssak M, Falk Petersen K, Dresner A, DiPietro L, Vogel SM, Rothman DL, Roden M, Shulman GI 1999 Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia [Errata (1999) 42:386 and 42: 1269] 42:113-116
33. Goodyear LJ, Giorgino F, Sherman LA, Carey J, Smith RJ, Dohm GL 1995 Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects. J Clin Invest 95:2195-2204
34. Adams 2nd JM, Pratipanawatr T, Berria R, Wang E, DeFronzo RA, Sullards MC, Mandarino LJ 2004 Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 53:25-31
35. Cusi K, Maezono K, Osman A, Pendergrass M, Patti ME, Pratipanawatr T, DeFronzo RA, Kahn CR, Mandarino LJ 2000 Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J Clin Invest 105:311-320
36. Lowell BB, Shulman GI 2005 Mitochondrial dysfunction and type 2 diabetes. Science 307:384-387
37. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI 2004 Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes [see comment]. N Engl J Med 350:664-671
38. Noland RC, Koves TR, Seiler SE, Lum H, Lust RM, Ilkayeva O, Stevens RD, Hegardt FG, Muoio DM 2009 Carnitine insufficiency caused by aging and overnutrition compromises mitochondrial performance and metabolic control. J Biol Chem 284:22840-22852
39. 2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119:573-581