Insulin resistance is associated with higher intramyocellular triglycerides in type I but not type II myocytes concomitant with higher ceramide content

Diabetes

Volumn 59, Issue 1, 2010, Pages 80-88

  Coen, Paul M ^a   Dubé, John J ^a   Amati, Francesca ^b   Stefanovic Racic, Maja ^a   Ferrell, Robert E ^c   Toledo, Frederico G S ^a   Goodpaster, Bret H ^a  

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

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; FAT DROPLET; LIGNOCERIC ACID; MYRISTIC ACID; PALMITIC ACID; PALMITOLEIC ACID; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; STEARIC ACID; TRIACYLGLYCEROL; ACTIN; BETA 2 MICROGLOBULIN; DIACYLGLYCEROL; FATTY ACID; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; RNA; SPHINGOLIPID;

ADULT; AEROBIC CAPACITY; AGED; ARTICLE; BODY COMPOSITION; CELL LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; FAST MUSCLE FIBER; FATTY ACID METABOLISM; FEMALE; GENE EXPRESSION; GLUCOSE CLAMP TECHNIQUE; HUMAN; HUMAN TISSUE; INSULIN RESISTANCE; INSULIN SENSITIVITY; MUSCLE CELL; OBESITY; PRIORITY JOURNAL; SLOW MUSCLE FIBER; VASTUS LATERALIS MUSCLE; BIOPSY; BLOOD; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SKELETAL MUSCLE;

ACTINS; BETA 2-MICROGLOBULIN; BIOPSY; BODY COMPOSITION; CERAMIDES; DIGLYCERIDES; FATTY ACIDS, NONESTERIFIED; FEMALE; GENE EXPRESSION; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HUMANS; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INSULIN RESISTANCE; MUSCLE CELLS; MUSCLE, SKELETAL; POLYMERASE CHAIN REACTION; RNA; SPHINGOLIPIDS; TRIGLYCERIDES;

EID: 77449161528     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0988     Document Type: Article

References (50)

1. Boden G, Chen X, Ruiz J, White JV, Rossetti L. Mechanisms of fatty acid-induced inhibition of glucose uptake. J Clin Invest 1994;93:2438-2446
2. Randle PJ, Newsholme EA, Garland PB. Regulation of glucose uptake by muscle. 8. Effects of fatty acids, ketone bodies and pyruvate, and of alloxan-diabetes and starvation, on the uptake and metabolic fate of glucose in rat heart and diaphragm muscles. Biochem J 1964;93:652-665
3. 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
4. Goodpaster BH, Kelley DE. Skeletal muscle triglyceride: marker or mediator of obesity-induced insulin resistance in type 2 diabetes mellitus? Curr Diab Rep 2002;2:216-222
5. Goodpaster BH, Theriault R, Watkins SC, Kelley DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 2000;49:467-472
6. Consitt LA, Bell JA, Houmard JA. Intramuscular lipid metabolism, insulin action, and obesity. IUBMB Life 2009;61:47-55
7. Summers SA. Ceramides in insulin resistance and lipotoxicity. Prog Lipid Res 2006;45:42-72
8. Yu C, Chen Y, Cline GW, Zhang D, Zong H, Wang Y, Bergeron R, Kim JK, Cushman SW, Cooney GJ, Atcheson B, White MF, Kraegen EW, Shulman GI. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem 2002;277:50230-50236
9. Turinsky J, O'Sullivan DM, Bayly BP. 1,2-Diacylglycerol and ceramide levels in insulin-resistant tissues of the rat in vivo. J Biol Chem 1990;265:16880-16885
10. Hoy AJ, Brandon AE, Turner N, Watt MJ, Bruce CR, Cooney GJ, Kraegen EW. Lipid and insulin infusion-induced skeletal muscle insulin resistance is likely due to metabolic feedback and not changes in IRS-1, Akt, or AS160 phosphorylation. Am J Physiol Endocrinol Metab 2009;297:E67-E75
11. Boden G. Ceramide: a contributor to insulin resistance or an innocent bystander? Diabetologia 2008;51:1095-1096
12. Straczkowski M, Kowalska I, Baranowski M, Nikolajuk A, Otziomek E, Zabielski P, Adamska A, Blachnio A, Gorski J, Gorska M. Increased skeletal muscle ceramide level in men at risk of developing type 2 diabetes. Diabetologia 2007;50:2366-2373
13. Adams JM 2nd, Pratipanawatr T, Berria R, Wang E, DeFronzo RA, Sullards MC, Mandarino LJ. Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 2004;53:25-31
14. Straczkowski M, Kowalska I, Nikolajuk A, Dzienis-Straczkowska S, Kinalska I, Baranowski M, Zendzian-Piotrowska M, Brzezinska Z, Gorski J. Relationship between insulin sensitivity and sphingomyelin signaling pathway in human skeletal muscle. Diabetes 2004;53:1215-1221
15. Thrush AB, Chabowski A, Heigenhauser GJ, McBride BW, Or-Rashid M, Dyck DJ. Conjugated linoleic acid increases skeletal muscle ceramide content and decreases insulin sensitivity in overweight, non-diabetic humans. Appl Physiol Nutr Metab 2007;32:372-382
16. Dubé JJ, Amati F, Stefanovic-Racic M, Toledo FG, Sauers SE, Goodpaster BH. Exercise-induced alterations in intramyocellular lipids and insulin resistance: the athlete's paradox revisited. Am J Physiol Endocrinol Metab 2008;294:E882-E888
17. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ, Dyck DJ. Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab 2006;291:E99-E107
18. Skovbro M, Baranowski M, Skov-Jensen C, Flint A, Dela F, Gorski J, Helge JW. Human skeletal muscle ceramide content is not a major factor in muscle insulin sensitivity. Diabetologia 2008;51:1253-1260
19. Itani SI, Ruderman NB, Schmieder F, Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 2002;51:2005-2011
20. Moro C, Galgani JE, Luu L, Pasarica M, Mairal A, Bajpeyi S, Schmitz G, Langin D, Liebisch G, Smith SR. Influence of gender, obesity, and muscle lipase activity on intramyocellular lipids in sedentary individuals. J Clin Endocrinol Metab 2009;94:3440-3447
21. Anastasiou CA, Kavouras SA, Lentzas Y, Gova A, Sidossis LS, Melidonis A. Diabetes mellitus is associated with increased intramyocellular triglyceride, but not diglyceride, content in obese humans. Metabolism 2009;58:1636-1642
22. He J, Watkins S, Kelley DE. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 2001;50:817-823
23. Essén B, Jansson E, Henriksson J, Taylor AW, Saltin B. Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiol Scand 1975;95:153-165
24. van Loon LJ, Koopman R, Manders R, van der Weegen W, van Kranenburg GP, Keizer HA. Intramyocellular lipid content in type 2 diabetes patients compared with overweight sedentary men and highly trained endurance athletes. Am J Physiol Endocrinol Metab 2004;287:E558-E565
25. Malenfant P, Joanisse DR, Thériault R, Goodpaster BH, Kelley DE, Simoneau JA. Fat content in individual muscle fibers of lean and obese subjects. Int J Obes Relat Metab Disord 2001;25:1316-1321
26. Kern M, Wells JA, Stephens JM, Elton CW, Friedman JE, Tapscott EB, Pekala PH, Dohm GL. Insulin responsiveness in skeletal muscle is determined by glucose transporter (Glut4) protein level. Biochem J 1990;270:397-400
27. Henriksen EJ, Bourey RE, Rodnick KJ, Koranyi L, Permutt MA, Holloszy JO. Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. Am J Physiol 1990;259:E593-E598
28. Goodpaster BH, Thaete FL, Simoneau JA, Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes 1997;46:1579-1585
29. Wolfe RR, Chinkes DL, Wolfe RR: Isotope Tracers in Metabolic Research: Principles and Practice of Kinetic Analysis. Hoboken, NJ, Wiley-Liss, 2005
30. Kelley DE, McKolanis TM, Hegazi RA, Kuller LH, Kalhan SC. Fatty liver in type 2 diabetes mellitus: relation to regional adiposity, fatty acids, and insulin resistance. Am J Physiol Endocrinol Metab 2003;285:E906-E916
31. Steele R. Influences of glucose loading and of injected insulin on hepatic glucose output. Ann N Y Acad Sci 1959;82:420-430
32. Pruchnic R, Katsiaras A, He J, Kelley DE, Winters C, Goodpaster BH. Exercise training increases intramyocellular lipid and oxidative capacity in older adults. Am J Physiol Endocrinol Metab 2004;287:E857-E862
33. Bielawski J, Szulc ZM, Hannun YA, Bielawska A. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 2006;39:82-91
34. Menshikova EV, Ritov VB, Fairfull L, Ferrell RE, Kelley DE, Goodpaster BH. Effects of exercise on mitochondrial content and function in aging human skeletal muscle. J Gerontol A Biol Sci Med Sci 2006;61:534-540
35. Phielix E, Mensink M. Type 2 diabetes mellitus and skeletal muscle metabolic function. Physiol Behav 2008;94:252-258
36. Hickey MS, Carey JO, Azevedo JL, Houmard JA, Pories WJ, Israel RG, Dohm GL. Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans. Am J Physiol 1995;268:E453-E457
37. Oberbach A, Bossenz Y, Lehmann S, Niebauer J, Adams V, Paschke R, Schön MR, Blüher M, Punkt K. Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 2006;29:895-900
38. James DE, Jenkins AB, Kraegen EW. Heterogeneity of insulin action in individual muscles in vivo: euglycemic clamp studies in rats. Am J Physiol 1985;248:E567-E574
39. Cowart LA. Sphingolipids: players in the pathology of metabolic disease. Trends Endocrinol Metab 2009;20:34-42
40. Chavez JA, Holland WL, Bär J, Sandhoff K, Summers SA. Acid ceramidase overexpression prevents the inhibitory effects of saturated fatty acids on insulin signaling. J Biol Chem 2005;280:20148-20153
41. Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, Liu Y, Narra K, Hoehn KL, Knotts TA, Siesky A, Nelson DH, Karathanasis SK, Fontenot GK, Birnbaum MJ, Summers SA. Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab 2007;5:167-179
42. Dbaibo GS, El-Assaad W, Krikorian A, Liu B, Diab K, Idriss NZ, El-Sabban M, Driscoll TA, Perry DK, Hannun YA. Ceramide generation by two distinct pathways in tumor necrosis factor alpha-induced cell death. FEBS Lett 2001;503:7-12
43. Watt MJ, Steinberg GR. Regulation and function of triacylglycerol lipases in cellular metabolism. Biochem J 2008;414:313-325
44. Watt MJ, van Denderen BJ, Castelli LA, Bruce CR, Hoy AJ, Kraegen EW, Macaulay L, Kemp BE. Adipose triglyceride lipase regulation of skeletal muscle lipid metabolism and insulin responsiveness. Mol Endocrinol 2008;22:1200-1212
45. Jocken JW, Roepstorff C, Goossens GH, van der Baan P, van Baak M, Saris WH, Kiens B, Blaak EE. Hormone-sensitive lipase serine phosphorylation and glycerol exchange across skeletal muscle in lean and obese subjects: effect of beta-adrenergic stimulation. Diabetes 2008;57:1834-1841
46. Phillips SA, Choe CC, Ciaraldi TP, Greenberg AS, Kong AP, Baxi SC, Christiansen L, Mudaliar SR, Henry RR. Adipocyte differentiation-related protein in human skeletal muscle: relationship to insulin sensitivity. Obes Res 2005;13:1321-1329
47. Jocken JW, Smit E, Goossens GH, Essers YP, van Baak MA, Mensink M, Saris WH, Blaak EE. Adipose triglyceride lipase (ATGL) expression in human skeletal muscle is type I (oxidative) fiber specific. Histochem Cell Biol 2008;129:535-538
48. Shaw CS, Sherlock M, Stewart PM, Wagenmakers AJ. Adipophilin distribution and colocalization with lipid droplets in skeletal muscle. Histochem Cell Biol 2009;131:575-581
49. Kim JY, Tillison K, Lee JH, Rearick DA, Smas CM. The adipose tissue triglyceride lipase ATGL/PNPLA2 is downregulated by insulin and TNF-alpha in 3T3-L1 adipocytes and is a target for transactivation by PPARgamma. Am J Physiol Endocrinol Metab 2006;291:E115-E127
50. Boström P, Andersson L, Rutberg M, Perman J, Lidberg U, Johansson BR, Fernandez-Rodriguez J, Ericson J, Nilsson T, Borén J, Olofsson SO. SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nat Cell Biol 2007;9:1286-1293