Determinants of intramyocellular triglyceride turnover: Implications for insulin sensitivity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 294, Issue 2, 2008, Pages

  Moro, Cédric ^a   Bajpeyi, Sudip ^a   Smith, Steven R ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Exercise; Lipid storage; Lipolysis; Skeletal muscle; Type 2 diabetes

Indexed keywords

FAT DROPLET; FATTY ACID; INSULIN; LIPID; TRIACYLGLYCEROL;

DIABETIC OBESITY; ENDURANCE; FATTY ACID OXIDATION; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIPOLYSIS; MITOCHONDRIAL RESPIRATION; MUSCLE LEVEL; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; TRAINING;

ANIMALS; FATTY ACIDS, NONESTERIFIED; HUMANS; INSULIN RESISTANCE; LIPOPROTEINS; MUSCLE FIBERS; OXIDATION-REDUCTION; TRIGLYCERIDES;

EID: 38949161524     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00624.2007     Document Type: Review

References (142)

1. Aas V, Kase ET, Solberg R, Jensen J, Rustan AC. Chronic hyperglycaemia promotes lipogenesis and triacylglycerol accumulation in human skeletal muscle cells. Diabetologia 47: 1452-1461, 2004.
2. 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 53: 25-31, 2004.
3. Andres R, Cader G, Zierler KL. The quantitatively minor role of carbohydrate in oxidative metabolism by skeletal muscle in intact man in the basal state; measurements of oxygen and glucose uptake and carbon dioxide and lactate production in the forearm. J Clin Invest 35: 671-682, 1956.
4. Bachmann OP, Dahl DB, Brechtel K, Machann J, Haap M, Maier T, Loviscach M, Stumvoll M, Claussen CD, Schick F, Haring HU, Jacob S. Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes 50: 2579-2584, 2001.
5. Baltzan MA, Andres R, Cader G, Zierler KL. Heterogeneity of forearm metabolism with special reference to free fatty acids. J Clin Invest 41: 116-125, 1962.
6. Bandyopadhyay GK, Yu JG, Ofrecio J, Olefsky JM. Increased malonyl-CoA levels in muscle from obese and type 2 diabetic subjects lead to decreased fatty acid oxidation and increased lipogenesis; thiazolidinedione treatment reverses these defects. Diabetes 55: 2277-2285, 2006.
7. Belfrage P, Jergil B, Stralfors P, Tornqvist H. Hormone-sensitive lipase of rat adipose tissue: identification and some properties of the enzyme protein. FEBS Lett 75: 259-264, 1977.
8. Blaak EE, Schiffelers SL, Saris WH, Mensink M, Kooi ME. Impaired beta-adrenergically mediated lipolysis in skeletal muscle of obese subjects. Diabetologia 47: 1462-1468, 2004.
9. Blaak EE, van Aggel-Leijssen DP, Wagenmakers AJ, Saris WH, van Baak MA. Impaired oxidation of plasma-derived fatty acids in type 2 diabetic subjects during moderate-intensity exercise. Diabetes 49: 2102-2107, 2000.
10. Blaak EE, Wagenmakers AJ. The fate of [U-(13)C]palmitate extracted by skeletal muscle in subjects with type 2 diabetes and control subjects. Diabetes 51: 784-789, 2002.
11. Boden G, Chen X, Ruiz J, White JV, Rossetti L. Mechanisms of fatty acid-induced inhibition of glucose uptake. J Clin Invest 93: 2438-2446, 1994.
12. Boden G, Lebed B, Schatz M, Homko C, Lemieux S. Effects of acute changes of plasma free fatty acids on intramyocellular fat content and insulin resistance in healthy subjects. Diabetes 50: 1612-1617, 2001.
13. Bonen A, Parolin ML, Steinberg GR, Calles-Escandon J, Tandon NN, Glatz JF, Luiken JJ, Heigenhauser GJ, Dyck DJ. 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, 2004.
14. Boon H, Blaak EE, Saris WH, Keizer HA, Wagenmakers AJ, van Loon LJ. Substrate source utilisation in long-term diagnosed type 2 diabetes patients at rest, and during exercise and subsequent recovery. Diabetologia 50: 103-112, 2007.
15. Braun B, Sharoff C, Chipkin SR, Beaudoin F. Effects of insulin resistance on substrate utilization during exercise in overweight women. J Appl Physiol 97: 991-997, 2004.
16. Bruce CR, Anderson MJ, Carey AL, Newman DG, Bonen A, Kriketos AD, Cooney GJ, Hawley JA. Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J Clin Endocrinol Metab 88: 5444-5451, 2003.
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 291: E99-E107, 2006.
18. Carter SL, Rennie C, Tarnopolsky MA. Substrate utilization during endurance exercise in men and women after endurance training. Am J Physiol Endocrinol Metab 280: E898-E907, 2001.
19. Clifford GM, Londos C, Kraemer FB, Vernon RG, Yeaman SJ. Translocation of hormone-sensitive lipase and perilipin upon lipolytic stimulation of rat adipocytes. J Biol Chem 275: 5011-5015, 2000.
20. Coggan AR, Raguso CA, Gastaldelli A, Sidossis LS, Yeckel CW. Fat metabolism during high-intensity exercise in endurance-trained and untrained men. Metabolism 49: 122-128, 2000.
21. Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, Holloszy JO. Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J Appl Physiol 72: 1780-1786, 1992.
22. Cooney GJ, Thompson AL, Furler SM, Ye J, Kraegen EW. Muscle long-chain acyl CoA esters and insulin resistance. Ann NY Acad Sci 967: 196-207, 2002.
23. Coppack SW, Persson M, Judd RL, Miles JM. Glycerol and nonesterified fatty acid metabolism in human muscle and adipose tissue in vivo. Am J Physiol Endocrinol Metab 276: E233-E240, 1999.
24. Coyle EF, Jeukendrup AE, Oseto MC, Hodgkinson BJ, Zderic TW. Low-fat diet alters intramuscular substrates and reduces lipolysis and fat oxidation during exercise. Am J Physiol Endocrinol Metab 280: E391-E398, 2001.
25. Dagenais GR, Tancredi RG, Zierler KL. Free fatty acid oxidation by forearm muscle at rest, and evidence for an intramuscular lipid pool in the human forearm. J Clin Invest 58: 421-431, 1976.
26. Dalen KT, Dahl T, Holter E, Arntsen B, Londos C, Sztalryd C, Nebb HI. LSDP5 is a PAT protein specifically expressed in fatty acid oxidizing tissues. Biochim Biophys Acta 1771: 210-227, 2007.
27. Decombaz J, Schmitt B, Ith M, Decarli B, Diem P, Kreis R, Hoppeler H, Boesch C. Postexercise fat intake repletes intramyocellular lipids but no faster in trained than in sedentary subjects. Am J Physiol Regul Integr Comp Physiol 281: R760-R769, 2001.
28. Donsmark M, Langfort J, Holm C, Ploug T, Galbo H. Contractions activate hormone-sensitive lipase in rat muscle by protein kinase C and mitogen-activated protein kinase. J Physiol 550: 845-854, 2003.
29. Dresner A, Laurent D, Marcucci M, Griffin ME, Dufour S, Cline GW, Slezak LA, Andersen DK, Hundal RS, Rothman DL, Petersen KF, Shulman GI. Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity. J Clin Invest 103: 253-259, 1999.
30. Dulloo AG, Gubler M, Montani JP, Seydoux J, Solinas G. Substrate cycling between de novo lipogenesis and lipid oxidation: a thermogenic mechanism against skeletal muscle lipotoxicity and glucolipotoxicity. Int J Obes Relat Metab Disord 28, Suppl 4: S29-S37, 2004.
31. Dyck DJ, Peters SJ, Glatz J, Gorski J, Keizer H, Kiens B, Liu S, Richter EA, Spriet LL, van der Vusse GJ, Bonen A. Functional differences in lipid metabolism in resting skeletal muscle of various fiber types. Am J Physiol Endocrinol Metab 272: E340-E351, 1997.
32. Flatt JP. Macronutrient composition and food selection. Obes Res 9, Suppl 4: 256S-262S, 2001.
33. Forouhi NG, Jenkinson G, Thomas EL, Mullick S, Mierisova S, Bhonsle U, McKeigue PM, Bell JD. Relation of triglyceride stores in skeletal muscle cells to central obesity and insulin sensitivity in European and South Asian men. Diabetologia 42: 932-935, 1999.
34. Gaster M, Beck-Nielsen H. Triacylglycerol accumulation is not primarily affected in myotubes established from type 2 diabetic subjects. Biochim Biophys Acta 1761: 100-110, 2006.
35. Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 86: 5755-5761, 2001.
36. Goodpaster BH, Thaete FL, Simoneau JA, Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes 46: 1579-1585, 1997.
37. Goodpaster BH, Wolfe RR, Kelley DE. Effects of obesity on substrate utilization during exercise. Obes Res 10: 575-584, 2002.
38. Griffin ME, Marcucci MJ, Cline GW, Bell K, Barucci N, Lee D, Goodyear LJ, Kraegen EW, White MF, Shulman GI. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes 48: 1270-1274, 1999.
39. Guillet-Deniau I, Pichard AL, Kone A, Esnous C, Nieruchalski M, Girard J, Prip-Buus C. Glucose induces de novo lipogenesis in rat muscle satellite cells through a sterol-regulatory-element-binding-protein-1c-dependent pathway. J Cell Sci 117: 1937-1944, 2004.
40. Guo Z, Jensen MD. Blood glycerol is an important precursor for intramuscular triacylglycerol synthesis. J Biol Chem 274: 23702-23706, 1999.
41. Haemmerle G, Lass A, Zimmermann R, Gorkiewicz G, Meyer C, Rozman J, Heldmaier G, Maier R, Theussl C, Eder S, Kratky D, Wagner EF, Klingenspor M, Hoefler G, Zechner R. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312: 734-737, 2006.
42. Haemmerle G, Zimmermann R, Hayn M, Theussl C, Waeg G, Wagner E, Sattler W, Magin TM, Wagner EF, Zechner R. Hormone-sensitive lipase deficiency in mice causes diglyceride accumulation in adipose tissue, muscle, and testis. J Biol Chem 277: 4806-4815, 2002.
43. Haugaard SB, Vaag A, Hoy CE, Madsbad S. Desaturation of skeletal muscle structural and depot lipids in obese individuals during a very-low-calorie diet intervention. Obesity (Silver Spring) 15: 117-125, 2007.
44. Helge JW, Biba TO, Galbo H, Gaster M, Donsmark M. Muscle triacylglycerol and hormone-sensitive lipase activity in untrained and trained human muscles. Eur J Appl Physiol 97: 566-572, 2006.
45. Helge JW, Dobrzyn A, Saltin B, Gorski J. Exercise and training effects on ceramide metabolism in human skeletal muscle. Exp Physiol 89: 119-127, 2004.
46. 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 Endocrinol Metab 259: E593-E598, 1990.
47. 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 Endocrinol Metab 268: E453-E457, 1995.
48. Hulver MW, Berggren JR, Carper MJ, Miyazaki M, Ntambi JM, Hoffman EP, Thyfault JP, Stevens R, Dohm GL, Houmard JA, Muoio DM. Elevated stearoyl-CoA desaturase-1 expression in skeletal muscle contributes to abnormal fatty acid partitioning in obese humans. Cell Metab 2: 251-261, 2005.
49. Hulver MW, Berggren JR, Cortright RN, Dudek RW, Thompson RP, Pories WJ, MacDonald KG, Cline GW, Shulman GI, Dohm GL, Houmard JA. Skeletal muscle lipid metabolism with obesity. Am J Physiol Endocrinol Metab 284: E741-E747, 2003.
50. Hurley BF, Nemeth PM, Martin WH 3rd, Hagberg JM, Dalsky GP, Holloszy JO. Muscle triglyceride utilization during exercise: effect of training. J Appl Physiol 60: 562-567, 1986.
51. 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 51: 2005-2011, 2002.
52. Jacob S, Machann J, Rett K, Brechtel K, Volk A, Renn W, Maerker E, Matthaei S, Schick F, Claussen CD, Haring HU. Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes 48: 1113-1119, 1999.
53. Jansson E, Kaijser L. Substrate utilization and enzymes in skeletal muscle of extremely endurance-trained men. J Appl Physiol 62: 999-1005, 1987.
54. Jong-Yeon K, Hickner RC, Dohm GL, Houmard JA. Long- and medium-chain fatty acid oxidation is increased in exercise-trained human skeletal muscle. Metabolism 51: 460-464, 2002.
55. Kelley DE, Goodpaster B, Wing RR, Simoneau JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol Endocrinol Metab 277: E1130-E1141, 1999.
56. Kelley DE, Goodpaster BH, Storlien L. Muscle triglyceride and insulin resistance. Annu Rev Nutr 22: 325-346, 2002.
57. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
58. Kelley DE, Simoneau JA. Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest 94: 2349-2356, 1994.
59. 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 270: 397-400, 1990.
60. Kiens B. Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev 86: 205-243, 2006.
61. Kiens B, Essen-Gustavsson B, Gad P, Lithell H. Lipoprotein lipase activity and intramuscular triglyceride stores after long-term high-fat and high-carbohydrate diets in physically trained men. Clin Physiol 7: 1-9, 1987.
62. Kiens B, Kristiansen S, Jensen P, Richter EA, Turcotte LP. Membrane associated fatty acid binding protein (FABPpm) in human skeletal muscle is increased by endurance training. Biochem Biophys Res Commun 231: 463-465, 1997.
63. Kiens B, Richter EA. Utilization of skeletal muscle triacylglycerol during postexercise recovery in humans. Am J Physiol Endocrinol Metab 275: E332-E337, 1998.
64. Kiens B, Roepstorff C, Glatz JF, Bonen A, Schjerling P, Knudsen J, Nielsen JN. Lipid-binding proteins and lipoprotein lipase activity in human skeletal muscle: influence of physical activity and gender. J Appl Physiol 97: 1209-1218, 2004.
65. Kim JY, Hickner RC, Cortright RL, Dohm GL, Houmard JA. Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab 279: E1039-E1044, 2000.
66. Kjaer M, Howlett K, Langfort J, Zimmerman-Belsing T, Lorentsen J, Bulow J, Ihlemann J, Feldt-Rasmussen U, Galbo H. Adrenaline and glycogenolysis in skeletal muscle during exercise: a study in adrenal-ectomised humans. J Physiol 528: 371-378, 2000.
67. Klein S, Coyle EF, Wolfe RR. Fat metabolism during low-intensity exercise in endurance-trained and untrained men. Am J Physiol Endocrinol Metab 267: E934-E940, 1994.
68. Krssak M, Petersen KF, Dresner A, DiPietro L, Vogel SM, Rothman DL, Roden M, Shulman GI. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 42: 113-116, 1999.
69. Krssak M, Petersen KF, Bergeron R, Price T, Laurent D, Rothman DL, Roden M, Shulman GI. Intramuscular glycogen and intramyocellular lipid utilization during prolonged exercise and recovery in man: a 13C and 1H nuclear magnetic resonance spectroscopy study. J Clin Endocrinol Metab 85: 748-754, 2000.
70. Langfort J, Ploug T, Ihlemann J, Holm C, Galbo H. Stimulation of hormone-sensitive lipase activity by contractions in rat skeletal muscle. Biochem J 351: 207-214, 2000.
71. Langfort J, Ploug T, Ihlemann J, Saldo M, Holm C, Galbo H. Expression of hormone-sensitive lipase and its regulation by adrenaline in skeletal muscle. Biochem J 340: 459-465, 1999.
72. Langin D, Dicker A, Tavernier G, Hoffstedt J, Mairal A, Ryden M, Arner E, Sicard A, Jenkins CM, Viguerie N, van Harmelen V, Gross RW, Holm C, Arner P. Adipocyte lipases and defect of lipolysis in human obesity. Diabetes 54: 3190-3197, 2005.
73. Lessard SJ, Rivas DA, Chen ZP, Bonen A, Febbraio MA, Reeder DW, Kemp BE, Yaspelkis BB 3rd, Hawley JA. Tissue-specific effects of rosiglitazone and exercise in the treatment of lipid-induced insulin resistance. Diabetes 56: 1856-1864, 2007.
74. Lillioja S, Young AA, Culter CL, Ivy JL, Abbott WG, Zawadzki JK, Yki-Jarvinen H, Christin L, Secomb TW, Bogardus C. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 80: 415-424, 1987.
75. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV Jr, Ory DS, Schaffer JE. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 100: 3077-3082, 2003.
76. Liu L, Zhang Y, Chen N, Shi X, Tsang B, Yu YH. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J Clin Invest 117: 1679-1689, 2007.
77. Menshikova EV, Ritov VB, Toledo FG, Ferrell RE, Goodpaster BH, Kelley DE. Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity. Am J Physiol Endocrinol Metab 288: E818-E825, 2005.
78. Mittendorfer B, Horowitz JF, Klein S. Effect of gender on lipid kinetics during endurance exercise of moderate intensity in untrained subjects. Am J Physiol Endocrinol Metab 283: E58-E65, 2002.
79. Montell E, Lerin C, Newgard CB, Gomez-Foix AM. Effects of modulation of glycerol kinase expression on lipid and carbohydrate metabolism in human muscle cells. J Biol Chem 277: 2682-2686, 2002.
80. Neptune EM Jr, Sudduth HC, Foreman DR. Labile fatty acids of rat diaphragm muscle and their possible role as the major endogenous substrate for maintenance of respiration. J Biol Chem 234: 1659-1660, 1959.
81. Nyholm B, Qu Z, Kaal A, Pedersen SB, Gravholt CH, Andersen JL, Saltin B, Schmitz O. Evidence of an increased number of type IIb muscle fibers in insulin-resistant first-degree relatives of patients with NIDDM. Diabetes 46: 1822-1828, 1997.
82. O'Neill M, Watt MJ, Heigenhauser GJ, Spriet LL. Effects of reduced free fatty acid availability on hormone-sensitive lipase activity in human skeletal muscle during aerobic exercise. J Appl Physiol 97: 1938-1945, 2004.
83. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, Storlien LH. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46: 983-988, 1997.
84. Pelsers MM, Tsintzas K, Boon H, Jewell K, Norton L, Luiken JJ, Glatz JF, van Loon LJ. Skeletal muscle fatty acid transporter protein expression in type 2 diabetes patients compared with overweight, sedentary men and age-matched, endurance-trained cyclists. Acta Physiol (Oxf) 190: 209-219, 2007.
85. Pender C, Trentadue AR, Pories WJ, Dohm GL, Houmard JA, Youngren JF. Expression of genes regulating malonyl-CoA in human skeletal muscle. J Cell Biochem 99: 860-867, 2006.
86. Perez-Martin A, Dumortier M, Raynaud E, Brun JF, Fedou C, Bringer J, Mercier J. Balance of substrate oxidation during submaximal exercise in lean and obese people. Diabetes Metab 27: 466-474, 2001.
87. Perseghin G, Scifo P, De Cobelli F, Pagliato E, Battezzati A, Arcelloni C, Vanzulli A, Testolin G, Pozza G, Del Maschio A, Luzi L. Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 48: 1600-1606, 1999.
88. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 664-671, 2004.
89. Petersen KF, Shulman GI. Pathogenesis of skeletal muscle insulin resistance in type 2 diabetes mellitus. Am J Cardiol 90: 11G-18G, 2002.
90. Phillips DI, Caddy S, Ilic V, Fielding BA, Frayn KN, Borthwick AC, Taylor R. Intramuscular triglyceride and muscle insulin sensitivity: evidence for a relationship in nondiabetic subjects. Metabolism 45: 947-950, 1996.
91. 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 13: 1321-1329, 2005.
92. Pickersgill L, Litherland GJ, Greenberg AS, Walker M, Yeaman SJ. Key role for ceramides in mediating insulin resistance in human muscle cells. J Biol Chem 282: 12583-12589, 2007.
93. Pinnamaneni SK, Southgate RJ, Febbraio MA, Watt MJ. Stearoyl CoA desaturase 1 is elevated in obesity but protects against fatty acid-induced skeletal muscle insulin resistance in vitro. Diabetologia 49: 3027-3037, 2006.
94. Prats C, Donsmark M, Qvortrup K, Londos C, Sztalryd C, Holm C, Galbo H, Ploug T. Decrease in intramuscular lipid droplets and translocation of HSL in response to muscle contraction and epinephrine. J Lipid Res 47: 2392-2399, 2006.
95. Proctor DN, Sinning WE, Walro JM, Sieck GC, Lemon PW. Oxidative capacity of human muscle fiber types: effects of age and training status. J Appl Physiol 78: 2033-2038, 1995.
96. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54: 8-14, 2005.
97. Roden M. Muscle triglycerides and mitochondrial function: possible mechanisms for the development of type 2 diabetes. Int J Obes (Lond) 29, Suppl 2: S111-S115, 2005.
98. Roden M, Price TB, Perseghin G, Petersen KF, Rothman DL, Cline GW, Shulman GI. Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 97: 2859-2865, 1996.
99. Roepstorff C, Donsmark M, Thiele M, Vistisen B, Stewart G, Vissing K, Schjerling P, Hardie DG, Galbo H, Kiens B. Sex differences in hormone-sensitive lipase expression, activity, and phosphorylation in skeletal muscle at rest and during exercise. Am J Physiol Endocrinol Metab 291: E1106-E1114, 2006.
100. Roepstorff C, Vistisen B, Donsmark M, Nielsen JN, Galbo H, Green KA, Hardie DG, Wojtaszewski JF, Richter EA, Kiens B. Regulation of hormone-sensitive lipase activity and Ser563 and Ser565 phosphorylation in human skeletal muscle during exercise. J Physiol 560: 551-562, 2004.
101. Roepstorff C, Vistisen B, Kiens B. Intramuscular triacylglycerol in energy metabolism during exercise in humans. Exerc Sport Sci Rev 33: 182-188, 2005.
102. Roorda BD, Hesselink MK, Schaart G, Moonen-Kornips E, Martinez-Martinez P, Losen M, De Baets MH, Mensink RP, Schrauwen P. DGAT1 overexpression in muscle by in vivo DNA electroporation increases intramyocellular lipid content. J Lipid Res 46: 230-236, 2005.
103. Ruan H, Pownall HJ. Overexpression of 1-acyl-glycerol-3-phosphate acyltransferase-alpha enhances lipid storage in cellular models of adipose tissue and skeletal muscle. Diabetes 50: 233-240, 2001.
104. Russell AP. Lipotoxicity: the obese and endurance-trained paradox. Int J Obes Relat Metab Disord 28, Suppl 4: S66-S71, 2004.
105. Russell AP, Gastaldi G, Bobbioni-Harsch E, Arboit P, Gobelet C, Deriaz O, Golay A, Witztum JL, Giacobino JP. Lipid peroxidation in skeletal muscle of obese as compared to endurance-trained humans: a case of good vs. bad lipids? FEBS Lett 551: 104-106, 2003.
106. Schenk S, Horowitz JF. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest 117: 1690-1698, 2007.
107. Schmitz-Peiffer C, Craig DL, Biden TJ. Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J Biol Chem 274: 24202-24210, 1999.
108. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK, Moonen-Kornips E, Schaart G, Mustard KJ, Hardie DG, Saris WH, Nicolay K, Schrauwen P. Intramyocellular lipid content and molecular adaptations in response to a 1-week high-fat diet. Obes Res 13: 2088-2094, 2005.
109. Schrauwen-Hinderling VB, Schrauwen P, Hesselink MK, van Engelshoven JM, Nicolay K, Saris WH, Kessels AG, Kooi ME. The increase in intramyocellular lipid content is a very early response to training. J Clin Endocrinol Metab 88: 1610-1616, 2003.
110. Sengenes C, Bouloumie A, Hauner H, Berlan M, Busse R, Lafontan M, Galitzky J. Involvement of a cGMP-dependent pathway in the natriuretic peptide-mediated hormone-sensitive lipase phosphorylation in human adipocytes. J Biol Chem 278: 48617-48626, 2003.
111. Sidossis LS, Stuart CA, Shulman GI, Lopaschuk GD, Wolfe RR. Glucose plus insulin regulate fat oxidation by controlling the rate of fatty acid entry into the mitochondria. J Clin Invest 98: 2244-2250, 1996.
112. Simoneau JA, Colberg SR, Thaete FL, Kelley DE. Skeletal muscle glycolytic and oxidative enzyme capacities are determinants of insulin sensitivity and muscle composition in obese women. FASEB J 9: 273-278, 1995.
113. Simoneau JA, Veerkamp JH, Turcotte LP, Kelley DE. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J 13: 2051-2060, 1999.
114. Smith AC, Mullen KL, Junkin KA, Nickerson J, Chabowski A, Bonen A, Dyck DJ. Metformin and exercise reduce muscle FAT/CD36 and lipid accumulation and blunt the progression of high-fat diet-induced hyperglycemia. Am J Physiol Endocrinol Metab 293: E172-E181, 2007.
115. Souza SC, de Vargas LM, Yamamoto MT, Lien P, Franciosa MD, Moss LG, Greenberg AS. Overexpression of perilipin A and B blocks the ability of tumor necrosis factor alpha to increase lipolysis in 3T3-L1 adipocytes. J Biol Chem 273: 24665-24669, 1998.
116. Sztalryd C, Bell M, Lu X, Mertz P, Hickenbottom S, Chang BH, Chan L, Kimmel AR, Londos C. Functional compensation for adipose differentiation-related protein (ADFP) by Tip47 in an ADFP null embryonic cell line. J Biol Chem 281: 34341-34348, 2006.
117. Sztalryd C, Xu G, Dorward H, Tansey JT, Contreras JA, Kimmel AR, Londos C. Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation. J Cell Biol 161: 1093-1103, 2003.
118. Talanian JL, Tunstall RJ, Watt MJ, Duong M, Perry CG, Steinberg GR, Kemp BE, Heigenhauser GJ, Spriet LL. Adrenergic regulation of HSL serine phosphorylation and activity in human skeletal muscle during the onset of exercise. Am J Physiol Regul Integr Comp Physiol 291: R1094-R1099, 2006.
119. Tanner CJ, Barakat HA, Dohm GL, Pories WJ, MacDonald KG, Cunningham PR, Swanson MS, Houmard JA. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 282: E1191-E1196, 2002.
120. Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC, Hamadeh MJ. 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, 2007.
121. Toledo FG, Menshikova EV, Ritov VB, Azuma K, Radikova Z, DeLany J, Kelley DE. Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes. Diabetes 56: 2142-2147, 2007.
122. Turpin SM, Lancaster GI, Darby I, Febbraio MA, Watt MJ. Apoptosis in skeletal muscle myotubes is induced by ceramides and is positively related to insulin resistance. Am J Physiol Endocrinol Metab 291: E1341-E1350, 2006.
123. van Loon LJ. Intramyocellular triacylglycerol as a substrate source during exercise. Proc Nutr Soc 63: 301-307, 2004.
124. van Loon LJ. Use of intramuscular triacylglycerol as a substrate source during exercise in humans. J Appl Physiol 97: 1170-1187, 2004.
125. van Loon LJ, Koopman R, Stegen JH, Wagenmakers AJ, Keizer HA, Saris WH. Intramyocellular lipids form an important substrate source during moderate intensity exercise in endurance-trained males in a fasted state. J Physiol 553: 611-625, 2003.
126. van Loon LJ, Manders RJ, Koopman R, Kaastra B, Stegen JH, Gijsen AP, Saris WH, Keizer HA. Inhibition of adipose tissue lipolysis increases intramuscular lipid use in type 2 diabetic patients. Diabetologia 48: 2097-2107, 2005.
127. van Loon LJ, Thomason-Hughes M, Constantin-Teodosiu D, Koopman R, Greenhaff PL, Hardie DG, Keizer HA, Saris WH, Wagenmakers AJ. Inhibition of adipose tissue lipolysis increases intramuscular lipid and glycogen use in vivo in humans. Am J Physiol Endocrinol Metab 289: E482-E493, 2005.
128. Vogt M, Puntschart A, Howald H, Mueller B, Mannhart C, Gfeller-Tuescher L, Mullis P, Hoppeler H. Effects of dietary fat on muscle substrates, metabolism, and performance in athletes. Med Sci Sports Exerc 35: 952-960, 2003.
129. Watt MJ, Heigenhauser GJ, O'Neill M, Spriet LL. Hormone-sensitive lipase activity and fatty acyl-CoA content in human skeletal muscle during prolonged exercise. J Appl Physiol 95: 314-321, 2003.
130. Watt MJ, Heigenhauser GJ, Spriet LL. Effects of dynamic exercise intensity on the activation of hormone-sensitive lipase in human skeletal muscle. J Physiol 547: 301-308, 2003.
131. Watt MJ, Heigenhauser GJ, Spriet LL. Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: is there a controversy? J Appl Physiol 93: 1185-1195, 2002.
132. Watt MJ, Hevener A, Lancaster GI, Febbraio MA. Ciliary neurotrophic factor prevents acute lipid-induced insulin resistance by attenuating ceramide accumulation and phosphorylation of c-Jun N-terminal kinase in peripheral tissues. Endocrinology 147: 2077-2085, 2006.
133. Watt MJ, Holmes AG, Pinnamaneni SK, Garnham AP, Steinberg GR, Kemp BE, Febbraio MA. Regulation of HSL serine phosphorylation in skeletal muscle and adipose tissue. Am J Physiol Endocrinol Metab 290: E500-E508, 2006.
134. Watt MJ, Holmes AG, Steinberg GR, Mesa JL, Kemp BE, Febbraio MA. Reduced plasma FFA availability increases net triacylglycerol degradation, but not GPAT or HSL activity, in human skeletal muscle. Am J Physiol Endocrinol Metab 287: E120-E127, 2004.
135. Watt MJ, Steinberg GR, Chan S, Garnham A, Kemp BE, Febbraio MA. Beta-adrenergic stimulation of skeletal muscle HSL can be overridden by AMPK signaling. FASEB J 18: 1445-1446, 2004.
136. Watt MJ, Stellingwerff T, Heigenhauser GJ, Spriet LL. Effects of plasma adrenaline on hormone-sensitive lipase at rest and during moderate exercise in human skeletal muscle. J Physiol 550: 325-332, 2003.
137. Wolins NE, Quaynor BK, Skinner JR, Tzekov A, Croce MA, Gropler MC, Varma V, Yao-Borengasser A, Rasouli N, Kern PA, Finck BN, Bickel PE. OXPAT/PAT-1 is a PPAR-induced lipid droplet protein that promotes fatty acid utilization. Diabetes 55: 3418-3428, 2006.
138. Wolins NE, Skinner JR, Schoenfish MJ, Tzekov A, Bensch KG, Bickel PE. Adipocyte protein S3-12 coats nascent lipid droplets. J Biol Chem 278: 37713-37721, 2003.
139. Yamaguchi T, Matsushita S, Motojima K, Hirose F, Osumi T. MLDP, a novel PAT family protein localized to lipid droplets and enriched in the heart, is regulated by peroxisome proliferator-activated receptor alpha. J Biol Chem 281: 14232-14240, 2006.
140. Ye J. Role of insulin in the pathogenesis of free fatty acid-induced insulin resistance in skeletal muscle. Endocr Metab Immune Disord Drug Targets 7: 65-74, 2007.
141. 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 277: 50230-50236, 2002.
142. Zderic TW, Davidson CJ, Schenk S, Byerley LO, Coyle EF. High-fat diet elevates resting intramuscular triglyceride concentration and whole body lipolysis during exercise. Am J Physiol Endocrinol Metab 286: E217-E225, 2004.