The effect of exercise and nutrition on intramuscular fat metabolism and insulin sensitivity

Annual Review of Nutrition

Volumn 30, Issue , 2010, Pages 13-34

  Shaw, Christopher S ^a   Clark, Juliette ^a   Wagenmakers, Anton J M ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

diet; intramuscular triglyceride (IMTG); intramyocellular lipid (IMCL); lipolysis; skeletal muscle; triglyceride synthesis

Indexed keywords

TRIACYLGLYCEROL;

CALORIC INTAKE; DIETARY INTAKE; ENERGY EXPENDITURE; EXERCISE; HUMAN; INSULIN SENSITIVITY; LIFESTYLE; LIPID COMPOSITION; LIPID METABOLISM; LIPID STORAGE; LIPOLYSIS; MUSCLE METABOLISM; NUTRITION; PRIORITY JOURNAL; REVIEW; DIET; INSULIN RESISTANCE; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE;

DIET; ENERGY INTAKE; EXERCISE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MUSCLE, SKELETAL; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; TRIGLYCERIDES;

EID: 77955593045     PISSN: 01999885     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.nutr.012809.104817     Document Type: Review

References (144)

1. Achten J, Gleeson M, Jeukendrup AE. 2002. Determination of the exercise intensity that elicits maximal fat oxidation. Med. Sci. Sports Exerc. 34:92-97
2. Alsted TJ, Nybo L, Schweiger M, Fledelius C, Jacobsen P, et al. 2009. Adipose triglyceride lipase in human skeletalmuscle is upregulated by exercise training. Am. J. Physiol. Endocrinol. Metab. 296:E445-53
3. Bachmann OP,DahlDB, Brechtel K, Machann J,Haap M, et al. 2001. Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes 50:2579-2584 (Pubitemid 33642777)
4. Bergman BC, Butterfield GE, Wolfel EE, Casazza GA, Lopaschuk GD, Brooks GA. 1999. Evaluation of exercise and training on muscle lipid metabolism. Am. J. Physiol. 276:E106-17
5. Bergstrom J,Hermansen L, Hultman E, Saltin B. 1967. Diet,muscle glycogen and physical performance. Acta Physiol. Scand. 71:140-150
6. Blaak EE, Schiffelers SL, SarisWH, MensinkM,Kooi ME. 2004. Impaired beta-adrenergically mediated lipolysis in skeletal muscle of obese subjects. Diabetologia 47:1462-1468
7. Blaak EE, Van Aggel-LeijssenDP, Wagenmakers AJ, Saris WH, Van Baak MA. 2000. Impaired oxidation of plasma-derived fatty acids in type 2 diabetic subjects during moderate-intensity exercise. Diabetes 49:2102-2107
8. Blaak EE, Wagenmakers AJ, Glatz JF, Wolffenbuttel BH, Kemerink GJ, et al. 2000. Plasma FFA utilization and fatty acid-binding protein content are diminished in type 2 diabetic muscle. Am. J. Physiol. Endocrinol. Metab. 279:E146-54
9. Bonen A, Parolin ML, Steinberg GR, Calles-Escandon J, Tandon NN, et al. 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
10. Bostrom P, Andersson L, Rutberg M, Perman J, Lidberg U, et al. 2007. SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nat. Cell Biol. 9:1286-1293
11. Bruce CR, Kriketos AD, Cooney GJ, Hawley JA. 2004. Disassociation of muscle triglyceride content and insulin sensitivity after exercise training in patients with type 2 diabetes. Diabetologia 47:23-30
12. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, et al. 2006. Endurance training in obese humans improves glucose tolerance andmitochondrial fatty acid oxidation and altersmuscle lipid content. Am. J. Physiol. Endocrinol. Metab. 291:E99-107
13. Budohoski L, Gorski J, Nazar K, Kaciuba-Uscilko H, Terjung RL. 1996. Triacylglycerol synthesis in the different skeletal muscle fiber sections of the rat. Am. J. Physiol. 271:E574-81
14. Chalkley SM, Hettiarachchi M, Chisholm DJ, Kraegen EW. 1998. Five-hour fatty acid elevation increases muscle lipids and impairs glycogen synthesis in the rat. Metabolism 47:1121-1126
15. Chanarin I, Patel A, Slavin G, Wills EJ, Andrews TM, Stewart G. 1975. Neutral-lipid storage disease: a new disorder of lipid metabolism. Br. Med. J. 1:553-555
16. Chatzinikolaou A, Fatouros I, Petridou A, Jamurtas A, Avloniti A, et al. 2008. Adipose tissue lipolysis is upregulated in lean and obese men during acute resistance exercise. Diabetes Care 31:1397-1399
17. Chavez JA, Summers SA. 2003. Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch. Biochem. Biophys. 419:101-109
18. Coggan AR, Coyle EF. 1989. Metabolism and performance following carbohydrate ingestion late in exercise. Med. Sci. Sports Exerc. 21:59-65
19. Coggan AR, Raguso CA, Gastaldelli A, Sidossis LS, Yeckel CW. 2000. Fat metabolism during highintensity exercise in endurance-trained and untrained men. Metabolism 49:122-128
20. Coleman RA, Lee DP. 2004. Enzymes of triacylglycerol synthesis and their regulation. Prog. Lipid Res. 43:134-176
21. Coll T, Eyre E, Rodriguez-Calvo R, Palomer X, Śanchez RM, et al. 2008. Oleate reverses palmitateinduced insulin resistance and inflammation in skeletal muscle cells. J. Biol. Chem. 283:11107-11116
22. Coyle EF, Jeukendrup AE, Wagenmakers AJ, SarisWH. 1997. Fatty acid oxidation is directly regulated by carbohydrate metabolism during exercise. Am. J. Physiol. 273:E268-75
23. De BK, Dresselaers T, Kiens B, Richter EA, Van HP, Hespel P. 2007. Evaluation of intramyocellular lipid breakdown during exercise by biochemical assay, NMR spectroscopy, and oil red O staining. Am. J. Physiol. Endocrinol. Metab. 293:E428-34
24. De BK, Richter EA, Russell AP, Eijnde BO, Derave W, et al. 2005. Exercise in the fasted state facilitates fibre type-specific intramyocellular lipid breakdown and stimulates glycogen resynthesis in humans. J. Physiol. 564:649-660
25. Decombaz J, Schmitt B, Ith M, Decarli B, Diem P, et al. 2001. Postexercise fat intake repletes intramyocellular lipids but no faster in trained than in sedentary subjects. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R760-69
26. Dube JJ, Amati F, Stefanovic-Racic M, Toledo FG, Sauers SE, Goodpaster BH. 2008. Exercise-induced alterations in intramyocellular lipids and insulin resistance: the athlete's paradox revisited.Am. J. Physiol. Endocrinol. Metab. 294:E882-88
27. Dyck DJ, Steinberg G, Bonen A. 2001. Insulin increases FA uptake and esterification but reduces lipid utilization in isolated contracting muscle. Am. J. Physiol. Endocrinol. Metab. 281:E600-7
28. Egan JJ, Greenberg AS, Chang MK, Wek SA, Moos MC Jr, Londos C. 1992. Mechanism of hormonestimulated lipolysis in adipocytes: translocation of hormone-sensitive lipase to the lipid storage droplet. Proc. Natl. Acad. Sci. USA 89:8537-8541
29. Ellis BA, Poynten A, Lowy AJ, Furler SM, Chisholm DJ, et al. 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:E554-60
30. Enevoldsen LH, Stallknecht B, Langfort J, Petersen LN, Holm C, et al. 2001. The effect of exercise training on hormone-sensitive lipase in rat intra-abdominal adipose tissue and muscle. J. Physiol. 536:871-877
31. Essen-Gustavsson B, Tesch PA. 1990. Glycogen and triglyceride utilization in relation to muscle metabolic characteristics in men performing heavy-resistance exercise. Eur. J. Appl. Physiol.Occup. Physiol. 61:5-10
32. Fox AK, Kaufman AE, Horowitz JF. 2004. Adding fat calories to meals after exercise does not alter glucose tolerance. J. Appl. Physiol. 97:11-16
33. Frangioudakis G, Ye JM, Cooney GJ. 2005. Both saturated and n-6 polyunsaturated fat diets reduce phosphorylation of insulin receptor substrate-1 and protein kinase B in muscle during the initial stages of in vivo insulin stimulation. Endocrinology 146:5596-5603
34. Gan SK, Kriketos AD, Ellis BA, Thompson CH, Kraegen EW, Chisholm DJ. 2003. Changes in aerobic capacity and visceral fat but not myocyte lipid levels predict increased insulin action after exercise in overweight and obese men. Diabetes Care 26:1706-1713
35. Giacco R, Clemente G, Busiello L, Lasorella G, Rivieccio AM, et al. 2004. Insulin sensitivity is increased and fat oxidation after a high-fat meal is reduced in normal-weight healthy men with strong familial predisposition to overweight. Int. J. Obes. Relat. Metab. Disord. 28:342-348
36. Gonzalez-Baro MR, Lewin TM, Coleman RA. 2007. Regulation of triglyceridemetabolism II. Function of mitochondrial GPAT1 in the regulation of triacylglycerol biosynthesis and insulin action. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G1195-99
37. Goodpaster BH, He J,Watkins S, Kelley DE. 2001. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J. Clin. Endocrinol. Metab. 86:5755-5761
38. 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
39. Granneman JG, Moore HP, Krishnamoorthy R, Rathod M. 2009. Perilipin controls lipolysis by regulating the interactions of Ab-hydrolase containing 5 (Abhd5) and adipose trigylceride lipase (ATGL). J. Biol. Chem. 284:34538-34544
40. Greco AV, Mingrone G, Giancaterini A,Manco M, Morroni M, et al. 2002. Insulin resistance in morbid obesity. Diabetes 51:144-151
41. Greenberg AS, Egan JJ, Wek SA, Garty NB, Blanchette-Mackie EJ, Londos C. 1991. Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J. Biol. Chem. 266:11341-11346
42. Haemmerle G, Zimmermann R, Hayn M, Theussl C, Waeg G, et al. 2002. Hormone-sensitive lipase deficiency in mice causes diglyceride accumulation in adipose tissue, muscle, and testis. J. Biol. Chem. 277:4806-4815
43. Hammond LE, Neschen S, Romanelli AJ, Cline GW, Ilkayeva OR, et al. 2005. Mitochondrial glycerol-3-phosphate acyltransferase-1 is essential in liver for the metabolism of excess acyl-CoAs. J. Biol. Chem. 280:25629-25636
44. Harber MP, Crane JD, DouglassMD, Weindel KD, Trappe TA, et al. 2008. Resistance exercise reduces muscular substrates in women. Int. J. Sports Med. 29:719-725
45. He J, Goodpaster BH, Kelley DE. 2004. Effects of weight loss and physical activity on muscle lipid content and droplet size. Obes. Res. 12:761-769
46. Helge JW, Biba TO, Galbo H, Gaster M, Donsmark M. 2006. Muscle triacylglycerol and hormonesensitive lipase activity in untrained and trained human muscles. Eur. J. Appl. Physiol. 97:566-572
47. Helge JW, Dela F 2003. Effect of training on muscle triacylglycerol and structural lipids: a relation to insulin sensitivity? Diabetes 52:1881-1887
48. Helge JW, Watt PW, Richter EA, RennieMJ, Kiens B. 2001. Fat utilization during exercise: adaptation to a fat-rich diet increases utilization of plasma fatty acids and very low density lipoprotein-triacylglycerol in humans. J. Physiol. 537:1009-1020
49. Hirsch AH, Rosen OM. 1984. Lipolytic stimulation modulates the subcellular distribution of hormonesensitive lipase in 3T3-L1 cells. J. Lipid Res. 25:665-677
50. Hoppeler H. 1999. Skeletal muscle substrate metabolism. Int. J. Obes. Relat. Metab. Disord. 23(Suppl. 3):S7-10
51. Hulver MW, Berggren JR, Cortright RN, Dudek RW, Thompson RP, et al. 2003. Skeletal muscle lipid metabolism with obesity. Am. J. Physiol. Endocrinol. Metab. 284:E741-47
52. Hulver MW, Dohm GL. 2004. The molecular mechanism linking muscle fat accumulation to insulin resistance. Proc. Nutr. Soc. 63:375-380
53. Hurley BF, Nemeth PM, MartinWHIII, Hagberg JM, Dalsky GP, Holloszy JO. 1986. Muscle triglyceride utilization during exercise: effect of training. J. Appl. Physiol. 60:562-567
54. Jeukendrup AE. 2004. Carbohydrate intake during exercise and performance. Nutrition 20:669-677
55. Jocken JW, Blaak EE. 2008. Catecholamine-induced lipolysis in adipose tissue and skeletal muscle in obesity. Physiol. Behav. 94:219-230
56. Jocken JW, Smit E, Goossens GH, Essers YP, Van Baak MA, et al. 2008. Adipose triglyceride lipase (ATGL) expression in human skeletal muscle is type I (oxidative) fiber specific. Histochem. Cell Biol. 129:535-538
57. Johnson NA, Stannard SR, Rowlands DS, Chapman PG, Thompson CH, et al. 2006. Effect of shortterm starvation versus high-fat diet on intramyocellular triglyceride accumulation and insulin resistance in physically fit men. Exp. Physiol. 91:693-703
58. Kelley DE, Simoneau JA. 1994. Impaired free fatty acid utilization by skeletal muscle in non-insulindependent diabetes mellitus. J. Clin. Invest. 94:2349-2356
59. Kennedy A, Martinez K, Chuang CC, LaPoint K, McIntosh M. 2009. Saturated fatty acid-mediated inflammation and insulin resistance in adipose tissue: mechanisms of action and implications. J. Nutr. 139:1-4
60. Kienesberger PC, Lee D, Pulinilkunnil T, Brenner DS, Cai L, et al. 2009. Adipose triglyceride lipase deficiency causes tissue-specific changes in insulin signaling. J. Biol. Chem. 284:30218-30229
61. Kiens B. 2006. Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol. Rev. 86:205-243
62. Kiens B,Essen-Gustavsson B,Christensen NJ, Saltin B. 1993. Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training. J. Physiol. 469:459-478
63. Klein S, Coyle EF,Wolfe RR. 1994. Fat metabolism during low-intensity exercise in endurance-trained and untrained men. Am. J. Physiol. 267:E934-40
64. Koopman R, Manders RJ, Jonkers RA, Hul GB, Kuipers H, Van Loon LJ. 2006. Intramyocellular lipid and glycogen content are reduced following resistance exercise in untrained healthy males. Eur. J. Appl. Physiol. 96:525-534
65. Langfort J, Ploug T, Ihlemann J, Baranczuk E, Donsmark M, et al. 2003. Additivity of adrenaline and contractions on hormone-sensitive lipase, but not on glycogen phosphorylase, in ratmuscle. Acta Physiol. Scand. 178:51-60
66. Langfort J, Ploug T, Ihlemann J, Enevoldsen LH, Stallknecht B, et al. 1998. Hormone-sensitive lipase (HSL) expression and regulation in skeletal muscle. Adv. Exp. Med. Biol. 441:219-228
67. Langfort J, Ploug T, Ihlemann J, Holm C, Galbo H. 2000. Stimulation of hormone-sensitive lipase activity by contractions in rat skeletal muscle. Biochem. J. 351:207-214
68. Langfort J, Ploug T, Ihlemann J, Saldo M, Holm C, Galbo H. 1999. Expression of hormone-sensitive lipase and its regulation by adrenaline in skeletal muscle. Biochem. J. 340(Pt. 2):459-465
69. Lara-Castro C, Newcomer BR, Rowell J, Wallace P, Shaughnessy SM, et al. 2008. Effects of short-term very low-calorie diet on intramyocellular lipid and insulin sensitivity in nondiabetic and type 2 diabetic subjects. Metabolism 57:1-8
70. Larson-Meyer DE, Newcomer BR, Hunter GR. 2002. Influence of endurance running and recovery diet on intramyocellular lipid content in women: a 1H NMR study. Am. J. Physiol. Endocrinol. Metab. 282:E95-106
71. Lee JS, Pinnamaneni SK, Eo SJ, Cho IH, Pyo JH, et al. 2006. Saturated, but not n-6 polyunsaturated, fatty acids induce insulin resistance: role of intramuscular accumulation of lipid metabolites. J. Appl. Physiol. 100:1467-1474
72. Linden D, William-Olsson L, RhedinM, Asztely AK, Clapham JC, Schreyer S. 2004. Overexpression of mitochondrial GPAT in rat hepatocytes leads to decreased fatty acid oxidation and increased glycerolipid biosynthesis. J. Lipid Res. 45:1279-1288
73. Liu L, Zhang Y, Chen N, Shi X, Tsang B, Yu YH. 2007. Upregulation ofmyocellular DGAT1 augments triglyceride synthesis in skeletalmuscle and protects against fat-induced insulin resistance. J. Clin. Invest. 117:1679-1689
74. Liu L, Shi X, Bharadwaj KG, Ikeda S, Yamashita H, et al. 2009. DGAT1 expression increases heart triglyceride content but ameliorates lipotoxicity. J. Biol. Chem. 284:36312-36323
75. MartinWHIII, Dalsky GP,Hurley BF, MatthewsDE, Bier DM, et al. 1993. Effect of endurance training on plasma free fatty acid turnover and oxidation during exercise. Am. J. Physiol. 265:E708-14
76. Meex RCR, Schrauwen P, Hesselink MKC. 2009. Modulation of myocellular fat stores: lipid droplet dynamics in health and disease. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297:R913-24
77. Moberg E, Sjoberg S, Hagstrom-Toft E, Bolinder J. 2002. No apparent suppression by insulin of in vivo skeletal muscle lipolysis in nonobese women. Am. J. Physiol. Endocrinol. Metab. 283:E295-301
78. Moro C, Bajpeyi S, Smith SR. 2008. Determinants of intramyocellular triglyceride turnover: implications for insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 294:E203-13
79. Moro C, Galgani JE, Luu L, Pasarica M, Mairal A, et al. 2009. Influence of gender, obesity, and muscle lipase activity on intramyocellular lipids in sedentary individuals. J. Clin. Endocrinol. Metab. 94:3440-3447
80. Muoio DM, Dohm GL, Tapscott EB, Coleman RA. 1999. Leptin opposes insulin's effects on fatty acid partitioning in muscles isolated from obese ob/ob mice. Am. J. Physiol. Endocrinol. Metab. 276:E913-21
81. Olofsson SO, Bostr ̈om P, Andersson L, Rutberg M, Perman J, Boŕen J. 2009. Lipid droplets as dynamic organelles connecting storage and efflux of lipids. Biochim. Biophys. Acta 1791:448-458
82. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, et al. 1997. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46:983-988
83. Pehleman TL, Peters SJ, Heigenhauser GJ, Spriet LL. 2005. Enzymatic regulation of glucose disposal in human skeletal muscle after a high-fat, low-carbohydrate diet. J. Appl. Physiol. 98:100-107
84. Peters SJ, Harris RA, Wu P, Pehleman TL, Heigenhauser GJ, Spriet LL. 2001. Human skeletal muscle PDHkinase activity and isoform expression during a 3-day high-fat/low-carbohydrate diet. Am. J. Physiol. Endocrinol. Metab. 281:E1151-58
85. Petersen KF, Dufour S, Befroy D, Lehrke M, Hendler RE, Shulman GI. 2005. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes 54:603-608
86. Phillips DI, Caddy S, Ilic V, Fielding BA, Frayn KN, et al. 1996. Intramuscular triglyceride and muscle insulin sensitivity: evidence for a relationship in nondiabetic subjects. Metabolism 45:947-950
87. Phillips SM, Green HJ, Tarnopolsky MA, Heigenhauser GF, Hill RE, Grant SM. 1996. Effects of training duration on substrate turnover and oxidation during exercise. J. Appl. Physiol. 81:2182-2191
88. Prats C, Donsmark M, Qvortrup K, Londos C, Sztalryd C, et al. 2006. Decrease in intramuscular lipid droplets and translocation of HSL in response to muscle contraction and epinephrine. J. Lipid Res. 47:2392-2399
89. Pruchnic R, Katsiaras A, He J, Kelley DE, Winters C, Goodpaster BH. 2004. Exercise training increases intramyocellular lipid and oxidative capacity in older adults. Am. J. Physiol. Endocrinol. Metab. 287:E857-62
90. Rabol R, Svendsen PF, Skovbro M, Boushel R, Haugaard SB, et al. 2009. Reduced skeletal muscle mitochondrial respiration and improved glucose metabolism in nondiabetic obese women during a very low calorie dietary intervention leading to rapid weight loss. Metabolism 58:1145-1152
91. Randle PJ,Garland PB, Hales CN, Newsholme EA. 1963. The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1:785-789
92. Roepstorff C, Donsmark M, Thiele M, Vistisen B, Stewart G, et al. 2006. Sex differences in hormonesensitive lipase expression, activity, and phosphorylation in skeletal muscle at rest and during exercise. Am. J. Physiol. Endocrinol. Metab. 291:E1106-14
93. Roepstorff C, Vistisen B, Donsmark M, Nielsen JN, Galbo H, et al. 2004. Regulation of hormonesensitive lipase activity and Ser563 and Ser565 phosphorylation in human skeletal muscle during exercise. J. Physiol. 560:551-562
94. Sacchetti M, Saltin B, Osada T, Van HG. 2002. Intramuscular fatty acid metabolism in contracting and non-contracting human skeletal muscle. J. Physiol. 540:387-395
95. Schenk S, Horowitz JF. 2007. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J. Clin. Invest. 117:1690-1698
96. Schenk S, Saberi M, Olefsky JM. 2008. Insulin sensitivity: modulation by nutrients and inflammation. J. Clin. Invest. 118:2992-3002
97. Schmitz-Peiffer C, Craig DL, Biden TJ. 1999. 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
98. Schrauwen P, Van Aggel-Leijssen DPC, Hul G, Wagenmakers AJM, Vidal H, et al. 2002. The effect of a 3-month low-intensity endurance training program on fat oxidation and acetyl-CoA carboxylase-2 expression. Diabetes 51:2220-2226
99. Schrauwen-HinderlingVB, SchrauwenP,HesselinkMKC, vanEngelshoven JMA, Nicolay K, et al. 2003. The increase in intramyocellular lipid content is a very early response to training. J. Clin. Endocrinol. Metab. 88:1610-1616
100. Schrauwen-Hinderling VB, Van Loon LJ, Koopman R, Nicolay K, SarisWH, Kooi ME. 2003. Intramyocellular lipid content is increased after exercise in nonexercising human skeletal muscle. J. Appl. Physiol. 95:2328-2332
101. Schrauwen-Hinderling VB, Kooi ME, Hesselink MKC, Moonen-Kornips E, Schaart G, et al. 2005. Intramyocellular lipid content and molecular adaptations in response to a 1-week high-fat diet. Obesity 13:2088-2094
102. Shaw CS, Jones DA, Wagenmakers AJ. 2008. Network distribution of mitochondria and lipid droplets in human muscle fibres. Histochem. Cell Biol. 129:65-72
103. Shaw CS, SherlockM, Stewart PM,Wagenmakers AJ. 2009. Adipophilin distribution and colocalization with lipid droplets in skeletal muscle. Histochem. Cell Biol. 131:575-581
104. Shulman GI. 2000. Cellular mechanisms of insulin resistance. J. Clin. Invest. 106:171-176
105. Sollner TH. 2007. Lipid droplets highjack SNAREs. Nat. Cell Biol. 9:1219-1220
106. Solomon TP, Sistrun SN, Krishnan RK, Del Aguila LF, Marchetti CM, et al. 2008. Exercise and diet enhance fat oxidation and reduce insulin resistance in older obese adults. J. Appl. Physiol. 104:1313-1319
107. Stannard SR, ThompsonMW, Fairbairn K, Huard B, Sachinwalla T, Thompson CH. 2002. Fasting for 72 h increases intramyocellular lipid content in nondiabetic, physically fit men. Am. J. Physiol. Endocrinol. Metab. 283:E1185-91
108. Starling RD, Trappe TA, Parcell AC, Kerr CG, Fink WJ, Costill DL. 1997. Effects of diet on muscle triglyceride and endurance performance. J. Appl. Physiol. 82:1185-1189
109. Steffensen CH, Roepstorff C, Madsen M, Kiens B. 2002. Myocellular triacylglycerol breakdown in females but not in males during exercise. Am. J. Physiol. Endocrinol. Metab. 282:E634-42
110. Stellingwerff T, Boon H, Gijsen AP, Stegen JH, Kuipers H, Van Loon LJ. 2007. Carbohydrate supplementation during prolonged cycling exercise sparesmuscle glycogen but does not affect intramyocellular lipid use. Pflugers Arch. 454:635-647
111. Stellingwerff T, Boon H, JonkersRA, Senden JM, Spriet LL, et al. 2007. Significant intramyocellular lipid use during prolonged cycling in endurance-trained males as assessed by three different methodologies. Am. J. Physiol. Endocrinol. Metab. 292:E1715-23
112. Stettler R, Ith M, Acheson KJ, Decombaz J, Boesch C, et al. 2005. Interaction between dietary lipids and physical inactivity on insulin sensitivity and on intramyocellular lipids in healthy men. Diabetes Care 28:1404-1409
113. Stevenson EJ, Thelwall PE, Thomas K, Smith F, Brand-Miller J, Trenell MI. 2009. Dietary glycemic index influences lipid oxidation but notmuscle or liver glycogen oxidation during exercise.Am. J. Physiol. Endocrinol. Metab. 296:E1140-47
114. Sztalryd C, Xu G, Dorward H, Tansey JT, Contreras JA, et al. 2003. Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation. J. Cell Biol. 161:1093-1103
115. Takeuchi K, Reue K. 2009. Biochemistry, physiology, and genetics of GPAT, AGPAT, and lipin enzymes in triglyceride synthesis. Am. J. Physiol. Endocrinol. Metab. 296:E1195-209
116. Tamura Y, Tanaka Y, Sato F, Choi JB, Watada H, et al. 2005. Effects of diet and exercise on muscle and liver intracellular lipid contents and insulin sensitivity in type 2 diabetic patients. J. Clin. Endocrinol. Metab. 90:3191-3196
117. Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC, 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:R1271-78
118. Thrush AB, Brindley DN, Chabowski A, Heigenhauser GJ, Dyck DJ. 2009. Skeletal muscle lipogenic protein expression is not different between lean and obese individuals; a potential factor in ceramide accumulation. J. Clin. Endocrinol. Metab. 94:5053-5061
119. Trenell MI, Stevenson E, Stockmann K, Brand-Miller J. 2008. Effect of high and low glycaemic index recovery diets on intramuscular lipid oxidation during aerobic exercise. Br. J. Nutr. 99:326-332
120. Van Loon LJ. 2004. Use of intramuscular triacylglycerol as a substrate source during exercise in humans. J. Appl. Physiol. 97:1170-1187
121. Van Loon LJ, Greenhaff PL, Constantin-Teodosiu D, Saris WH, Wagenmakers AJ. 2001. The effects of increasing exercise intensity on muscle fuel utilisation in humans. J. Physiol. 536:295-304
122. Van Loon LJ, Koopman R, Manders R, Van Der Weegen W, Van Kranenburg GP, Keizer HA. 2004. Intramyocellular lipid content in type 2 diabetes patients compared with overweight sedentary men and highly trained endurance athletes. Am. J. Physiol. Endocrinol. Metab. 287:E558-65
123. Van Loon LJ, Koopman R, Stegen JH, Wagenmakers AJ, Keizer HA, SarisWH. 2003. Intramyocellular lipids form an important substrate source during moderate intensity exercise in endurance-trained males in a fasted state. J. Physiol. 553:611-625
124. Van Loon LJ, Manders RJ, Koopman R, Kaastra B, Stegen JH, et al. 2005. Inhibition of adipose tissue lipolysis increases intramuscular lipid use in type 2 diabetic patients. Diabetologia 48:2097-2107 (Pubitemid 41416922)
125. Van Loon LJ, Schrauwen-Hinderling VB, Koopman R, Wagenmakers AJ, Hesselink MK, et al. 2003. Influence of prolonged endurance cycling and recovery diet on intramuscular triglyceride content in trained males. Am. J. Physiol. Endocrinol. Metab. 285:E804-11
126. Van Loon LJ, Thomason-Hughes M, Constantin-Teodosiu D, Koopman R, Greenhaff PL, et al. 2005. Inhibition of adipose tissue lipolysis increases intramuscular lipid and glycogen use in vivo in humans. Am. J. Physiol. Endocrinol. Metab. 289:E482-93
127. Varma V, Yao-Borengasser A, Rasouli N, Nolen GT, Phanavanh B, et al. 2009. Muscle inflammatory response and insulin resistance: synergistic interaction between macrophages and fatty acids leads to impaired insulin action. Am. J. Physiol. Endocrinol. Metab. 296:E1300-10
128. Vessby B,Unsitupa M, HermansenK,Riccardi G, Rivellese AA, et al. 2001. Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: the KANWU Study. Diabetologia 44:312-319
129. Vogt M, Puntschart A, Howald H, Mueller B, Mannhart C, et al. 2003. Effects of dietary fat on muscle substrates, metabolism, and performance in athletes. Med. Sci. Sports Exerc. 35:952-960
130. Walther TC, Farese J. 2009. The life of lipid droplets. Biochim. Biophys. Acta 1791:459-466
131. Watt MJ. 2009. Storing up trouble: Does accumulation of intramyocellular triglyceride protect skeletal muscle from insulin resistance? Clin. Exp. Pharmacol. Physiol. 36:5-11
132. Watt MJ, Heigenhauser GJ, Dyck DJ, Spriet LL. 2002. Intramuscular triacylglycerol, glycogen and acetyl group metabolism during 4 h of moderate exercise in man. J. Physiol. 541:969-978
133. Watt MJ, Heigenhauser GJ, O'Neill M, Spriet LL. 2003. Hormone-sensitive lipase activity and fatty acyl-CoA content in human skeletal muscle during prolonged exercise. J. Appl. Physiol. 95:314-321
134. Watt MJ,Heigenhauser GJ, Spriet LL. 2002. Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: Is there a controversy? J. Appl. Physiol. 93:1185-1195
135. Watt MJ, Heigenhauser GJ, Spriet LL. 2003. Effects of dynamic exercise intensity on the activation of hormone-sensitive lipase in human skeletal muscle. J. Physiol. 547:301-308
136. Watt MJ, Holmes AG, Pinnamaneni SK, Garnham AP, Steinberg GR, et al. 2006. Regulation of HSL serine phosphorylation in skeletalmuscle and adipose tissue.Am. J. Physiol. Endocrinol.Metab. 290:E500-8
137. Watt MJ, Holmes AG, Steinberg GR, Mesa JL, Kemp BE, Febbraio MA. 2004. Reduced plasma FFA availability increases net triacylglycerol degradation, but not GPAT or HSL activity, in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 287:E120-27
138. Watt MJ, Krustrup P, Secher NH, Saltin B, Pedersen BK, Febbraio MA. 2004. Glucose ingestion blunts hormone-sensitive lipase activity in contracting human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 286:E144-50
139. Watt MJ, Steinberg GR, Chan S, Garnham A, Kemp BE, Febbraio MA. 2004. Beta-adrenergic stimulation of skeletal muscle HSL can be overridden by AMPK signaling. FASEB J. 18:1445-1446
140. Wendel AA, Lewin TM, Coleman RA. 2009. Glycerol-3-phosphate acyltransferases: rate limiting enzymes of triacylglycerol biosynthesis. Biochim. Biophys. Acta 1791:501-506
141. Wolins NE, Brasaemle DL, Bickel PE. 2006. A proposed model of fat packaging by exchangeable lipid droplet proteins. FEBS Lett. 580:5484-5491
142. Yu C, Chen Y, Cline GW, ZhangD, ZongH, et al. 2002. 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
143. Zderic TW, Davidson CJ, Schenk S, Byerley LO, Coyle EF. 2004. High-fat diet elevates resting intramuscular triglyceride concentration and whole body lipolysis during exercise. Am. J. Physiol. Endocrinol. Metab. 286:E217-25
144. Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner-Gruenberger R, et al. 2004. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306:1383-1386