Intramyocellular lipid content in human skeletal muscle

Obesity

Volumn 14, Issue 3, 2006, Pages 357-367

  Schrauwen Hinderling, Vera B ^a,b   Hesselink, Matthijs K C ^b   Schrauwen, Patrick ^b   Kooi, Marianne Eline ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; LIPID;

BLOOD; ENDURANCE; EXERCISE; FAT INTAKE; HUMAN; INSULIN RESISTANCE; LIPID METABOLISM; METABOLISM; MUSCLE CELL; PHYSIOLOGY; REVIEW; SKELETAL MUSCLE;

DIETARY FATS; EXERCISE; FATTY ACIDS; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; LIPIDS; MUSCLE FIBERS; MUSCLE, SKELETAL; PHYSICAL ENDURANCE;

EID: 33749170655     PISSN: 19307381     EISSN: 1930739X     Source Type: Journal    
DOI: 10.1038/oby.2006.47     Document Type: Article

References (111)

1. Greene CW. The storage of fat in the muscular tissue of the King salmon and its resorption during the fast of the spawning migration. Bull Bur Fisheries. 1913:33:73-138.
2. Morgan TE, Short FA, Cobb LA. Effect of long-term exercise on skeletal muscle lipid composition. Am J Physiol. 1969;216:82-6.
3. Hoppeler H, Luthi P, Claassen H, Weibel ER, Howald H. The ultrastructure of the normal human skeletal muscle: a morphometric analysis on untrained men, women and well-trained orienteers. Pflugers Arch. 1973;344:217-32.
4. Jerusalem F, Engel AG, Peterson HA. Human muscle fiber fine structure: morphometric data on controls. Neurology. 1975;25:127-34.
5. Hoppeler H. Exercise-induced ultrastructural changes in skeletal muscle. Int J Spurts Med. 1986;7:187-204.
6. Havel RJ, Carlson LA, Ekelund LG, Holmgren A. Turnover rate and oxidation of different free fatty acids in man during exercise. J Appl Physiol. 1964;19:613-8.
7. Havel RJ, Pernow B, Jones NL. Uptake and release of free fatty acids and other metabolites in the legs of exercising men. J Appl Physiol. 1967;23:90-9.
8. Issekutz B Jr, Issekutz AC, Nash D. Mobilization of energy sources in exercising dogs. J Appl Physiol. 1970;29:691-7.
9. Steffensen CH, Roepstorff C, Madsen M, Kiens B. Myocellular triacylglycerol breakdown in females but not in males during exercise. Am J Physiol Endocrinol Metab. 2002;282:E634-42.
10. Krssak M, Falk Petersen K, Dresner A, et al. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia. 1999;42:113-6.
11. 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. 2001;86:5755-61.
12. Pan DA, Lillioja S, Kriketos AD, et al. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes. 1997;46:983-8.
13. van Loon LJ. Use of intramuscular triacylglycerol as a substrate source during exercise in human.s. J Appl Physiol. 2004;97:1170-87.
14. Watt MJ, Heigenhauser GJ, Spriet LL. Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: is there a controversy? J Appl Physiol. 2002;93:1185-95.
15. Stannard SR, Johnson NA. Insulin resistance and elevated triglyceride in muscle: more important for survival than "thrifty" genes? J Physiol. 2004;554:595-607.
16. Goodpaster BH, Wolf D. Skeletal muscle lipid accumulation in obesity, insulin resistance, and type 2 diabetes. Pediatr Diabetes. 2004;5:219-26.
17. Russell AP. Lipotoxicity: the obese and endurance-trained paradox. Int J Oben Relat Metab Disord. 2004;28(Suppl 4):S66-71.
18. Machann J, Haring H, Schick F, Stunivoll M. Intramyocellular lipids and insulin resistance. Diabetes Obes Metab. 2004;6:239-48.
19. Schrauwen P, Hesselink MK. Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes. 2004:53:1412-7.
20. Krssak M, Roden M. The role of lipid accumulation in liver and muscle for insulin resistance and type 2 diabetes mellitus in humans. Rev Endocr Metab Disord. 2004;5:127-34.
21. Kelley DE. Influence of weight loss and physical activity interventions upon muscle lipid content in relation to insulin resistance. Curr Diab Rep. 2004;4:165-8.
22. Wendung PS, Peters SJ, Heigenhauser GJ, Spriet LL. Variability of triacylglycerol content in human skeletal muscle biopsy samples. J Appl Physiol. 1996;81:1150-5.
23. 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. 2003;95:314-21.
24. Guo Z, Mishra P, Macura S. Sampling the intramyocellular triglycerides from skeletal muscle. J Lipid Res. 2001;42:1041-8.
25. Howald H, Boesch C, Kreis R, et al. Content of intramyocellular lipids derived by electron microscopy, biochemical assays, and (1)H-MR spectroscopy. J Appl Physiol. 2002;92:2264-72.
26. Thornell LE, Carlsson E, Kugelberg E, Grove BK. Myofibrillar M-band structure and composition of physiologically defined rat motor units. Am J Physiol. 1987;253:C456-68.
27. Bayliss-High O. Theory and Practice of Histological Techniques. Edinburgh, UK: Churchill Livingstone; 1977, pp. 168-85.
28. Goodpaster BH, Theriault R, Watkins SC, Kelley DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism. 2000;49:467-72.
29. Koopman R, Schaart G, Hesselink MK. Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem Cell Biol. 2001;116:63-8.
30. Schick F, Eismann B, Jung WI, Bongers H, Bunse M, Lutz O. Comparison of localized proton NMR signals of skeletal muscle and fat tissue in vivo: two lipid compartments in muscle tissue. Magn Reson Med. 1993;29:158-67.
31. Boesch C, Slotboom J, Hoppeler H, Kreis R. In vivo determination of intra-myocellular lipids in human muscle by means of localized 1H-MR-spectroscopy. Magn Reson Med. 1997;37:484-93.
32. Szczepaniak LS, Dobbins RL, Stein DT, McGarry JD. Bulk magnetic susceptibility effects on the assessment of intra- and extramyocellular lipids in vivo. Magn Reson Med. 2002;47:607-10.
33. Schrauwen-Hinderling VB, Schrauwen P, Hesselink MK, et al. The increase in intramyocellular lipid content is a very early response to training. J Clin Endocrinol Metab. 2003;88:1610-6.
34. Rico-Sanz J, Hajnal JV, Thomas EL, Mierisova S, Ala-Korpela M, Bell JD. Intracellular and extracellular skeletal muscle triglyceride metabolism during alternating intensity exercise in humans. J Physiol (Lond). 1998;510:615-22.
35. Szczepaniak LS, Babcock EE, Schick F, et al. Measurement of intracellular triglyceride stores by H spectroscopy: validation in vivo. Am J Physiol. 1999;276:E977-89.
36. Brechtel K, Machann J, Jacob S, et al. In-vivo 1H-MR spectroscopy: the determination of the intra- and extramyocellular lipid content depending on the insulin effect in the direct offspring of type-2 diabetics. Rofo. 1999;171:113-20.
37. Arrowsmith FE, Ward J, Rooney K, Kriketos AD, Baur LA, Thompson CH. Body fatness, insulin sensitivity and muscle oxygen supply in adolescents. Clin Sci (Lond). 2002;103:391-6.
38. Vermathen P, Kreis R, Boesch C. Distribution of intramyocellular lipids in human calf muscles as determined by MR spectroscopic imaging. Magn Reson Med. 2004;51:253-62.
39. Goodpaster BH, Stenger VA, Boada F, et al. Skeletal muscle lipid concentration quantified by magnetic resonance imaging. Am J Clin Nutr. 2004;79:748-54.
40. Schick F, Machann J, Brechtel K, et al. MRI of muscular fat. Magn Reson Med. 2002;47:720-7.
41. Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R. Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol. 2000;89:104-10.
42. van Loon LJ, Schrauwen-Hinderling VB, Koopman R, et al. Influence of prolonged endurance cycling and recovery diet on intramuscular triglyceride content in trained males. Am J Physiol Endocrinol Metab. 2003;285:E804-11.
43. Carlson LA, Ekelund LG, Froberg SO. Concentration of triglycerides, phospholipids and glycogen in skeletal muscle and of free fatty acids and beta-hydroxybutyric acid in blood in man in response to exercise. Eur J Clin Invest. 1971;1:248-54.
44. Bergstrom J, Hultman E, Saltin B. Muscle glycogen consumption during cross-country skiing (the Vasa ski race). Int Z Angew Physiol. 1973;31:71-5.
45. Cleroux J, Van Nguyen P, Taylor AW, Leenen FH. Effects of beta 1- vs. beta 1 + beta 2-blockade on exercise endurance and muscle metabolism in humans. J Appl Physiol. 1989;66:548-54.
46. Costill DL, Gollnick PD, Jansson ED, Saltin B, Stein EM. Glycogen depletion pattern in human muscle fibres during distance running. Acta Physiol Scand. 1973;89:374-83.
47. Essen B, Jansson E, Henriksson J, Taylor AW, Saltin B. Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiol Scand. 1975;95:153-65.
48. Froberg SO, Mossfeldt F. Effect of prolonged strenuous exercise on the concentration of triglycerides, phospholipids and glycogen in muscle of man. Acta Physiol Scand. 1971;82:167-71.
49. Watt MJ, Heigenhauser GJ, Dyck DJ, Spriet LL. Intramuscular triacylglycerol, glycogen and acetyl group metabolism during 4 h of moderate exercise in man. J Physiol. 2002;541:969-78.
50. Essen-Gustavsson B, Tesch PA. Glycogen and triglyceride utilization in relation to muscle metabolic characteristics in men performing heavy-resistance exercise. Eur J Appl Physiol Occup Physiol. 1990;61:5-10.
51. Hurley BF, Nemeth PM, Martin WH 3rd, Hagberg JM, Dalsky GP, Holloszy JO. Muscle triglyceride utilization during exercise: effect of training. J Appl Physiol. 1986;60:562-7.
52. Kiens B, Richter EA. Utilization of skeletal muscle triacylglycerol during postexercise recovery in humans. Am J Physiol. 1998;275:E332-7.
53. Roepstorff C, Steffensen CH, Madsen M, et al. Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects. Am J Physiol Endocrinol Metab. 2002;282:E435-47.
54. Starling RD, Trappe TA, Parcell AC, Kerr CG, Fink WJ, Costill DL. Effects of diet on muscle triglyceride and endurance performance. J Appl Physiol. 1997;82:1185-9.
55. Staron RS, Hikida RS, Murray TF, Hagerman FC, Hagerman MT. Lipid depletion and repletion in skeletal muscle following a marathon. J Neural Sci. 1989;94:29-40.
56. Kayar SR, Hoppeler H, Howald H, Claassen H, Oberholzer F. Acute effects of endurance exercise on mitochondrial distribution and skeletal muscle morphology. Eur J Appl Physiol Occup Physiol. 1986;54:578-84.
57. Boesch C, Decombaz J, Slotboom J, Kreis R. Observation of intramyocellular lipids by means of 1H magnetic resonance spectroscopy. Proc Nutr Soc. 1999;58:841-50.
58. Krssak M, Petersen KF, Bergeron R, et al. 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. 2000;85:748-54.
59. Rico-Sanz J, Moosavi M, Thomas EL, et al. In vivo evaluation of the effects of continuous exercise on skeletal muscle triglycerides in trained humans. Lipids. 2000;35:1313-8.
60. Brechtel K, Niess AM, Machann J, et al. Utilisation of intramyocellular lipids (IMCLs) during exercise as assessed by proton magnetic resonance spectroscopy (1H-MRS). Horm Metab Res. 2001;33:63-6.
61. Decombaz J, Schmitt B, Ith M, et al. Postexercise fat intake repletes intramyocellular lipids but no faster in trained than in sedentary subjects. Am J Physiol Regul Integr Comp Physiol. 2001;281:R760-9.
62. Larson-Meyer DE, Newcomer BR, Hunter GR. Influence of endurance running and recovery diet on intramyocellular lipid content in women: a 1H NMR study. Am J Physiol Endocrinol Metab. 2002;282:E95-E106.
63. Schrauwen-Hinderling VB, van Loon LJ, Koopman R, Nicolay K, Saris WH, Kooi ME. Intramyocellular lipid content is increased after exercise in nonexercising human skeletal muscle. J Appl Physiol. 2003;95:2328-32.
64. White LJ, Robergs RA, Sibbitt WL Jr, Ferguson MA, McCoy S, Brooks WM. Effects of intermittent cycle exercise on intramyocellular lipid use and recovery. Lipids. 2003;38:9-13.
65. Hwang JH, Pan JW, Heydari S, Hetherington HP, Stein DT. Regional differences in intramyocellular lipids in humans observed by in vivo 1H-MR spectroscopic imaging. J Appl Physiol. 2001;90:1267-74.
66. Johnson MA, Polgar J, Weightman D, Appleton D. Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neural Sci. 1973;18:111-29.
67. Howald H, Hoppeler H, Claassen H, Mathieu O, Straub R. Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflugers Arch. 1985;403:369-76.
68. 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 rnen and highly trained endurance athletes. Am J Physiol Endocrinol Metab. 2004;287:E558-65.
69. Decombaz J, Fleith M, Hoppeler H, Kreis R, Boesch C. Effect of diet on the replenishment of intramyocellular lipids after exercise. Eur J Nutr. 2000;39:244-7.
70. Lambert EV, Speechly DP, Dennis SC, Noakes TD. Enhanced endurance in trained cyclists during moderate intensity exercise following 2 weeks adaptation to a high fat diet. Eur J Appl Physiol Occup Physiol. 1994;69:287-93.
71. O'Keefe KA, Keith RE, Wilson GD, Blessing DL. Dietary carbohydrate intake and endurance exercise performance of trained female cyclists. Nutr Res. 1989;9:819-30.
72. Phinney SD, Bistrian BR, Evans WJ, Gervino E, Blackburn GL. The human metabolic response to chronic ketosis without caloric restriction: preservation of submaximal exercise capability with reduced carbohydrate oxidation. Metabolism. 1983;32:769-76.
73. Goedecke JH, Christie C, Wilson G, et al. Metabolic adaptations to a high-fat diet in endurance cyclists. Metabolism. 1999;48:1509-17.
74. Rowlands DS, Hopkins WG. Effects of high-fat and high-carbohydrate diets on metabolism and performance in cycling. Metabolism. 2002;51:678-90.
75. Burke LM, Kiens B, Ivy JL. Carbohydrates and fat for training and recovery. J Sports Sci. 2004;22:15-30.
76. Phillips SM, Green HJ, Tarnopolsky MA, Heigenhauser GJ, Grant SM. Progressive effect of endurance training on metabolic adaptations in working skeletal muscle. Am J Physiol. 1996;270:E265-72.
77. Bergman BC, Butterfield GE, Wolfel EE, Casazza GA, Lopaschuk GD, Brooks GA. Evaluation of exercise and training on muscle lipid metabolism. Am J Physiol. 1999;276:E106-17.
78. Trendafilov B, Tanuschev M. Morphometrische Untersuchungen an Skelettmuskeln von Wettkaempfern im Rudern. Med Sport. 1981;21:264-8.
79. Kiessling KH, Pilstrom L, Bylund AC, Saltin B, Piehl K. Enzyme activities and morphometry in skeletal muscle of middle-aged men after training. Scand J Clin Lab Invent. 1974;33:63-9.
80. Hoppeler H, Howald H, Conley K, et al. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol. 1985;59:320-7.
81. Orlander J, Aniansson A. Effect of physical training on skeletal muscle metabolism and ultrastructure in 70- to 75-year-old men. Acta Physiol Scand. 1980;109:149-54.
82. Rosier K, Hoppeler H, Conley KE, Claassen H, Gehr P, Howald H. Transfer effects in endurance exercise: adaptations in trained and untrained muscles. Eur J Appl Physiol Occup Physiol. 1985;54:355-62.
83. Alway SE, MacDougall JD, Sale DG, Sutton JR, McComas AJ. Functional and structural adaptations in skeletal muscle of trained athletes. J Appl Physiol. 1988;64:1114-20.
84. Prince FP, Hikida RS, Hagerman FC, Staron RS, Allen WH. A morphometric analysis of human muscle fibers with relation to fiber types and adaptations to exercise. J Neural Sci. 1981;49:165-79.
85. Staron RS, Hikida RS, Hagerman FC, Dudley GA, Murray TF. Human skeletal muscle fiber type adaptability to various workloads. J Histochem Cytochem. 1984;32:146-52.
86. Friden J, Sjöström M, Ekblom B. Muscle fibre type characteristics in endurance trained and untrained individuals. Eur J Appl Physiol Occup Physiol. 1984;52:266-71.
87. Pruchnic R, Katsiaras A, He J, Winters C, Kelley DE, Goodpaster BH. Exercise training increases intramyocellular lipid and oxidative capacity in older adults. Am J Physiol Endocrinol Metab. 2004;287:E857-62.
88. Thamer C, Machann J, Bachmann O, et al. Intramyocellular lipids: anthropometric determinants and relationships with maximal aerobic capacity and insulin sensitivity. J Clin Endocrinol Metab. 2003;88:1785-91.
89. Helge JW, Wulff B, Kiens B. Impact of a fat-rich diet on endurance in man: role of the dietary period. Med Sci Sports Exerc. 1998;30:456-61.
90. Helge JW, Watt PW, Richter EA, Rennie MJ, Kiens B. 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. 2001;537:1009-20.
91. 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. 2003;286:E217-25.
92. 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. 1987;7:1-9.
93. Jansson E, Kaijser L. Effect of diet on muscle glycogen and blood glucose utilization during a short-term exercise in man. Acta Physiol Scand. 1982;115:341-7.
94. Vogt M, Puntschart A, Howald H, et al. Effects of dietary fat on muscle substrates, metabolism, and performance in athletes. Med Sci Sports Exerc. 2003;35:952-60.
95. Bachmann OP, Dahl DB, Brechtel K, et al. Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes. 2001;50:2579-84.
96. Johnson NA, Stannard SR, Mehalski K, et al. Intramyocellular triacylglycerol in prolonged cycling with high- and low-carbohydrate availability. J Appl Physiol. 2003;94:1365-72.
97. Schrauwen-Hinderling VB, Kooi ME, Hesselink MKC, et al. Intramyocellular lipid content and molecular adaptations in response to a 1-week high-fat diet. Obes Res. 2005;13:2088-94.
98. Schrauwen P, Wagenmakers AJ, van Marken Lichtenbelt WD, Saris WH, Westerterp KR. Increase in fat oxidation on a high-fat diet is accompanied by an increase in triglyceride-derived fatty acid oxidation. Diabetes. 2000;49:640-6.
99. Perseghin G, Scifo P, Danna M, et al. Normal insulin sensitivity and IMCL content in overweight humans are associated with higher fasting lipid oxidation. Am J Physiol Endocrinol Metab. 2002;283:E556-64.
100. 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. 2001;50:1612-7.
101. Stannard SR, Thompson MW, Fairbairn K, Huard B, Sachinwalla T, Thompson CH. Fasting for 72 h increases intramyocellular lipid content in nondiabetic, physically fit men. Am J Physiol Endocrinol Metab. 2002;283:E1185-91.
102. Phillips DI, Caddy S, Ilic V, et al. Intramuscular triglyceride and muscle insulin sensitivity: evidence for a relationship in nondiabetic subjects. Metabolism. 1996;45:947-50.
103. Perseghin G, Scifo P, De Cobelli F, et al. 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. 1999;48:1600-6.
104. Jacob S, Machann J, Rett K, et al. Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes. 1999;48:1113-9.
105. Falholt K, Jensen I, Lindkaer Jensen S, et al. Carbohydrate and lipid metabolism of skeletal muscle in type 2 diabetic patients. Diabet Med. 1988;5:27-31.
106. Gray RE, Tanner CJ, Pories WJ, MacDonald KG, Houmard JA. Effect of weight loss on muscle lipid content in morbidly obese subjects. Am J Physiol Endocrinol Metab. 2003;284:E726-32.
107. Greco AV, Mingrone G, Giancaterini A, et al. Insulin resistance in morbid obesity: reversal with intramyocellular fat depletion. Diabetes. 2002;51:144-51.
108. Tunstall RJ, Mehan KA, Wadley GD, et al. Exercise training increases lipid metabolism gene expression in human skeletal muscle. Am J Physiol Endocrinol Metab. 2002;283:E66-72.
109. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant off-spring of patients with type 2 diabetes. W Engl J Med. 2004;350:664-71.
110. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest. 2000;106:171-6.
111. Bramble DM, Lieberman DE. Endurance running and the evolution of Homo. Nature. 2004;432:345-52.