Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: Is there a controversy?

Journal of Applied Physiology

Volumn 93, Issue 4, 2002, Pages 1185-1195

  Watt, Matthew J ^a   Heigenhauser, George J F ^b   Spriet, Lawrence L ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Fat metabolism; Hydrogen 1 magnetic resonance spectroscopy; Isotope tracer; Muscle biopsy

Indexed keywords

ISOTOPE; TRIACYLGLYCEROL;

CALORIMETRY; CONTROLLED STUDY; EXERCISE; FATTY ACID METABOLISM; FATTY ACID OXIDATION; HUMAN; HUMAN TISSUE; ISOTOPE TRACING; LIPID METABOLISM; MUSCLE BIOPSY; MUSCLE CONTRACTION; MUSCLE METABOLISM; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SKELETAL MUSCLE;

EID: 0036785028     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.00197.2002     Document Type: Review

References (86)

1. Asmussen E. Muscle metabolism during exercise in man: a historical survey. In: Advances in Experimental Medicine and Biology, edited by Pernow B and Saltin B. New York: Plenum, 1971, p. 1-12.
2. Bachmann OP, Dahl DB, Brechtel K, Machann J, Haap M, Maier T, Loviscach M, Stumvoll M, Claussen CD, Schick F, Haring HU, and 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.
3. Bergman BC and Brooks GA. Respiratory gas-exchange ratios during graded exercise in fed and fasted trained and untrained men. J Appl Physiol 86: 479-487, 1999.
4. Bergman BC, Butterfield GE, Wolfel EE, Casazza GA, Lopaschuk GD, and Brooks GA. Evaluation of exercise and training on muscle lipid metabolism. Am J Physiol Endocrinol Metab 276: E106-E117, 1999.
5. Bergström J, Hultman E, and Saltin B. Muscle glycogen consumption during cross-country skiing (the Vasa ski race). Int Z Angew Physiol Einschl Arbeitsphysiol 31: 71-75, 1973.
6. Boden G, Lebed B, Schatz M, Homko C, and Lemieux S. Effects of acute changes of plasma free fatty acids on intramyo-cellular fat content and insulin resistance in healthy subjects. Diabetes 50: 1612-1617, 2001.
7. 1H magnetic resonance spectroscopy. Proc Nutr Soc 58: 841-850, 1999.
8. 1H-MR-spectroscopy. Magn Reson Med 37: 484-493, 1997.
9. 1H-MRS). Horm Metab Res 33: 63-66, 2001.
10. Carey AL, Staudacher HM, Cummings NK, Stepto NK, Nikolopoulos V, Burke LM, and Hawley JA. Effects of fat adaptation and carbohydrate restoration on prolonged endurance exercise. J Appl Physiol 91: 115-122, 2001.
11. Carlson LA, Ekelund LG, and 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 1: 248-254, 1971.
12. 2-blockade on exercise endurance and muscle metabolism in humans. J Appl Physiol 66: 548-554, 1989.
13. Costill DL, Gollnick PD, Jansson ED, Saltin B, and Stein EM. Glycogen depletion pattern in human muscle fibres during distance running. Acta Physiol Scand 89: 374-383, 1973.
14. Coyle EF, Jeukendrup AE, Oseto MC, Hodgkinson BJ, and 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.
15. Coyle EF, Jeukendrup AE, Wagenmakers AJ, and Saris WH. Fatty acid oxidation is directly regulated by carbohydrate metabolism during exercise. Am J Physiol Endocrinol Metab 273: E268-E275, 1997.
16. Coyle EF, Jeukendrup AE, Wagenmakers AJ, and Saris WH. Intramuscular triglceride oxidation during exercise acutely increases with reduced plasma FFA mobilization and oxidation (Abstract). FASEB J 10: A143, 1998.
17. Dagenais GR, Tancredi RG, and 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.
18. Décombaz J, Schmitt B, Ith M, Decarli B, Diem P, Kreis R, Hoppeler H, and 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.
19. Dobbins RL, Szczepaniak LS, Bentley B, Esser V, Myhill J, and McGarry JD. Prolonged inhibition of muscle carnitine palmitoyltransferase-1 promotes intramyocellular lipid accumulation and insulin resistance in rats. Diabetes 50: 123-130, 2001.
20. Dyck DJ, Peters SJ, Glatz J, Gorski J, Keizer H, Kiens B, Liu S, Richter EA, Spriet LL, Van Der Vusse GJ, and Bonen A. Functional differences in lipid metabolism in resting skeletal muscle of various fiber types. Am J Physiol Endocrinol Metab 272: E340-E351, 1997.
21. Ebeling P, Essen-Gustavsson B, Tuominen JA, and Koivisto VA. Intramuscular triglyceride content is increased in IDDM. Diabetologia 41: 111-115, 1998.
22. Essen B, Hagenfeldt L, and Kaijser L. Utilization of blood-borne and intramuscular substrates during continuous and intermittent exercise in man. J Physiol 265: 489-506, 1977.
23. Essen B, Jansson E, Henriksson J, Taylor AW, and Saltin B. Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiol Scand 95: 153-165, 1975.
24. Essen-Gustavsson B and Tesch PA. Glycogen and triglyceride utilization in relation to muscle metabolic characteristics in men performing heavy-resistance exercise. Eur J Appl Physiol 61: 5-10, 1990.
25. Febbraio MA, Chiu A, Angus DJ, Arkinstall MJ, and Hawley JA. Effects of carbohydrate ingestion before and during exercise on glucose kinetics and performance. J Appl Physiol 89: 2220-2226, 2000.
26. Frayn KN. Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol 55: 628-634, 1983.
27. Frayn KN and Maycock PF. Skeletal muscle triacylglycerol in the rat: methods for sampling and measurement, and studies of biological variability. J Lipid Res 21: 139-144, 1980.
28. Fredrikson G, Stralfors P, Nilsson NO, and Belfrage P. Hormone-sensitive lipase from adipose tissue of rat. Methods Enzymol 71: 636-646, 1981.
29. Friedlander AL, Casazza GA, Horning MA, Usaj A, and Brooks GA. Endurance training increases fatty acid turnover, but not fat oxidation, in young men. J Appl Physiol 86: 2097-2105, 1999.
30. Fröberg SO and Mossfeldt F. Effect of prolonged strenuous exercise on the concentration of triglycerides, phospholipids and glycogen in muscle of man. Acta Physiol Scand 82: 167-171, 1971.
31. Gollnick PD and Saltin B. Fuel for muscular exercise: role of fat. In: Exercise, Nutrition and Energy Metabolism, edited by Horton ES and Terjung RL. New York: MacMillan, 1988, p. 72-88.
32. Goodpaster BH, He J, Watkins S, and 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.
33. Goodpaster BH, Theriault R, Watkins SC, and Kelley DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 49: 467-472, 2000.
34. Greco AV, Mingrone G, Giancaterini A, Manco M, Morroni M, Cinti S, Granzotto M, Vettor R, Camastra S, and Ferrannini E. Insulin resistance in morbid obesity: reversal with intramyocellular fat depletion. Diabetes 51: 144-151, 2002.
35. Guo Z, Burguera B, and Jensen MD. Kinetics of intramuscular triglyceride fatty acids in exercising humans. J Appl Physiol 89: 2057-2064, 2000.
36. Hagstrom-Toft E, Enoksson S, Moberg E, Bolinder J, and Arner P. β-Adrenergic regulation of lipolysis and blood flow in human skeletal muscle in vivo. Am J Physiol Endocrinol Metab 275: E909-E916, 1998.
37. Havel RJ, Carlson LA, Ekelund LG, and Holmgren A. Turnover rate and oxidation of different free fatty acids in man during exercise. J Appl Physiol 19: 613-618, 1964.
38. Havel RJ, Pernow B, and Jones NL. Uptake and release of free fatty acids and other metabolites in the legs of exercising men. J Appl Physiol 23: 90-99, 1967.
39. He J, Watkins S, and Kelley DE. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 50: 817-823, 2001.
40. Helge JW, Watt PW, Richter EA, Rennie MJ, and 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 537: 1009-1020, 2001.
41. Holm C, Belfrage P, and Fredrikson G. Immunological evidence for the presence of hormone-sensitive lipase in rat tissues other than adipose tissue. Biochem Biophys Res Commun 148: 99-105, 1987.
42. Holm C, Kirchgessner TG, Svenson KL, Fredrikson G, Nilsson S, Miller CG, Shively JE, Heinzmann C, Sparkes RS, and Mohandas T. Hormone-sensitive lipase: sequence, expression, and chromosomal localization to 19 cent-q13.3. Science 241: 1503-1506, 1988.
43. Horowitz JF and Klein S. Lipid metabolism during endurance exercise. Am J Clin Nutr 72: 558S-563S, 2000.
44. Howald H, Hoppeler H, Claassen H, Mathieu O, and Straub R. Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflügers Arch 403: 369-376, 1985.
45. Hurley BF, Nemeth PM, Martin WH III, Hagberg JM, Dalsky GP, and Holloszy JO. Muscle triglyceride utilization during exercise: effect of training. J Appl Physiol 60: 562-567, 1986.
46. Jansson E and Kaijser L. Effect of diet on the utilization of blood-borne and intramuscular substrates during exercise in man. Acta Physiol Scand 115: 19-30, 1982.
47. Jansson E and Kaijser L. Substrate utilization and enzymes in skeletal muscle of extremely endurance-trained men. J Appl Physiol 62: 999-1005, 1987.
48. Kiens B, Essen-Gustavsson B, Christensen NJ, and Saltin B. Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training. J Physiol 469: 459-478, 1993.
49. Kiens B, Essen-Gustavsson B, Gad P, and 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.
50. Kiens B and Richter EA. Utilization of skeletal muscle triacylglycerol during postexercise recovery in humans. Am J Physiol Endocrinol Metab 275: E332-E337, 1998.
51. Kjaer M, Howlett K, Langfort J, Zimmerman-Belsing T, Lorentsen J, Bulow J, Ihlemann J, Feldt-Rasmussen U, and Galbo H. Adrenaline and glycogenolysis in skeletal muscle during exercise: a study in adrenalectomised humans. J Physiol 528: 371-378, 2000.
52. 1H nuclear magnetic resonance spectroscopy study. J Clin Endocrinol Metab 85: 748-754, 2000.
53. Langfort J, Ploug T, Ihlemann J, Holm C, and Galbo H. Stimulation of hormone-sensitive lipase activity by contractions in rat skeletal muscle. Biochem J 351: 207-214, 2000.
54. Langfort J, Ploug T, Ihlemann J, Saldo M, Holm C, and Galbo H. Expression of hormone-sensitive lipase and its regulation by adrenaline in skeletal muscle. Biochem J 340: 459-465, 1999.
55. 1H NMR study. Am J Physiol Endocrinol Metab 282: E95-E106, 2002.
56. Levin K, Daa SH, Alford FP, and Beck-Nielsen H. Morphometric documentation of abnormal intramyocellular fat storage and reduced glycogen in obese patients with Type II diabetes. Diabetologia 44: 824-833, 2001.
57. Malenfant P, Tremblay A, Doucet E, Imbeault P, Simoneau JA, and Joanisse DR. Elevated intramyocellular lipid concentration in obese subjects is not reduced after diet and exercise training. Am J Physiol Endocrinol Metab 280: E632-E639, 2001.
58. Martin WH III, Dalsky GP, Hurley BF, Matthews DE, Bier DM, Hagberg JM, Rogers MA, King DS, and Holloszy JO. Effect of endurance training on plasma free fatty acid turnover and oxidation during exercise. Am J Physiol Endocrinol Metab 265: E708-E714, 1993.
59. Morgan TE, Short FA, and Cobb LA. Effect of long-term exercise on skeletal muscle lipid composition. Am J Physiol 216: 82-86, 1969.
60. Odland LM, Heigenhauser GJ, Lopaschuk GD, and Spriet LL. Human skeletal muscle malonyl-CoA at rest and during prolonged submaximal exercise. Am J Physiol Endocrinol Metab 270: E541-E544, 1996.
61. Odland LM, Heigenhauser GJ, Wong D, Hollidge-Horvat MG, and Spriet LL. Effects of increased fat availability on fat-carbohydrate interaction during prolonged exercise in men. Am J Physiol Regul Integr Comp Physiol 274: R894-R902, 1998.
62. Palmer GS, Borghouts LB, Noakes TD, and Hawley JA. Metabolic and performance responses to constant-load vs. variable-intensity exercise in trained cyclists. J Appl Physiol 87: 1186-1196, 1999.
63. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, and Storlien LH. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46: 983-988, 1997.
64. Peters SJ, Dyck DJ, Bonen A, and Spriet LL. Effects of epinephrine on lipid metabolism in resting skeletal muscle. Am J Physiol Endocrinol Metab 275: E300-E309, 1998.
65. 31P NMR studies on the mechanism of insulin resistance in obesity. Diabetes 47: 381-386, 1998.
66. Phillips SM, Green HJ, Tarnopolsky MA, Heigenhauser GJ, and Grant SM. Progressive effect of endurance training on metabolic adaptations in working skeletal muscle. Am J Physiol Endocrinol Metab 270: E265-E272, 1996.
67. Phillips SM, Green HJ, Tarnopolsky MA, Heigenhauser GF, Hill RE, and Grant SM. Effects of training duration on substrate turnover and oxidation during exercise. J Appl Physiol 81: 2182-2191, 1996.
68. Rico-Sanz J, Hajnal JV, Thomas EL, Mierisova S, Ala-Korpela M, and Bell JD. Intracellular and extracellular skeletal muscle triglyceride metabolism during alternating intensity exercise in humans. J Physiol 510: 615-622, 1998.
69. Rico-Sanz, J, Moosavi M, Thomas EL, McCarthy J, Coutts GA, Saeed N, and Bel JD. In vivo evaluation of the effects of continuous exercise on skeletal muscle triglycerides in trained humans. Lipids 35: 1313-1318, 2000.
70. Roepstorff C, Steffensen CH, Madsen M, Stallknecht B, Kanstrup IL, Richter EA, and Kiens B. Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects. Am J Physiol Endocrinol Metab 282: E435-E447, 2002.
71. Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E, and Wolfe RR. Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol Endocrinol Metab 265: E380-E391, 1993.
72. Schick F, Eismann B, Jung WI, Bongers H, Bunse M, and 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 29: 158-167, 1993.
73. Schrauwen P, Wagenmakers AJ, Marken Lichtenbelt WD, Saris WH, and Westerterp KR. Increase in fat oxidation on a high-fat diet is accompanied by an increase in triglyceride-derived fatty acid oxidation. Diabetes 49: 640-646, 2000.
74. Sidossis LS, Coggan AR, Gastaldelli A, and Wolfe RR. A new correction factor for use in tracer estimations of plasma fatty acid oxidation. Am J Physiol Endocrinol Metab 269: E649-E656, 1995.
75. Sidossis LS, Gastaldelli A, Klein S, and Wolfe RR. Regulation of plasma fatty acid oxidation during low- and high-intensity exercise. Am J Physiol Endocrinol Metab 272: E1065-E1070, 1997.
76. Starling RD, Trappe TA, Parcell AC, Kerr CG, Fink WJ, and Costill DL. Effects of diet on muscle triglyceride and endurance performance. J Appl Physiol 82: 1185-1189, 1997.
77. Staron RS, Hikida RS, Murray TF, Hagerman FC, and Hagerman MT. Lipid depletion and repletion in skeletal muscle following a marathon. J Neurol Sci 94: 29-40, 1989.
78. Steffensen CH, Roepstorff C, Madsen M, and Kiens B. Myocellular triacylglycerol breakdown in females but not in males during exercise. Am J Physiol Endocrinol Metab 282: E634-E642, 2002.
79. Szczepaniak LS, Babcock EE, Schick F, Dobbins RL, Garg A, Burns DK, McGarry JD, and Stein DT. Measurement of intracellular triglyceride stores by H spectroscopy: validation in vivo. Am J Physiol Endocrinol Metab 276: E977-E989, 1999.
80. Van Der Vusse GJ and Reneman RS. Lipid metabolism in muscle. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, chapt. 21, p. 952-994.
81. Van Loon LJ, Greenhaff PL, Constantin-Teodosiu D, Saris WH, and Wagenmakers AJ. The effects of increasing exercise intensity on muscle fuel utilisation in humans. J Physiol 536: 295-304, 2001.
82. Virkamaki A, Korsheninnikova E, Seppala-Lindroos A, Vehkavaara S, Goto T, Halavaara J, Hakkinen AM, and Yki-Jarvinen H. Intramyocellular lipid is associated with resistance to in vivo insulin actions on glucose uptake, antilipolysis, and early insulin signaling pathways in human skeletal muscle. Diabetes 50: 2337-2343, 2001.
83. Watt MJ, Heigenhauser GF, Dyck DJ, and Spriet LL. Intramuscular triacylglycerol, glycogen and acetyl group metabolism during 4 h of moderate exercise. J Physiol 541: 969-978, 2002.
84. Wendling PS, Peters SJ, Heigenhauser GJ, and Spriet LL. Variability of triacylglycerol content in human skeletal muscle biopsy samples. J Appl Physiol 81: 1150-1155, 1996.
85. Wicklmayr M, Dietze G, Rett K, and Mehnert H. Evidence for a substrate regulation of triglyceride lipolysis in human skeletal muscle. Horm Metab Res 17: 471-475, 1985.
86. Zierler KL. Fatty acids as substrates for heart and skeletal muscle. Circ Res 38: 459-463, 1976.