Intramyocellular lipid content in type 2 diabetes patients compared with overweight sedentary men and highly trained endurance athletes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 287, Issue 3 50-3, 2004, Pages

  Van Loon, Luc J C ^a   Koopman, René ^a   Manders, Ralph ^a   Van Der Weegen, Walter ^a   Van Kranenburg, Gerrit P ^a   Keizer, Hans A ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Endurance training; Insulin resistance; Intramuscular fat; Intramuscular triacylglycerol

Indexed keywords

GLUCOSE; INSULIN; LIPID; TRIACYLGLYCEROL;

ADULT; ARTICLE; ATHLETE; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENDURANCE; EXERCISE; GLUCOSE BLOOD LEVEL; HUMAN; IMMUNOFLUORESCENCE MICROSCOPY; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID ANALYSIS; MALE; MUSCLE CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; TRAINING;

ADULT; DIABETES MELLITUS, TYPE 2; HUMANS; LIFE STYLE; LIPID METABOLISM; MALE; MIDDLE AGED; MUSCLE FIBERS; MUSCLE, SKELETAL; OBESITY; PHYSICAL EDUCATION AND TRAINING; PHYSICAL ENDURANCE; TISSUE DISTRIBUTION;

EID: 4143060180     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00464.2003     Document Type: Article

References (60)

1. Andersson A, Sjodin A, Hedman A, Olsson R, and Vessby B. Fatty acid profile of skeletal muscle phospholipids in trained and untrained young men. Am J Physiol Endocrinol Metab 279: E744-E751, 2000.
2. Anderwald C, Bernroider E, Krssak M, Stingl H, Brehm A, Bischof MG, Nowotny P, Roden M, and Waldhausl W. Effects of insulin treatment in type 2 diabetic patients on intracellular lipid content in liver and skeletal muscle. Diabetes 51: 3025-3032, 2002.
3. Bergh U, Thorstensson A, Sjodin B, Hulten B, Piehl K, and Karlsson J. Maximal oxygen uptake and muscle fiber types in trained and untrained humans. Med Sci Sports Exerc 10: 151-154.
4. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35: 609-616, 1975.
5. Blaak EE, van Aggel-Leijssen DPC, Wagenmakers AJM, Saris WHM, and van Baak MA. Impaired oxidation of plasma-derived fatty acids in type 2 diabetic subjects during moderate-intensity exercise. Diabetes 49: 12, 2000.
6. Boden G, Lebed B, Schatz M, Homko C, and 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.
7. Boden G and Shulman GI. Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and beta-cell dysfunction. Eur J Clin Invest 32: 14-23, 2002.
8. 1H-magnetic resonance spectroscopy. Ann NY Acad Sci 904: 25-31, 2000.
9. 1H-MR-spectroscopy. Magn Reson Med 37: 484-493, 1997.
10. Borghouts LB, Wagenmakers AJ, Goyens PL, and Keizer HA. Substrate utilization in non-obese Type II diabetic patients at rest and during exercise. Clin Sci (Lond) 103: 559-566, 2002.
11. 1H-MRS study. Magn Reson Med 45: 179-183, 2001.
12. Cho M, Webster SG, and Blau HM. Evidence for myoblast-extrinsic regulation of slow myosin heavy chain expression during muscle fiber formation in embryonic development. J Cell Biol 121: 795-810, 1993.
13. Cogswell AM, Stevens RJ, and Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264: C383-C389, 1993.
14. Dresner A, Laurent D, Marcucci M, Griffin ME, Dufour S, Cline GW, Slezak LA, Andersen DK, Hundal RS, Rothman DL, Petersen KF, and 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.
15. Ebeling P, Bourey R, Koranyi L, Tuominen JA, Groop LC, Henriksson J, Mueckler M, Sovijarvi A, and Koivisto VA. Mechanism of enhanced insulin sensitivity in athletes. Increased blood flow, muscle glucose transport protein (GLUT-4) concentration, and glycogen synthase activity. J Clin Invest 92: 1623-1631, 1993.
16. 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.
17. Forouhi NG, Jenkinson G, Thomas EL, Mullick S, Mierisova S, Bhonsle U, McKeigue PM, and 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.
18. 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.
19. 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.
20. Griffin ME, Marcucci MJ, Cline GW, Bell K, Barucci N, Lee D, Goodyear LJ, Kraegen EW, White MF, and 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.
21. 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.
22. Henriksen EJ, Bourey RE, Rodnick KJ, Koranyi L, Permutt MA, and Holloszy JO. Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. Am J Physiol Endocrinol Metab 259: E593-E598, 1990.
23. Hickey MS, Carey JO, Azevedo JL, Houmard JA, Pories WJ, Israel RG, and 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.
24. Hoppeler H. Skeletal muscle substrate metabolism. Int J Obes Relat Metab Disord 23: S7-S10, 1999.
25. Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, and Weibel ER. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59: 320-327, 1985.
26. Jacob S, Machann J, Rett K, Brechtel K, Volk A, Renn W, Maerker E, Matthaei S, Schick F, Claussen CD, and 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.
27. James DE, Jenkins AB, and Kraegen EW. Heterogeneity of insulin action in individual muscles in vivo: euglycemic clamp studies in rats. Am J Physiol Endocrinol Metab 248: E567-E574, 1985.
28. Kautzky-Willer A, Krssak M, Winzer C, Pacini G, Tura A, Farhan S, Wagner O, Brabant G, Horn R, Stingl H, Schneider B, Waldhausl W, and Roden M. Increased intramyocellular lipid concentration identifies impaired glucose metabolism in women with previous gestational diabetes. Diabetes 52: 244-251, 2003.
29. Kelley D and Mandarino L. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 49: 677-683, 2000.
30. Kern M, Wells JA, Stephens JM, Elton CW, Friedman JE, Tapscott EB, Pekala PH, and Dohm GL. Insulin responsiveness in skeletal muscle is determined by glucose transporter (GLUT-4) protein level. Biochem J 270: 397-400, 1990.
31. Koopman R, Schaart G, and Hesselink MK. Optimisation of oil red O staining permits combination with immunofluorescence and automated quantification of lipids. Histochem Cell Biol 116: 63-68, 2001.
32. Koyama K, Chen G, Lee Y, and Unger RH. Tissue triglycerides, insulin resistance, and insulin production: implications for hyperinsulinemia of obesity. Am J Physiol Endocrinol Metab 273: E708-E713, 1997.
33. 1H-NMR spectroscopy study. Diabetologia 42: 113-116, 1999.
34. Kuipers H, Verstappen FT, Keizer HA, Geurten P, and van Kranenburg G. Variability of aerobic performance in the laboratory and its physiologic correlates. Int J Sports Med 6: 197-201, 1985.
35. Lohmann D, Liebold F, Heilmann W, Senger H, and Pohl A. Diminished insulin response in highly trained athletes. Metabolism 27: 521-524, 1978.
36. Malenfant P, Joanisse DR, Theriault R, Goodpaster BH, Kelley DE, and Simoneau JA. Fat content in individual muscle fibers of lean and obese subjects. Int J Obes Relat Metab Disord 25: 1316-1321, 2001.
37. 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.
38. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, and Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412-419, 1985.
39. Nyholm B, Qu Z, Kaal A, Pedersen SB, Gravholt CH, Andersen JL, Saltin B, and 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.
40. Oakes ND, Bell KS, Furler SM, Camilleri S, Saha AK, Ruderman NB, Chisholm DJ, and Kraegen EW. Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise: parallel relationship between insulin stimulation of glucose uptake and suppression of long-chain fatty acyl-CoA. Diabetes 46: 2022-2028, 1997.
41. Oakes ND, Cooney GJ, Camilleri S, Chisholm DJ, and Kraegen EW. Mechanisms of liver and muscle insulin resistance induced by chronic high-fat feeding. Diabetes 46: 1768-1774, 1997.
42. 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.
43. Paolisso G, Tataranni PA, Foley JE, Bogardus C, Howard BV, and Ravussin E. A high concentration of fasting plasma non-esterified fatty acids is a risk factor for the development of NIDDM. Diabetologia 38: 1213-1217, 1995.
44. Perseghin G, Ghosh S, Gerow K, and Shulman GI. Metabolic defects in lean nondiabetic offspring of NIDDM parents: a cross-sectional study. Diabetes 46: 1001-1009, 1997.
45. Perseghin G, Scifo P, Danna M, Battezzati A, Benedini S, Meneghini E, Del Maschio A, and Luzi L. Normal insulin sensitivity and IMCL content in overweight humans are associated with higher fasting lipid oxidation. Am J Physiol Endocrinol Metab 283: E556-E564, 2002.
46. 13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 48: 1600-1606, 1999.
47. Phillips DI, Caddy S, Ilic V, Fielding BA, Frayn KN, Borthwick AC, and Taylor R. Intramuscular triglyceride and muscle insulin sensitivity: evidence for a relationship in nondiabetic subjects. Metabolism 45: 947-950, 1996.
48. 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.
49. Reaven GM, Hollenbeck C, Jeng CY, Wu MS, and Chen YD. Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes 37: 1020-1024, 1988.
50. Roden M, Price TB, Perseghin G, Petersen KF, Rothman DL, Cline GW, and Shulman GI. Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 97: 2859-2865, 1996.
51. Rodnick KJ, Haskell WL, Swislocki AL, Foley JE, and Reaven GM. Im-proved insulin action in muscle, liver, and adipose tissue in physically trained human subjects. Am J Physiol Endocrinol Metab 253: E489-E495, 1987.
52. Schrauwen P, van Aggel-Leijssen DP, Hul G, Wagenmakers AJ, Vidal H, Saris WH, and van Baak MA. The effect of a 3-month low-intensity endurance training program on fat oxidation and acetyl-CoA carboxylase-2 expression. Diabetes 51: 2220-2226, 2002.
53. Schrauwen-Hinderling VB, Schrauwen P, Hesselink MK, van Engelshoven JM, Nicolay K, Saris WH, Kessels AG, and Kooi ME. The increase in intramyocellular lipid content is a very early response to training. J Clin Endocrinol Metab 88: 1610-1616, 2003.
54. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest 106: 171-176, 2000.
55. Simoneau JA, Colberg SR, Thaete FL, and 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.
56. Storlien LH, Jenkins AB, Chisholm DJ, Pascoe WS, Khouri S, and Kraegen EW. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid. Diabetes 40: 280-289, 1991.
57. Thamer C, Machann J, Bachmann O, Haap M, Dahl D, Wietek B, Tschritter O, Niess A, Brechtel K, Fritsche A, Claussen C, Jacob S, Schick F, Haring HU, and Stumvoll M. Intramyocellular lipids: anthropometric determinants and relationships with maximal aerobic capacity and insulin sensitivity. J Clin Endocrinol Metab 88: 1785-1791, 2003.
58. Van Loon LJC, Koopman R, Stegen JHCH, Wagenmakers AJM, Keizer HA, and Saris WHM. 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.
59. Van Loon LJC, Schrauwen-Hinderling VB, Koopman R, Wagenmakers AJM, Hesselink MK, Schaart G, Kooi ME, and Saris WHM. Influence of prolonged endurance cycling and recovery diet on intramuscular triglyceride content in humans. Am J Physiol Endocrinol Metab 285: E804-E811, 2003.
60. 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, and 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.