Skeletal Muscle Triglyceride: An aspect of regional adiposity and insulin resistance

Diabetes Care

Volumn 24, Issue 5, 2001, Pages 933-941

  Kelley, David E ^a,b   Goodpaster, Bret H ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRIACYLGLYCEROL;

ADIPOSE TISSUE; DIABETES MELLITUS; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; METABOLISM; MUSCLE MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SKELETAL MUSCLE;

ADIPOSE TISSUE; DIABETES MELLITUS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN RESISTANCE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OBESITY; TRIGLYCERIDES;

EID: 0035345532     PISSN: 01495992     EISSN: None     Source Type: Journal    
DOI: 10.2337/diacare.24.5.933     Document Type: Review

References (87)

1. Despres JP: Abdominal obesity as important component of insulin-resistance syndrome (Review). Nutrition 9:452-459, 1993
2. Tchernof A, Lamarche B, Prud'Homme D, Nadeau A, Moorjani S, Labrie F, Lupien PJ, Despres JP: The dense LDL phenotype: association with plasma lipoprotein levels, visceral obesity, and hyperinsulinemia in men. Diabetes Care 19:629-637, 1996
3. Björntorp P: Metabolic implications of body fat distribution. Diabetes Care 14: 1132-1143, 1991
4. Fujioka S, Matsuzawa Y, Tokunaga K, Tarui S: Contribution of intra-abdominal fat accumulation to the impairment of glucose and lipid metabolism in human obesity. Metabolism 36:54-59, 1987
5. Banerji M, Chaiken R, Gordon D, Lebowitz H: Does intra-abdominal adipose tissue in black men determine whether NIDDM is insulin-resistant or insulin-sensitive? Diabetes 44:141-146, 1995
6. Goodpaster BH, Kelley DE, Wing RR, Meier A, Thaete FL: Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 48:839-847, 1999
7. Marceau P, Biron S, Hould FS, Marceau S, Simard S, Thung SN, Kral JG: Liver pathology and the metabolic syndrome X in severe obesity. J Clin Endocrinol 84:1513-1517, 1999
8. Marchesmi G, Brizi M, Morselli-Labate AM, Bianchi G, Bugianesi E, McCullough AJ, Forlani G, Melchionda N: Association of nonalcoholic fatty liver disease with insulin resistance. Am J Med 107:450-455, 1999
9. Ryysy L, Hakkinen AM, Goto T, Vehkavaara S, Westerbacka J, Halavaara J, Yki-Jarvinen H: Hepatic fat content and insulin action on free fatty acids and glucose metabolism rather than insulin absorption are associated with insulin requirements during insulin therapy in type 2 diabetic patients. Diabetes 49:749-758, 2000
10. Rebrin K, Steil GM, Getty L, Bergman RN: Free fatty acid as a link in the regulation of hepatic glucose output by peripheral insulin. Diabetes 44:1038-1045, 1995
11. Carey DG, Jenkins AB, Campbell LV, Freund J, Chisholm DJ: Abdominal fat and insulin resistance in normal and overweight women. Diabetes 45:633-638, 1996
12. Goodpaster BH, Thaete FL, Kelley DE: Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr 71:885-892, 2000
13. 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
14. Kelley DE, Slasky S, Janosky J: Skeletal muscle density: effects of obesity and non-insulin-dependent diabetes mellitus. Am J Clin Nutr 54:509-515, 1991
15. 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 89:104-110, 2000
16. 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
17. Boesch C, Slotboom J, Hoppeler H, Kreis R: In vivo determination of intra-myocellular lipids in human muscle by means of localized IH-MR-spectroscopy. Magn Reson Med 37:484-493, 1997
18. Szczepaniak LS, Babcock EE, Schick F, Dobbins RL, Garg A, Burns DK, McGarry JD, Stein DT: Measurement of intracellular triglyceride stores by H spectroscopy: validation in vivo. Am J Physiol 276:E977-E989, 1999
19. 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
20. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, Storlein LH: Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46:983-988, 1997
21. Storlien L, Jenkins A, Chisholm D, Pascoe W, Khouri S, 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
22. Shimabukuro M, Koyama K, Chen G, Wang MY, Trieu F, Lee Y, Newgard CB, Unger RH: Direct antidiabetic effect of leptin through triglyceride depletion of tissues. Proc Natl Acad Sci U S A 94:4637-4641, 1997
23. 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
24. Goodpaster BH, Theriault R, Watkins SC, Kelley DE: Intramuscular lipid content is increased in obesity and decreased by weight loss Metabolism 49:467-472, 2000
25. Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, Weibel ER: Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59:320-327, 1985
26. Morgan TE, Short FA, Cobb LA: Effect of long-term exercise on skeletal muscle lipid composition. J Appl Physiol 216:82-86, 1969
27. Dela F, Larsen JJ, Mikmes KJ, Ploug T, Petersen LN, Galbo H: Insulin-stimulated muscle glucose clearance in patients with NIDDM. Diabetes 44:1010-1020, 1995
28. Mayer-Davis EJ, D'Agostino R Jr, Karter AJ, Haffner SM, Rewers MJ, Saad M, Bergman RN: Intensity and amount of physical activity in relation to insulin sensitivity: the Insulin Resistance Atherosclerosis Study. JAMA 279:669-674, 1998
29. Gollnick PD, Saltin B: Significance of skeletal muscle oxidative enzyme enhancement with endurance training. Clin Physiol 2:1-12, 1982
30. Carlson LA, Ekelund LG, Froberg SO: Concentration of triglycerides, phospholipids and glycogen in skeletal muscle and of free fatty acids and β-hydroxybutyric acid in blood in man in response to exercise. Eur J Clin Invest 1:248-254, 1971
31. Fröberg SO, 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
32. Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E, Wolfe RR: Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol 265:E380-E391, 1993
33. 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 271:E340-E351, 1997
34. Ruderman NB, Saha AK, Vavvas D, Kurowski T, Laybutt DR, Schmitz-Peiffer C, Biden T, Kraegen EW: Malonyl CoA as a metabolic switch and a regulator of insulin sensitivity. In Skeletal Muscle Metabolism in Exercise and Diabetes. Richter EA, Kiens B, Galbo H, Eds. New York, Plenum Press, 1998, p. 263-270
35. Andres R, Cadar G, Zierler K: The quantitatively minor role of carbohydrate in oxidative metabolism by skeletal muscle in intact man in the basal state. J Clin Invest 35:671-682, 1956
36. Colberg S, Simoneau JA, Thaete FL, Kelley DE: Impaired FFA utilization by skeletal muscle in women with visceral obesity. J Clin Invest 95:1846-1853, 1995
37. Kelley DE, Goodpaster BH, Wing RR, Simoneau JA: Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity and weight loss. Am J Physiol 277:E1130-E1141, 1999
38. 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
39. Berk PD, Zhou S-L, Bradbury M, Stump D, Han N-I: Characterization of membrane transport processes: lessons learned from the study of BSP, bilirubin, and fatty acid uptake. Semin Liver Dis 16:107-120, 1996
40. 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
41. Felber JP, Ferrannini E, Golay A, Meyer H, Thiebauld D, Curchod B, Maeder E, Jequier E, DeFronzo R: Role of lipid oxidation in the pathogenesis of insulin resistance of obesity and type II diabetes. Diabetes 36:1341-1350, 1987
42. Groop LC, Saloranta C, Shank M, Bonnadonna RC, Ferrannini E, DeFronzo RA: The role of free fatty acid metabolism in the pathogenesis of insulin resistance in obesity and noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 72: 96-107, 1991
43. Kelley DE, Mokan M, Simoneau JA, Mandarino LJ: Interaction between glucose and free fatty acid metabolism in human skeletal muscle. J Clin Invest 92:93-98, 1993
44. Kelley DE, Simoneau JA: Impaired FFA utilization by skeletal muscle in NIDDM. J Clin Invest 94:2349-2356, 1994
45. 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
46. Randle PJ, Garland PB, Hales CN, Newsholme EA: The glucose fatty acid cycle: its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 1:785-789, 1963
47. Boden G, Chen X: Effects of fat on glucose uptake and utilization in patients with non-insulin-dependent diabetes. J Clin Invest 96:1261-1268, 1995
48. Cortright RN, Azevedo JL Jr, Zhou Q, Sinha M, Pories WJ, Itani SI, Dohm GL: Protein kinase C modulates insulin action in human skeletal muscle. Am J Physiol 278:E553-E662, 2000
49. Itani SI, Zhou Q, Pories WJ, MacDonald KG, Dohm GL: Involvement of protein kinase C in human skeletal muscle insulin resistance and obesity. Diabetes 49:1353-1358, 2000
50. Laybutt DR, Schmitz-Peiffer S, Ruderman NB, Chisholm D, Biden T, Kraegen EW: Activation of protein kinase C 101 ∴φ ∴σ 12 may contribute to muscle insulin resistance induced by lipid accumulation during chronic glucose infusion in rats (Abstract). Diabetes 46:241A, 1997
51. Schmitz-Peiffer C, Oakes ND, Browne CL, Kraegen EW, Biden TJ: Alterations in the expression and cellular localization of protein kinase C isozymes ε and θ are associated with insulin resistance in skeletal muscle of the high-fat-fed rat. Diabetes 46: 169-178, 1997
52. Schmitz-Peiffer C, Oakes ND, Browne CL, Kraegen EW, Biden TJ: Reversal of chronic alterations of skeletal muscle protein kinase C from fat-fed rats by BRL-49653. Am J Physiol 273:E915-E921, 1997
53. Kelley DE, Mandarino LJ: Hyperglycemia normalizes insulin-stimulated skeletal muscle glucose oxidation and storage in noninsulin-dependent diabetes mellitus. J Clin Invest 86:1999-2007, 1990
54. Mandarino LJ, Consoli A, Kelley DE: Differential regulation of intracellular glucose metabolism by glucose and insulin in human muscle. Am J Physiol 265:E898-E905, 1996
55. Mandarino LJ, Consoli A, Kelley DE: Effects of obesity and NIDDM on glucose and insulin regulation of substrate oxidation in skeletal muscle. Am J Physiol 270: E463-E470, 1996
56. Cortez MY, Torgan CE, Brozinick JT, Miller RH, Ivy JI.: Effects of pyruvate and dihydroxyacetone consumption on the growth and metabolic state of obese Zucker rats. Am J Clin Nutr 53:847-853, 1991
57. Torgan CE, Brozinick JT, Willems MET, Ivy JL: Substrate utilization during acute exercise in obese Zucker rats. J Appl Physiol 69:1987-1991, 1990
58. Kelley D, Reilly J, Veneman T, Mandarino LJ: Effect of insulin on skeletal muscle glucose storage, oxidation, and glycolysis in humans. Am J Physiol 258:E923-E929, 1990
59. Kelley DE, Mintun MA, Watkins SC, Simoneau JA, Jadali F, Fredrickson A, Beattie J, Theriault R: The effect of non-insulin-dependent diabetes mellitus and obesity on glucose transport and phosphorylation in skeletal muscle. J Clin Invest 97:2705-2713, 1996
60. Turcotte LP: Fatty acid binding proteins and muscle lipid metabolism in skeletal muscle. In Biochemistry of Exercise. Hargreaves M, Ed. Champaign, IL, Human Kinetics, 1999, p. 210-215
61. 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
62. Blaak EE, Wagenmakers AJM, Glatz JFC, Wolffenbuttel BHR, Kemerink GJ, Langenberg CJM, Heidendal GAK, Saris WHM: Plasma FFA utilization and fatty acid-binding protein content are diminished in type 2 diabetic muscle. Am J Physiol 279: 146-154, 2000
63. McGarry JD, Brown NF: The mitochondrial carnitine palmitoyltransferase system: from concept to molecular analysis. Eur J Biochem 224:1-14, 1997
64. Saha AK, Vavvas T, Kurowski TG, Apazidis A, Witters LA, Shafrir E, Ruderman NB: Malonyl-CoA regulation in skeletal muscle: its link to cell citrate and the glucose-fatty acid cycle. Am J Physiol 272: E641-E648, 1997
65. Kruszynska YE, Mulford MI, Baloga J, Yu JG, Olefsky JM: Regulation of skeletal muscle hexokinase II by insulin in nondiabetic and NIDDM subjects. Diabetes 47: 1107-1113, 1998
66. Pendergrass M, Koval J, Vogt C, Yki-Jarvinen H, Iozzo P, Pipek R, Ardehali H, Printz R, Granner DK, DeFronzo RA, Mandarino LJ: Insulin-induced hexokinase II expression is reduced in obesity and NIDDM. Diabetes 47:387-394, 1998
67. Simoneau JA, Kelley DE: Altered skeletal muscle glycolytic and oxidative capacities contribute to insulin resistance in NIDDM. J Appl Physiol 83:166-171, 1997
68. Simoneau JA, Kelley DE, Neverova M, Warden CH: Overexpression of muscle uncoupling protein-2 content in human obesity associates with reduced skeletal muscle lipid utilization. FASEB J 12:1739-1745, 1998
69. Saltin B, Gollnick PD: Skeletal muscle adaptability: significance for metabolism and performance. In Handbook of Physiology. Section 10: Skeletal Muscle. Peachey LD, Adrian R, Geiger SR, Eds. Baltimore, Williams & Wilkins, 1983, p. 555-632
70. Kelley DE, Mandarino LJ: Fuel selection in human skeletal muscle in insulin resistance. Diabetes 49:677-683, 2000
71. Long SD, O'Brien K, MacDonald KG Jr, Leggett-Frazier N, Swanson MS, Pories WJ, Caro JF: Weight loss in severely obese subjects prevents the progression of impaired glucose tolerance to type II diabetes: a longitudinal interventional study Diabetes Care 17:372-375, 1994
72. Wing RR, Vendetti E, Jakicie JM, Polley BA, Lang W: Lifestyle intervention in overweight individuals with a family history of diabetes. Diabetes Care 21:350-359, 1998
73. Henry RR, Wallace P, Olefsky JM: Effects of weight loss on mechanisms of hyperglycemia in obese non-insulin-dependent diabetes mellitus. Diabetes 35:990-998, 1986
74. Kelley DE, Wing R, Buonocore C, Sturis J, Polonsky K, Fitzsimmons M: Relative effects of calorie restriction and weight loss in noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 77:1287-1293, 1993
75. Wing RR, Blair E, Marcus M, Epstein LH, Harvey J: Year-long weight loss treatment for obese patients with type II diabetes: does including an intermittent very-low-calorie diet improve outcome? Am J Med 97:354-362, 1994
76. Wing RR, Blair EH, Bononi P, Marcus MD, Watanabe R, Bergman RN: Calorie restriction per se is a significant factor in improvements in glycemic control and insulin sensitivity during weight loss in obese NIDDM patients. Diabetes Care 17: 30-36, 1994
77. Maggio CA, Pi-Sunyer FX: The prevention and treatment of obesity: application to type 2 diabetes (Review). Diabetes Care 20:1744-1766, 1997
78. Goldstein DJ Beneficial effects of modest weight loss. Int J Obes 16:397-415, 1992
79. Wing RR, Koeske R, Epstein LH, Nowalk MP, Gooding W, Becker D: Long-term effects of modest weight loss in type II diabetic patients. Arch Intern Med 147:1749-1753, 1987
80. Bodkin NL, Ortmeyer HK, Hansen BC: Long-term dietary restriction in older-aged rhesus monkeys: effects on insulin resistance. J Gerontol A Biol Sci Med Sci: B142-B147, 1995
81. Zurlo F, Lillioja S, Esposito-DelPuente A, Nyomba BL, Raz I, Saad MF, Swiunburn WC, Knowler WC, Bogardus C, Ravussin E: Low ratio of fat to carbohydrate oxidation as a predictor of weight gain: a study of 24-h RQ. Am J Physiol 259:E650-E657. 1990
82. Ferraro R, Eckel R, Larson E, Fontvielle A, Rising R, Jensen D, Ravussin E: Relationship between lipoprotein lipase activity and 24-hour macronutrient oxidation. J Clin Invest 92:441-445, 1993
83. Zurlo F, Nemeth PM, Choksi RM, Sesodia S, Ravussin E: Whole-body energy metabolism and skeletal muscle biochemical characteristics. Metabolism 43:481-486, 1994
84. Bryson JM, King SE, Burns CM, Baur LA, Swaraj S, Caterson ID: Changes in glucose and lipid metabolism following weight loss produced by a very low calorie diet in obese subjects. Int J Obes 20:338-345, 1996
85. Blaak EE, Van Baak MA, Kemerink GJ, Pakbiers MT, Heidendal GA, Saris WH: Beta-adrenergic stimulation of skeletal muscle metabolism in relation to weight reduction in obese men. Am J Physiol 267: E316-E322, 1994
86. Ranneries C, Bulow J, Buemann B, Christensen NJ, Madsen J, Astrup A: Fat metabolism in formerly obese women. Am J Physiol 274:E155-E161, 1998
87. Hurley BF, Nemeth PM, Martin WH, Hagberg JM, Dalsky GP, Holloszy JO: Muscle triglyceride utilization during exercise: effect of training. J Appl Physiol 60:562-567, 1986