Role of muscle in triglyceride metabolism

Current Opinion in Lipidology

Volumn 9, Issue 3, 1998, Pages 231-236

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

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

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRIACYLGLYCEROL;

ENERGY METABOLISM; EXERCISE; FATTY ACID OXIDATION; HUMAN; HUMAN TISSUE; INSULIN RESISTANCE; LIPID METABOLISM; LIPID STORAGE; MUSCLE LEVEL; MUSCLE METABOLISM; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE;

ANIMALS; DIABETES MELLITUS, TYPE 2; FATTY ACIDS; FATTY ACIDS, NONESTERIFIED; HUMANS; INSULIN RESISTANCE; MUSCLE, SKELETAL; OBESITY; TRIGLYCERIDES;

ANIMALIA;

EID: 0031800968     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041433-199806000-00008     Document Type: Review

References (46)

1. Dagenais GR, Tancredi RG, 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 1976; 58:421-431.
2. Bonadonna RC, Groop LC, Zych K, Shank M, DeFronzo RA. Dose-dependent effect of insulin on plasma free fatty acid turnover and oxidation in humans. Am J Physiol 1990; 259:E736-E750.
3. Colberg SR, Simoneau J-A, Theate FL, Kelley DE. Skeletal muscle utilization of FFA in women with visceral obesity. J Clin Invest 1995; 95:1846-1853.
4. Kelley DE, Simoneau J-A. Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest 1994; 94:2349-2356.
5. 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 1993; 265:E380-E391.
6. Sidossis LS, Wolfe RR. Glucose and insulin-induced inhibition of fatty acid oxidation: the glucose-fatty acid cycle reversed. Am J Physiol 1996; 270 (4 Pt 1):E733-E738.
7. Glatz JFC, van der Vusse GJ. Cellular fatty acid binding proteins: their function and physiological significance. Prog Lipid Res 1996; 35:243-282.
8. Dyck DJ, Peters SJ, Gorski J, Keizer H, Kiens B. et al. Functional differences in lipid metabolism in resting skeletal muscle of various fiber types. Am J Physiol 1997; 272 (3 Pt 1): E340-E351. This study found a greater incorporation of fatty acids into triglyceride of skeletal muscle with a higher oxidative capacity, with the majority of this due to an increased fatty acid oxidation rather than greater triglyceride synthesis, indicating that the turnover of muscle triglyceride in resting muscle is low.
9. Budohoski L, Gorski J, Nazar K, Kaciuba-Uscilko H, Terjung RL. Triacyl-glycerol synthesis in the different skeletal muscle fibre sections of the rat. Am J Physiol 1996; 271 (3 Pt 1):E574-E581. This report demonstrated that triglyceride synthesis is greater in muscle fibers possessing a greater oxidative capacity independent of blood flow characteristics of muscle.
10. Kelley DE, Reilly JP, Veneman T, Mandarino LJ. Effects of insulin on skeletal muscle glucose storage, oxidation, and glycolysis in humans. Am J Physiol 1990; 258:E923-E929.
11. Kelley DE, Mokan M, Simoneau J-A, Mandarino LJ. Interaction between glucose and free fatty acid metabolism in human skeletal muscle. J Clin Invest 1993; 92:91-98.
12. 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 1963; 1:785-789.
13. Mandarino LJ, Wright KS, Verity LS, Nichols J, Bell JM, Kolterman OG, Beck-Nielsen H. Effects of insulin infusion on human skeletal muscle pyruvate dehydrogenase, phosphofructokinase, and glycogen synthase. Evidence for their role in oxidative and nonoxidative glucose metabolism. J Clin Invest 1987; 80:655-663.
14. Mandarino LJ, Consoli A, Jain A, Kelly DE. Interaction of carbohydrate and fat fuels in human skeletal muscle: impact of obesity and NIDDM. Am J Physiol 1996; 270:E463-E470.
15. Kelley DE, Mandarino LJ. Hyperglycemia normalizes insulin-stimulated skeletal muscle glucose oxidation and storage in noninsulin-dependent diabetes mellitus. J Clin Invest 1990; 86:1999-2007.
16. Schwarz J-M, Neese RA, Turner S, Dare D, Hellerstein MK. Short-term alterations in carbohydrate energy intake in humans: striking effects on hepatic glucose production, de novo lipogenesis, lipolysis, and whole-body fuel selection. J Clin Invest 1995; 96:2735-2743.
17. McGarry JD. The mitochondrial carnitine palmitoyl transerase system: its broadening role in fuel homeostasis and new insights into its molecular features. Biochem Soc Trans 1995; 23:321-324.
18. Saha AK, Kurowski TG, Ruderman NB. A malonyl-CoA fuel-sensing mechanism in muscle: effects of insulin, glucose, and denervation. Am J Physiol 1995; 269:E283-E289.
19. Saha AK, Vavvas D, 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 1997; 272:E641-E648.
20. Winder WW, Arogyasami J, Elayan IM, Cartmill D. Time course of exercise-induced decline in malonyl-CoA in different muscle types. Am J Physiol 1990; 259 (2 Pt 1):E266-E271.
21. Odland LM, Heigenhauser GJ, Lopaschuk GD, Spriet LL. Human skeletal muscle malonyl-CoA at rest and during prolonged submaximal exercise. Am J Physiol 1996; 270 (3 Pt 1):E541-E544.
22. Saha AK, Kurowski TG, Colca JR, Ruderman NB. Lipid abnormalities in tissues of the KKAy mouse: effects of pioglitazone on malonyl-CoA and diacylglycerol. Am J Physiol 1994; 267 (1 Pt 1):E95-E101.
23. Oakes ND, Camilleri S, Furier SM, Chisholm DJ, Kraegen EW. The insulin sensitizer, BRL 49653, reduces systemic fatty acid supply and utilization and tissue lipid availability in the rat. Metab Clin Exp 1997; 46:935-42. This important study demonstrates the association of lipid supply within muscle with insulin sensitivity in rats given the insulin sensitizer, thiazolidinedione, in which glucose disposal was negatively related with muscle triglyceride content.
24. Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science 1995; 269:543-546.
25. Muoio DM, Dohn GL, Fiedorek FT Jr; Tapscott EB, Coleman RA. Leptin directly alters lipid partitioning in skeletal muscle. Diabetes 1997; 48:1360-1363. This report demonstrates that leptin administered to leptin-deficient mice increased intramuscular triglyceride oxidation in muscle and decreased incorporation of fatty acids into triglyceride, thereby altering partitioning of lipid substrate from that of storage toward utilization.
26. Shimabukuro M, Koyama K, Chen G, Wang MY, Trieu F, Lee Y, et al. Direct antidiabetic effect of leptin through triglyceride depletion of tissues. Proc Nat Acad Sci USA 1997; 94:4637-4641. In-vivo hyperleptinemia in rats resulted in depleted muscle triglyceride stores, presumably by increased rates of fatty acid oxidation within muscle.
27. Gollnick PD, Saltin B. Significance of skeletal muscle oxidative enzyme enhancement with endurance training. Clin Physiol 1982; 2:1-12.
28. Martin WH Jr. Effects of acute and chronic exercise on fat metabolism. Exerc Sport Sci Rev 1996; 24:203-231.
29. Sidossis LS, Gastaldelli A, Klein S, Wolfe RR. Regulation of plasma fatty acid oxidation during low- and high-intensity exercise. Am J Physiol 1997; 272 (6 Pt 1):E1065-E1070.
30. Coyle EF, Jeukendrup AE, Wagenmakers AJ, Saris WH. Fatty acid oxidation is directly regulated by carbohydrate metabolism during exercise. Am J Physiol 1997; 273 (2 Pt 1):E268-E275
31. 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; 82:1185-1189. Muscle triglyceride was found to be increased in human volunteers consuming a high fat diet 24 hours after 2 h moderate cycling, indicating the potential for acute dietary changes to alter muscle triglyceride stores.
32. Goodpaster BH, Thaete FL, Simoneau J-A, Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes 1997; 46:1579-1585. This study demonstrated that an increased lipid content in muscle determined by computed tomography was a marker of obesity and was as strong as visceral adipose content in predicting insulin sensitivity in a group of individuals ranging from lean to obese.
33. Oakes ND, Bell KS, Furler SM, Camilleri S, Saha AK, Ruderman NB, et al. Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise. Diabetes 1997; 46:2022-2028. This is the only known study that has examined the effects of acutely manipulated muscle triglyceride on insulin resistance. Muscle triglyceride stores were reduced, whereas the enhanced ability of insulin to suppress long chain coenzyme A in muscle was associated with increased insulin sensitivity in chronically high fat fed rats.
34. Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, et al. Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 1997; 46:983-988. This report demonstrated that higher intramuscular triglyceride levels were associated wtih insulin resistant glucose metabolism independent of other parameters of body composition in a group of nondiabetic human volunteers.
35. 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. Metab Clin Exp 1996; 45:947-950. This study used histochemical and biochemical determination of lipid content in human percutaneous muscle biopsy samples in observing a relationship between lipid content in muscle and glycogen synthase activity, a marker for insulin sensitivity.
36. Storlien L, Jenkins A, Chisholm D, Pascoe W, Khouri S, Kraegen E. Influence of dietary fat composition on development of insulin resistance in rats: relationship to muscle triglyceride and w3 fatty acids in muscle phospholipid. Diabetes 1991; 40:280-289.
37. Nuutila P, Koivisto VA, Knuuti J, Ruotsalainen U, Teras M, Haaparanta M, et al. Glucose-tree fatty acid cycle operates in human heart and skeletal muscle in vivo. J Clin Invest 1992; 89:1767-1774.
38. Boden G, Chen X, Ruiz J, White JV, Rossetti L. Mechanisms of fatty acid-induced inhibition of glucose uptake. J Clin Invest 1994; 93:2438-2446.
39. Wendung PS, Peters SJ, Heigenhauser GJ, Spriet LL. Variability of triacyl-glycerol content in human skeletal muscle biopsy samples. J Appl Physiol 1996; 81:1150-1155.
40. Kelley DE, Slasky BS, Janosky J. Skeletal muscle density: effects of obesity and non-insulin dependent diabetes mellitus. J Clin Nutr 1991; 54:509-515.
41. Simoneau J-A, 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 1995; 9:273-278.
42. Boesch C, Slotboom J, Hoppeier H, Kreis R. In vivo determination of intra-myocellular lipids in human muscle by means of localized 1H-MR-spectroscopy. Magn Reson Med 1997; 37:484-493. This study examined the utility of using MRS to measure intracellular and extracellular lipid content within muscle in human volunteers before and after excerise. This noninvasive method was able to give reliable, reproducible measures of intramyocelluar lipid content.
43. Vock R, Hoppeler H, Claassen H, Wu DX, Billeler R, Weber JM, et al. Design of the oxygen and substrate pathways. VI. structural basis of intracellular substrate supply to mitochondria in muscle cells. J Exp Biol 1996; 199 (Pt 8):1689-1697.
44. Stein DT, Dobbins R, Szczepaniak L, Malloy C, McGarry JD. Skeletal muscle triglyceride stores are increased in insulin resistance. [abstract] Diabetes 1997; 46(suppl 1):23A.
45. Hotamisligil GS, Spiegelman BM. Tumor necrosis factor alpha: a key component of the obesity-diabetes link. Diabetes 1994; 43:1271-1278.
46. Pan DA, Lillioja S, Milner MR, Kriketos AD, Baur LA, Bogards C, Storlien LH. Skeletal muscle membrane lipid composition is related to adiposity and insulin action. J Clin Invest 1995; 96:2802-2808.