Paradoxical coupling of triglyceride synthesis and fatty acid oxidation in skeletal muscle overexpressing DGAT1

Diabetes

Volumn 58, Issue 11, 2009, Pages 2516-2524

  Liu, Li ^a   Shi, Xiaojing ^a   Cheol, Soo Choi ^b   Shulman, Gerald I ^b   Klaus, Katherine ^c   Nair, K Sreekumaran ^c   Schwartz, Gary J ^d   Zhang, Yiying ^e   Goldberg, Ira J ^a   Yu, Yi Hao ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Mayo Clinic   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL ACYLTRANSFERASE 1; FATTY ACID; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; FOOD INTAKE; GENE EXPRESSION; INSULIN SENSITIVITY; LIPOGENESIS; MOUSE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE;

3-HYDROXYACYL COA DEHYDROGENASES; ADENOSINE TRIPHOSPHATE; ANIMALS; CARNITINE O-PALMITOYLTRANSFERASE; CITRATE (SI)-SYNTHASE; CREATINE KINASE, MM FORM; DIACYLGLYCEROL O-ACYLTRANSFERASE; DIETARY FATS; DNA, MITOCHONDRIAL; FATTY ACIDS; GENE EXPRESSION REGULATION; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; RESPIRATORY MECHANICS; TRIGLYCERIDES;

EID: 70350545945     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db08-1096     Document Type: Article

References (50)

1. 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;86:5755-5761 (Pubitemid 33152620)
2. Russell AP. Lipotoxicity: the obese and endurance-trained paradox. Int J Obes Relat Metab Disord 2004;28:S66-S71
3. Liu L, Zhang Y, Chen N, Shi X, Tsang B, Yu YH. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J Clin Invest 2007;117:1679-1689 (Pubitemid 46871352)
4. Bassel-Duby R, Olson EN. Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 2006;75:19-37 (Pubitemid 44118024)
5. 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 1995;9:273-278
6. Simoneau JA, Kelley DE. Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J Appl Physiol 1997;83:166-171
7. Papa S. Mitochondrial oxidative phosphorylation changes in the life span. Molecular aspects and physiopathological implications. Biochim Biophys Acta 1996;1276:87-105
8. Bruce CR, Thrush AB, Mertz VA, Bezaire V, Chabowski A, Heigenhauser GJ, Dyck DJ. Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab 2006;291:E99-E107
9. Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA, Coenen-Schimke JM, Nair KS. Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 2003;52:1888-1896
10. Hickey MS, Carey JO, Azevedo JL, Houmard JA, Pories WJ, Israel RG, Dohm GL. Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans. Am J Physiol 1995;268:E453-E457
11. Tanner CJ, Barakat HA, Dohm GL, Pories WJ, MacDonald KG, Cunningham PR, Swanson MS, Houmard JA. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 2002;282:E1191-E1196
12. Schenk S, Horowitz JF. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest 2007;117:1690-1698
13. 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, 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 2002;277:50230-50236
14. Griffin ME, Marcucci MJ, Cline GW, Bell K, Barucci N, Lee D, Goodyear LJ, Kraegen EW, White MF, 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 1999;48:1270-1274 (Pubitemid 29241025)
15. Lee JS, Pinnamaneni SK, Eo SJ, Cho IH, Pyo JH, Kim CK, Sinclair AJ, Febbraio MA, Watt MJ. Saturated, but not n-6 polyunsaturated, fatty acids induce insulin resistance: role of intramuscular accumulation of lipid metabolites. J Appl Physiol 2006;100:1467-1474
16. Summers SA, Garza LA, Zhou H, Birnbaum MJ. Regulation of insulin-stimulated glucose transporter GLUT4 translocation and Akt kinase activity by ceramide. Mol Cell Biol 1998;18:5457-5464 (Pubitemid 28388128)
17. Schmitz-Peiffer C, Craig DL, Biden TJ. Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J Biol Chem 1999;274:24202-24210 (Pubitemid 129528468)
18. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest 2000;106:171-176
19. Choi CS, Fillmore JJ, Kim JK, Liu ZX, Kim S, Collier EF, Kulkarni A, Distefano A, Hwang YJ, Kahn M, Chen Y, Yu C, Moore IK, Reznick RM, Higashimori T, Shulman GI. Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J Clin Invest 2007;117:1995-2003 (Pubitemid 47036334)
20. Youn JH, Buchanan TA. Fasting does not impair insulin-stimulated glucose uptake but alters intracellular glucose metabolism in conscious rats. Diabetes 1993;42:757-763
21. Cabrero A, Alegret M, Sanchez RM, Adzet T, Laguna JC, Vazquez M. Bezafibrate reduces mRNA levels of adipocyte markers and increases fatty acid oxidation in primary culture of adipocytes. Diabetes 2001;50:1883-1890 (Pubitemid 33641610)
22. Shen X, Zheng S, Thongboonkerd V, Xu M, Pierce WM, Jr, Klein JB, Epstein PN. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab 2004;287:E896-E905 (Pubitemid 39382925)
23. Short KR, Bigelow ML, Kahl J, Singh R, Coenen-Schimke J, Raghavakaimal S, Nair KS. Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci U S A 2005;102:5618-5623
24. Rooyackers OE, Senden JM, Soeters PB, Saris WH, Wagenmakers AJ. Prolonged activation of the branched-chain -keto acid dehydrogenase complex in muscle of zymosan treated rats. Eur J Clin Invest 1995;25:548-552
25. Kennedy S, Stanley WC, Panchal AR, Mazzeo RS. Alterations in enzymes involved in fat metabolism after acute and chronic altitude exposure. J Appl Physiol 2001;90:17-22 (Pubitemid 32038498)
26. Campbell SE, Febbraio MA. Effect of ovarian hormones on mitochondrial enzyme activity in the fat oxidation pathway of skeletal muscle. Am J Physiol Endocrinol Metab 2001;281:E803-E808 (Pubitemid 32948149)
27. Zhang Y, Guo K, LeBlanc RE, Loh D, Schwartz GJ, Yu YH. Increasing dietary leucine intake reduces diet-induced obesity and improves glucose and cholesterol metabolism in mice via multimechanisms. Diabetes 2007;56:1647-1654 (Pubitemid 46842599)
28. Yu YH, Zhu H. Chronological changes in metabolism and functions of cultured adipocytes: a hypothesis for cell aging in mature adipocytes. Am J Physiol Endocrinol Metab 2004;286:E402-E410 (Pubitemid 38292690)
29. Chen N, Liu L, Zhang Y, Ginsberg HN, Yu YH. Whole-body insulin resistance in the absence of obesity in FVB mice with overexpression of DGAT1 in adipose tissue. Diabetes 2005;54:3379-3386 (Pubitemid 43334326)
30. Yu YH, Zhang Y, Oelkers P, Sturley SL, Rader DJ, Ginsberg HN. Posttranscriptional control of the expression and function of diacylglycerol acyltransferase- 1 in mouse adipocytes. J Biol Chem 2002;277:50876-50884 (Pubitemid 36042254)
31. Sugden MC, Holness MJ. Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 2003;284:E855-E862
32. Pilegaard H, Neufer PD. Transcriptional regulation of pyruvate dehydrogenase kinase 4 in skeletal muscle during and after exercise. Proc Nutr Soc 2004;63:221-226 (Pubitemid 38787469)
33. Pilegaard H, Neufer PD. Transcriptional regulation of pyruvate dehydrogenase kinase 4 in skeletal muscle during and after exercise. Proc Nutr Soc 2004;63:221-226
34. Clapham JC, Arch JR, Chapman H, Haynes A, Lister C, Moore GB, Piercy V, Carter SA, Lehner I, Smith SA, Beeley LJ, Godden RJ, Herrity N, Skehel M, Changani KK, Hockings PD, Reid DG, Squires SM, Hatcher J, Trail B, Latcham J, Rastan S, Harper AJ, Cadenas S, Buckingham JA, Brand MD, Abuin A. Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 2000;406:415-418
35. Lowell BB, Shulman GI, Befroy DE, Petersen KF, Dufour S, Mason GF, de Graaf RA, Rothman DL. Mitochondrial dysfunction and type 2 diabetes. Science 2005;307:384-387
36. Se Jtump CS, Short KR, Bigelow ML, SchimkM, Nair KS. Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc Natl Acad Sci U S A 2003;100:7996-8001
37. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 2004;350:664-671 (Pubitemid 38364625)
38. Holloszy JO. Skeletal muscle "mitochondrial deficiency" does not mediate insulin resistance. Am J Clin Nutr 2009;89:463S-466S
39. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 2008;7:45-56
40. Dulloo AG, Gubler M, Montani JP, Seydoux J, Solinas G. Substrate cycling between de novo lipogenesis and lipid oxidation: a thermogenic mechanism against skeletal muscle lipotoxicity and glucolipotoxicity. Int J Obes Relat Metab Disord 2004;4 (Suppl.):S29-S37 (Pubitemid 40143846)
41. Bowker-Kinley MM, Davis WI, Wu P, Harris RA, Popov KM. Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem J 1998;329:191-196 (Pubitemid 28022308)
42. Gudi R, Bowker-Kinley MM, Kedishvili NY, Zhao Y, Popov KM. Diversity of the pyruvate dehydrogenase kinase gene family in humans. J Biol Chem 1995;270:28989-28994
43. Wu P, Sato J, Zhao Y, Jaskiewicz J, Popov KM, Harris RA. Starvation and diabetes increase the amount of pyruvate dehydrogenase kinase isoenzyme 4 in rat heart. Biochem J 1998;329:197-201 (Pubitemid 28022309)
44. Fuller SJ, Randle PJ. Reversible phosphorylation of pyruvate dehydrogenase in rat skeletal-muscle mitochondria. Effects of starvation and diabetes. Biochem J 1984;219:635-646
45. Kim YI, Lee FN, Choi WS, Lee S, Youn JH. Insulin regulation of skeletal muscle PDK4 mRNA expression is impaired in acute insulin-resistant states. Diabetes 2006;55:2311-2317 (Pubitemid 44743629)
46. Feldhoff PW, Arnold J, Oesterling B, Vary TC. Insulin-induced activation of pyruvate dehydrogenase complex in skeletal muscle of diabetic rats. Metabolism 1993;42:615-623 (Pubitemid 23141633)
47. Stace PB, Fatania HR, Jackson A, Kerbey AL, Randle PJ. Cyclic AMP and free fatty acids in the longer-term regulation of pyruvate dehydrogenase kinase in rat soleus muscle. Biochim Biophys Acta 1992;1135:201-206
48. Holness MJ, Bulmer K, Gibbons GF, Sugden MC. Up-regulation of pyruvate dehydrogenase kinase isoform 4 (PDK4) protein expression in oxidative skeletal muscle does not require the obligatory participation of peroxisome- proliferator-activated receptor alpha (PPAR). Biochem J 2002;366:839-846
49. Pilegaard H, Ordway GA, Saltin B, Neufer PD, Tunstall RJ, McAinch AJ, Hargreaves M, van Loon LJ, Cameron-Smith D. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 2000;279:E806-E814 (Pubitemid 30951407)
50. Tunstall RJ, McAinch AJ, Hargreaves M, van Loon LJ, Cameron-Smith D. Reduced plasma free fatty acid availability during exercise: effect on gene expression. Eur J Appl Physiol 2007;99:485-493 (Pubitemid 46766841)