Exercise improves skeletal muscle insulin resistance without reduced basal mTOR/S6K1 signaling in rats fed a high-fat diet

European Journal of Applied Physiology

Volumn 111, Issue 11, 2011, Pages 2743-2752

  Liao, Bagen ^a   Xu, Yong ^a  

^a Guangzhou Sports University   (China)

Author keywords

Exercise; High fat diet; Insulin resistance; mTOR; S6K1; Skeletal muscle

Indexed keywords

MTOR PROTEIN, RAT; S6 KINASE; S6K1 PROTEIN, RAT; TARGET OF RAPAMYCIN KINASE;

ANIMAL; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; DRUG EFFECT; EVALUATION; FAT INTAKE; GLUCOSE TOLERANCE TEST; HISTOLOGY; INSULIN RESISTANCE; INTRAABDOMINAL FAT; LIPID DIET; MALE; METABOLISM; ORGAN SIZE; PHOSPHORYLATION; PHYSIOLOGY; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

ANIMALS; BODY WEIGHT; DIET, HIGH-FAT; DIETARY FATS; GLUCOSE TOLERANCE TEST; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; MALE; MUSCLE, SKELETAL; ORGAN SIZE; PHOSPHORYLATION; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84855662246     PISSN: 14396319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00421-011-1892-5     Document Type: Article

References (40)

1. Atherton PJ, Higginson JM, Singh J, Wackerhage H (2004) Concen-trations of signal transduction proteins exercise and insulin responses in rat extensor digitorum longus and soleus muscles. Mol Cell Biochem 261(1):111-116 (Pubitemid 39004524)
2. Chanseaume E, Giraudet C, Gryson C, Walrand S, Rousset P, Boirie Y, Morio B (2007) Enhanced muscle mixed and mitochondrial protein synthesis rates after a high-fat or high-sucrose diet. Obesity 15(4):853-859 (Pubitemid 46740960)
3. Chul-Hee K, Youn JH, Park JY, Hong SK, Park KS, Park SW, Suh KI, Lee KU (2000) Effects of high-fat diet and exercise training on intracellular glucose metabolism in rats. Am J Physiol Endocrinol Metab 278(6):E977-E984 (Pubitemid 30439133)
4. Cleasby ME, Reinten TA, Cooney GJ, James DE, Kraegen EW (2007) Functional studies of Akt isoform specificity in skeletal muscle in vivo; maintained insulin sensitivity despite reduced IRS-1 expression. Mol Endocrinol 21(1):215-228 (Pubitemid 46041701)
5. Corcoran MP, Lamon-Fava S, Fielding RA (2007) Skeletal muscle lipid deposition and insulin resistance: effect of dietary fatty acids and exercise. Am J Clin Nutr 85(3):662-677 (Pubitemid 46393496)
6. de Wilde J, Mohren R, Berg van den S, Boekschoten M, Dijk KW, de Groot P, Muller M, Mariman E, Smit E (2008) Short-term high fat-feeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice. Physiol Genomics 32(3):360-369 (Pubitemid 351328559)
7. de Wilde J, Hulshof MFM, Boekschoten MV, de Groot P, Smit E, Mariman ECM (2010) The embryonic genes Dkk3, Hoxd8, Hoxd9 and Tbx1 identify muscle types in a diet-independent and fiber-type unrelated way. BMC Genomics 11:176. doi:10.1186/ 1471-2164-11-176
8. Dumke CL, Rhodes JS, Garland T Jr, Maslowski E, Swallow JG, Wetter AC, Cartee GD (2001) Genetic selection ofmice for high voluntary wheel running: effect on skeletal muscle glucose uptake. J Appl Physiol 91(3):1289-1297 (Pubitemid 32803925)
9. Hamalxinen N, Pette D (1993) The histochemical profiles of fast fiber Types IIB, ID, and IIA in skeletal muscles of mouse, rat and rabbit. J Histochem Cytochem 41(5):733-737
10. Handschin C, Chin S,Li P, Liu F, Maratos-Flier E, Le Brasseur NK, Yan Z, Spiegelman BM (2007) Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1α muscle-specific knock-out animals. J Biol Chem 282(41):30014-30021 (Pubitemid 350035265)
11. Henrikesen EJ (2002) Effects of acute exercise and exercise training on improved insulin resistance. J Appl Physiol 93(2):788-796
12. Izumiya Y, Hopkins T, Morris C, Sato K, Zeng L, Viereck J, Hamilton JA, Ouchi N, Le Brasseur NK, Walsh K (2008) Fast/ glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab 7(2):159-172 (Pubitemid 351168553)
13. Jensen CB, Storgaard H, Madsbad S, Richter EA, Vaag AA (2007) Altered skeletal muscle fiber composition and size precede whole-body insulin resistance in young men with low birth weight. J Clin Endocrinol Metab 92(4):1530-1534 (Pubitemid 46556435)
14. Kemp JG, Blazev R, Stephenson DG, Stephenson GM (2009) Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond) 33(8):831-841
15. Khamzina L, Veilleux A, Bergeron S, Marette A (2005) Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle ofobese rats: possible involvement in obesity-linked insulin resistance. Endocrinology 146(3):1473-1481 (Pubitemid 40289337)
16. Koopman R, Zorenc AH, Gransier RJ, Cameron-Smith D, van Loon LJ (2006) Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers. Am J Physiol Endocrinol Metab 290(6):E1245-E1252 (Pubitemid 43847910)
17. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7(1):45-56
18. Kraegen EW, Cooney GJ, Turner N (2008) Muscle insulin resistance: a case of fat over-consumption, not mitochondrial dysfunction. PNAS 105(22):7627-7628 (Pubitemid 351872687)
19. Krebs M, Brunmair B, Brehm A, Artwohl M, Szendroedi J, Nowotny P, Roth E, Fürnsinn C, Promintzer M, Anderwald C, Bischof M, Roden M (2007) The mammalian target of rapamycin pathway regulates nutrient-sensitive glucose uptake in man. Diabetes 56(6):1600-1607 (Pubitemid 46842618)
20. Le Bacquer O, Petroulakis E, Paglialunga S, Poulin F, Richard D, Cianflone K, Sonenberg N (2007) Elevated sensitivity to diet-induced obesity and insulin resistance in mice lacking 4E-BP1 and 4E-BP2. J Clin Invest 117(2):387-396 (Pubitemid 46203967)
21. Mc Ainch AJ, Lee JS, Bruce CR, Tunstall RJ, Hawley JA, Cameron-Smith D (2003) Dietary regulation of fat oxidative gene expression in different skeletal muscle fiber types. Obes Res 11(12):1471-1479 (Pubitemid 41127331)
22. Miyazaki M, Esser KA (2009) Cellular mechanisms regulating protein synthesis and skeletal muscle hypertrophy in animals. J Appl Physiol 106(4):1367-1373
23. Oberbach A, Bossenz Y, Lehmann S, Niebauer J, Adams V, Paschke R, Schon MR, Bluher M, Punkt K (2006) Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 29(4):895-900 (Pubitemid 44115313)
24. Pagel-Langenickel I, Bao J, Pang L, Sack MN (2010) The role of mitochondria in the patho-physiology of skeletal muscle insulin resistance. Endocr Rev 31(1):25-51
25. Rasmussen BB, Richter EA (2009) Balancing act between the cellular processes of protein synthesis and breakdown: exercise as a model to understand the molecular mechanisms regulating muscle mass. J Appl Physiol 106(4):1365-1366
26. Reynolds TH IV, Cinquino N, Anthony M, Phelps CB, Berk EZ (2009) Insulin resistance without elevated mammalian target of rapamycin complex 1 activity in muscles of mice fed a high-fat diet. J Appl Physiol 107(5):1479-1485
27. Rivas DA, Yaspelkis BB III, Hawley JA, Lessard SJ (2009) Lipid- induced m TOR activation in rat skeletal muscle reversed by exercise and 5-aminoimidazole-4-carboxamide-1-b-D ribo-furan- oside. J Endocrinol 202(3):441-451
28. Shortreed KE, Krause MP, Huang JH, Dhanani D, Moradi J, Ceddia RB, Hawke TJ (2009) Muscle-specific adaptations, impaired oxidative capacity and maintenance of contractile function characterize diet-induced obese mouse skeletal muscle. PLo S One 4(10):e7293. doi:10.1371/journal.pone.0007293
29. Shulman GJ (2004) Unraveling the cellular mechanism of insulin resistance in humans: new insights from magnetic resonance spectroscopy. Physiology 19(4):183-190
30. Simoneau JA, Kelley DE (1997) Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J Appl Physiol 83(1):166-171
31. Solaro RJ, Pang DC, Briggs FN (1971) The purification of cardiac myofibrils with Triton X-100. Biochim Biophys Acta 245(1): 259-262
32. Suwa M, Kumagai S, Higaki Y, Nakamura T, Katsuta S (2002) Dietary obesity-resistance and muscle oxidative enzyme activ- ities of the fast-twitch fibre dominant rat. Int J Obes Retat Metab Disord 26(6):830-837 (Pubitemid 34620876)
33. Talmadge RJ, Roy RD (1993) Electrophoretic separation of rat skeletal muscle myosin heavy chain isoforms. J Appl Physiol 75(5):2337-2340 (Pubitemid 23352414)
34. Tremblay F, Brûlé S, Hee Um S,Li Y, Masuda K, Roden M, Sun XJ, Krebs M, Polakiewicz RD, Thomas G, Marette A (2007) Identification of IRS-1 Ser-1101 as a target of S6K1 in nutrient- and obesity-induced insulin resistance. PNAS 104(35):14056-14061 (Pubitemid 350003334)
35. Turpin SM, Ryall JG, Southgate R, Danby I, Hevener AL, Febbraio MA, Kemp BE (2009) Examination of lipotoxicity in skeletal muscle of high fat-fed and Ob/Ob mice. J Physiol 587(7):1593-1605
36. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G (2004) Absence of S6K1 protects against age- and diet- induced obesity while enhancing insulin sensitivity. Nature 431(7005): 200-205 (Pubitemid 39243474)
37. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H, Evans RM (2004) Regulation of muscle fiber type and running endurance by PPARd. PLo S Biol 2(10): e294
38. Warmington SA, Tolan R, Mc Bennett S (2000) Functional and histological characteristics of skeletal muscle and the effects of leptin in the genetically obese (ob/ob) mouse. Int J Obes Relat Metab Disord 24(8):1040-1050 (Pubitemid 30618125)
39. Weng QR, Kozlowski M, Belham C, Zhang A, Comb MJ, Auruch J (1998) Regulation of the P70 S6 kinase by phosphorylation in vivo. Analysis using site-specific anti-phosphopeptide antibod-ies. J Biol Chem 273(26):16621-16629 (Pubitemid 28311452)
40. Yang C, Farberman A, Rideout TC, de Lange CFM, France J, Fan MZ (2008) The mammalian target of rapamycin-signaling pathway in regulating metabolism and growth. J Anim Sci 86(E. Suppl):E36-E50