Exercise in ZDF rats does not attenuate weight gain, but prevents hyperglycemia concurrent with modulation of amino acid metabolism and AKT/mTOR activation in skeletal muscle

European Journal of Nutrition

Volumn 54, Issue 5, 2015, Pages 751-759

  Adegoke, Olasunkanmi A J ^a,b   Bates, Holly E ^c,d   Kiraly, Michael A ^c,e   Vranic, Mladen ^c   Riddell, Michael C ^b   Marliss, Errol B ^a  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b YORK UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d TRENT UNIVERSITY   (Canada)

^e Capilano College   (Canada)

Author keywords

4E BP1; Branched chain amino acids; mRNA translation; Protein metabolism; Ubiquitin protein ligase

Indexed keywords

GLUCOSE; INSULIN; MESSENGER RNA; MUSCLE PROTEIN; PROTEIN KINASE B; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; AMINO ACID; CARRIER PROTEIN; EIF4EBP1 PROTEIN, RAT; MTOR PROTEIN, RAT; PHOSPHOPROTEIN; S6 KINASE; S6K1 PROTEIN, RAT; TARGET OF RAPAMYCIN KINASE;

AMINO ACID BLOOD LEVEL; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CATABOLISM; CONTROLLED STUDY; EXERCISE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; HYPERGLYCEMIA; MALE; NONHUMAN; PROTEIN METABOLISM; PROTEIN SYNTHESIS; RAT; SKELETAL MUSCLE; SWIMMING; WEIGHT GAIN; ZUCKER DIABETIC FATTY RAT; ANIMAL; BLOOD; GENETICS; METABOLISM; OBESITY; PHOSPHORYLATION;

RATTUS;

AMINO ACIDS; ANIMALS; CARRIER PROTEINS; HYPERGLYCEMIA; MALE; MUSCLE, SKELETAL; OBESITY; PHOSPHOPROTEINS; PHOSPHORYLATION; PHYSICAL CONDITIONING, ANIMAL; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RIBOSOMAL PROTEIN S6 KINASES; RNA, MESSENGER; TOR SERINE-THREONINE KINASES; WEIGHT GAIN;

EID: 84937521873     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-014-0754-4     Document Type: Article

References (51)

1. Chevalier S, Marliss EB, Morais JA, Lamarche M, Gougeon R (2005) Whole-body protein anabolic response is resistant to the action of insulin in obese women. Am J Clin Nutr 82(2):355–365
2. Gougeon R, Pencharz PB, Marliss EB (1994) Effect of NIDDM on the kinetics of whole-body protein metabolism. Diabetes 43(2):318–328
3. Gougeon R, Styhler K, Morais JA, Jones PJ, Marliss EB (2000) Effects of oral hypoglycemic agents and diet on protein metabolism in type 2 diabetes. Diabetes Care 23(1):1–8
4. Chevalier S, Gougeon R, Choong N, Lamarche M, Morais JA (2006) Influence of adiposity in the blunted whole-body protein anabolic response to insulin with aging. J Gerontol A Biol Sci Med Sci 61(2):156–164
5. Guillet C, Delcourt I, Rance M, Giraudet C, Walrand S, Bedu M, Duche P, Boirie Y (2009) Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men. J Clin Endocrinol Metab 94(8):3044–3050. doi:10.1210/jc.2008-2216
6. Gougeon R, Marliss EB, Jones PJ, Pencharz PB, Morais JA (1998) Effect of exogenous insulin on protein metabolism with differing nonprotein energy intakes in Type 2 diabetes mellitus. Int J Obes Relat Metab Disord 22(3):250–261
7. Pereira S, Marliss EB, Morais JA, Chevalier S, Gougeon R (2008) Insulin resistance of protein metabolism in type 2 diabetes. Diabetes 57(1):56–63. doi:10.2337/db07-0887
8. Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, Lien LF, Haqq AM, Shah SH, Arlotto M, Slentz CA, Rochon J, Gallup D, Ilkayeva O, Wenner BR, Yancy WS Jr, Eisenson H, Musante G, Surwit RS, Millington DS, Butler MD, Svetkey LP (2009) A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 9(4):311–326
9. Tai ES, Tan ML, Stevens RD, Low YL, Muehlbauer MJ, Goh DL, Ilkayeva OR, Wenner BR, Bain JR, Lee JJ, Lim SC, Khoo CM, Shah SH, Newgard CB (2010) Insulin resistance is associated with a metabolic profile of altered protein metabolism in Chinese and Asian-Indian men. Diabetologia 53(4):757–767
10. Holloszy JO (2005) Exercise-induced increase in muscle insulin sensitivity. J Appl Physiol 99(1):338–343
11. Marliss EB, Vranic M (2002) Intense exercise has unique effects on both insulin release and its roles in glucoregulation: implications for diabetes. Diabetes 51(Suppl 1):S271–S283
12. Zinman B, Ruderman N, Campaigne BN, Devlin JT, Schneider SH (2004) Physical activity/exercise and diabetes. Diabetes Care 27(Suppl 1):S58–S62
13. Diabetes Prevention Program (DPP) Research Group (2002) The Diabetes Prevention Program (DPP): description of lifestyle intervention. Diabetes Care 25(12):2165–2171
14. Delahanty LM, Nathan DM (2008) Implications of the diabetes prevention program and Look AHEAD clinical trials for lifestyle interventions. J Am Diet Assoc 108(4 Suppl 1):S66–S72. doi:10.1016/j.jada.2008.01.026
15. Peterson RG, Shaw WN, Neel M-A, Little LA, Eichberg J (1990) Zucker diabetic fatty rat as a model for non-insulin-dependent diabetes mellitus. ILAR 32(3):16–19
16. Finegood DT, McArthur MD, Kojwang D, Thomas MJ, Topp BG, Leonard T, Buckingham RE (2001) Beta-cell mass dynamics in Zucker diabetic fatty rats. Rosiglitazone prevents the rise in net cell death. Diabetes 50(5):1021–1029
17. Kiraly MA, Bates HE, Kaniuk NA, Yue JT, Brumell JH, Matthews SG, Riddell MC, Vranic M (2008) Swim training prevents hyperglycemia in ZDF rats: mechanisms involved in the partial maintenance of beta-cell function. Am J Physiol Endocrinol Metab 294(2):E271–E283
18. Kiraly MA, Bates HE, Yue JT, Goche-Montes D, Fediuc S, Park E, Matthews SG, Vranic M, Riddell MC (2007) Attenuation of type 2 diabetes mellitus in the male Zucker diabetic fatty rat: the effects of stress and non-volitional exercise. Metabolism 56(6):732–744
19. Dunn MA, Hartsook EW (1980) Comparative amino acid and protein metabolism in obese and non-obese Zucker rats. J Nutr 110(9):1865–1879
20. She P, Olson KC, Kadota Y, Inukai A, Shimomura Y, Hoppel CL, Adams SH, Kawamata Y, Matsumoto H, Sakai R, Lang CH, Lynch CJ (2013) Leucine and protein metabolism in obese Zucker rats. PLoS One 8(3):e59443. doi:10.1371/journal.pone.0059443
21. Glass DJ (2005) Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37(10):1974–1984
22. Kimball SR, Shantz LM, Horetsky RL, Jefferson LS (1999) Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR-mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6. J Biol Chem 274(17):11647–11652
23. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124(3):471–484. doi:10.1016/j.cell.2006.01.016
24. Mammucari C, Schiaffino S, Sandri M (2008) Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 4(4):524–526
25. Adams SH (2011) Emerging perspectives on essential amino acid metabolism in obesity and the insulin-resistant state. Adv Nutr Int Rev J 2(6):445–456. doi:10.3945/an.111.000737
26. Caballero B, Wurtman RJ (1991) Differential effects of insulin resistance on leucine and glucose kinetics in obesity. Metabolism 40(1):51–58
27. Felig P, Marliss E, Cahill GF Jr (1969) Plasma amino acid levels and insulin secretion in obesity. N Engl J Med 281(15):811–816
28. Adegoke OA, Chevalier S, Morais JA, Gougeon R, Kimball SR, Jefferson LS, Wing SS, Marliss EB (2009) Fed-state clamp stimulates cellular mechanisms of muscle protein anabolism and modulates glucose disposal in normal men. Am J Physiol Endocrinol Metab 296(1):E105–E113
29. Bassil M, Burgos S, Marliss EB, Morais JA, Chevalier S, Gougeon R (2011) Hyperaminoacidaemia at postprandial levels does not modulate glucose metabolism in type 2 diabetes mellitus. Diabetologia 54(7):1810–1818. doi:10.1007/s00125-011-2115-7
30. Wijekoon EP, Skinner C, Brosnan ME, Brosnan JT (2004) Amino acid metabolism in the Zucker diabetic fatty rat: effects of insulin resistance and of type 2 diabetes. Can J Physiol Pharmacol 82(7):506–514. doi:10.1139/y04-067y04-067
31. Abumrad NN, Robinson RP, Gooch BR, Lacy WW (1982) The effect of leucine infusion on substrate flux across the human forearm. J Surg Res 32(5):453–463
32. Tessari P, Inchiostro S, Biolo G, Duner E, Nosadini R, Tiengo A, Crepaldi G (1985) Hyperaminoacidaemia reduces insulin-mediated glucose disposal in healthy man. Diabetologia 28(11):870–872
33. Fiehn O, Garvey WT, Newman JW, Lok KH, Hoppel CL, Adams SH (2010) Plasma metabolomic profiles reflective of glucose homeostasis in non-diabetic and type 2 diabetic obese African-American women. PLoS One 5(12):e15234. doi:10.1371/journal.pone.0015234
34. Laferrere B, Reilly D, Arias S, Swerdlow N, Gorroochurn P, Bawa B, Bose M, Teixeira J, Stevens RD, Wenner BR, Bain JR, Muehlbauer MJ, Haqq A, Lien L, Shah SH, Svetkey LP, Newgard CB (2011) Differential metabolic impact of gastric bypass surgery versus dietary intervention in obese diabetic subjects despite identical weight loss. Sci Transl Med 3(80):80re82. doi:10.1126/scitranslmed.3002043
35. Lackey DE, Lynch CJ, Olson KC, Mostaedi R, Ali M, Smith WH, Karpe F, Humphreys SM, Bedinger DH, Dunn TN, Thomas AP, Oort PJ, Kieffer DA, Amin RH, Bettaieb A, Haj FG, Permana PA, Anthony TG, Adams SH (2013) Regulation of adipose branched chain amino acid catabolism enzyme expression and cross-adipose amino acid flux in human obesity. Am J Physiol Endocrinol Metab. doi:10.1152/ajpendo.00630.2012
36. Campbell JE, Kiraly MA, Atkinson DJ, D’Souza AM, Vranic M, Riddell MC (2010) Regular exercise prevents the development of hyperglucocorticoidemia via adaptations in the brain and adrenal glands in male Zucker diabetic fatty rats. Am J Physiol Regul Integr Comp Physiol 299(1):R168–R176. doi:10.1152/ajpregu.00155.2010
37. Kiraly MA, Campbell J, Park E, Bates HE, Yue JT, Rao V, Matthews SG, Bikopoulos G, Rozakis-Adcock M, Giacca A, Vranic M, Riddell MC (2010) Exercise maintains euglycemia in association with decreased activation of c-Jun NH2-terminal kinase and serine phosphorylation of IRS-1 in the liver of ZDF rats. Am J Physiol Endocrinol Metab 298(3):E671–E682. doi:10.1152/ajpendo.90575.2008
38. Phillips SM (2010) Out-FOX(O)ing proteolysis in sepsis. J physiol 588(Pt 8):1193. doi:10.1113/jphysiol.2010.189498
39. Tremblay F, Lavigne C, Jacques H, Marette A (2007) Role of dietary proteins and amino acids in the pathogenesis of insulin resistance. Annu Rev Nutr 27:293–310
40. Holecek M, Kovarik M (2011) Alterations in protein metabolism and amino acid concentrations in rats fed by a high-protein (casein-enriched) diet—effect of starvation. Food Chem Toxicol 49(12):3336–3342. doi:10.1016/j.fct.2011.09.016
41. Herrero MC, Remesar X, Blade C, Arola L (1997) Muscle amino acid pattern in obese rats. Int J Obes Relat Metab Disord 21(8):698–703
42. Christophe J, Winand J, Kutzner R, Hebbelinck M (1971) Amino acid levels in plasma, liver, muscle, and kidney during and after exercise in fasted and fed rats. Am J Physiol 221(2):453–457
43. Essen-Gustavsson B, Blomstrand E (2002) Effect of exercise on concentrations of free amino acids in pools of type I and type II fibres in human muscle with reduced glycogen stores. Acta Physiol Scand 174(3):275–281
44. Kobayashi R, Shimomura Y, Murakami T, Nakai N, Otsuka M, Arakawa N, Shimizu K, Harris RA (1999) Hepatic branched-chain alpha-keto acid dehydrogenase complex in female rats: activation by exercise and starvation. J Nutr Sci Vitaminol (Tokyo) 45(3):303–309
45. Xu M, Nagasaki M, Obayashi M, Sato Y, Tamura T, Shimomura Y (2001) Mechanism of activation of branched-chain alpha-keto acid dehydrogenase complex by exercise. Biochem Biophys Res Commun 287(3):752–756
46. Thong FS, Derave W, Kiens B, Graham TE, Urso B, Wojtaszewski JF, Hansen BF, Richter EA (2002) Caffeine-induced impairment of insulin action but not insulin signaling in human skeletal muscle is reduced by exercise. Diabetes 51(3):583–590
47. Wojtaszewski JF, Hansen BF, Kiens B, Gade, Markuns JF, Goodyear LJ, Richter EA (2000) Insulin signaling and insulin sensitivity after exercise in human skeletal muscle. Diabetes 49(3):325–331
48. Op den Kamp CM, Langen RC, Snepvangers FJ, de Theije CC, Schellekens JM, Laugs F, Dingemans AM, Schols AM (2013) Nuclear transcription factor kappaB activation and protein turnover adaptations in skeletal muscle of patients with progressive stages of lung cancer cachexia. Am J Clin Nutr. doi:10.3945/ajcn.113.058388
49. Liu HY, Hong T, Wen GB, Han J, Zuo D, Liu Z, Cao W (2009) Increased basal level of Akt-dependent insulin signaling may be responsible for the development of insulin resistance. Am J Physiol Endocrinol Metab 297(4):E898–E906. doi:10.1152/ajpendo.00374.2009
50. Tato I, Bartrons R, Ventura F, Rosa JL (2011) Amino acids activate mammalian target of rapamycin complex 2 (mTORC2) via PI3K/Akt signaling. J Biol Chem 286(8):6128–6142. doi:10.1074/jbc.M110.166991
51. Novellasdemunt L, Tato I, Navarro-Sabate A, Ruiz-Meana M, Mendez-Lucas A, Perales JC, Garcia-Dorado D, Ventura F, Bartrons R, Rosa JL (2013) Akt-dependent activation of the heart 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (PFKFB2) isoenzyme by amino acids. J Biol Chem 288(15):10640–10651. doi:10.1074/jbc.M113.455998