Amino acids are necessary for the insulin-induced activation of mTOR/S6K1 signaling and protein synthesis in healthy and insulin resistant human skeletal muscle

Clinical Nutrition

Volumn 27, Issue 3, 2008, Pages 447-456

  Drummond, Micah J ^a   Bell, Jill A ^c   Fujita, Satoshi ^b   Dreyer, Hans C ^a   Glynn, Erin L ^a   Volpi, Elena ^b   Rasmussen, Blake B ^a,c  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Adenosine 5 monophosphate activated protein kinase; Amino acid availability; Mammalian target of rapamycin; Muscle protein synthesis

Indexed keywords

AMINO ACID; INITIATION FACTOR 2ALPHA; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; SERINE;

ADULT; ARTICLE; CATHETERIZATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLUCOSE TRANSPORT; HUMAN; IMMUNOBLOTTING; INSULIN INFUSION; INSULIN RESISTANCE; KINETICS; LEG MUSCLE; MALE; MUSCLE BIOPSY; NEGATIVE FEEDBACK; NON INSULIN DEPENDENT DIABETES MELLITUS; NUTRIENT AVAILABILITY; PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ADULT; AMINO ACIDS; CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 2; FEMALE; GLUCOSE CLAMP TECHNIQUE; HUMANS; INSULIN; INSULIN RESISTANCE; MALE; MUSCLE, SKELETAL; PROTEIN BIOSYNTHESIS; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 46549084953     PISSN: 02615614     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.clnu.2008.01.012     Document Type: Article

References (46)

1. World Health Organization Global Strategy on Diet, Physical Activity, and Health (2003), World Health Organization (WHO). http://www.who.int/dietphysicalactivity/en Accessed September 10, 2006
2. Must A., Spadano J., Coakley E.H., Field A.E., Colditz G., and Dietz W.H. The disease burden associated with overweight and obesity. JAMA 282 (1999) 1523-1529
3. Tappy L., and D'Alessio D. Obesity and insulin resistance: is it due to body fat, energy balance, or gut factors?. Curr Opin Clin Nutr Metab Care 9 (2006) 455-457
4. Felig P., Marliss E., and Cahill Jr. G.F. Plasma amino acid levels and insulin secretion in obesity. N Engl J Med 281 (1969) 811-816
5. Felig P., Wahren J., Hendler R., and Brundin T. Splanchnic glucose and amino acid metabolism in obesity. J Clin Invest 53 (1974) 582-590
6. Boden G., and Tappy L. Effects of amino acids on glucose disposal. Diabetes 39 (1990) 1079-1084
7. Tappy L., Acheson K., Normand S., Schneeberger D., Thelin A., Pachiaudi C., et al. Effects of infused amino acids on glucose production and utilization in healthy human subjects. Am J Physiol 262 (1992) E826-E833
8. Abumrad N.N., Robinson R.P., Gooch B.R., and Lacy W.W. The effect of leucine infusion on substrate flux across the human forearm. J Surg Res 32 (1982) 453-463
9. Schwenk W.F., and Haymond M.W. Decreased uptake of glucose by human forearm during infusion of leucine, isoleucine, or threonine. Diabetes 36 (1987) 199-204
10. Tessari P., Inchiostro S., Biolo G., Duner E., Nosadini R., Tiengo A., et al. Hyperaminoacidaemia reduces insulin-mediated glucose disposal in healthy man. Diabetologia 28 (1985) 870-872
11. Krebs M., Krssak M., Bernroider E., Anderwald C., Brehm A., Meyerspeer M., et al. Mechanism of amino acid-induced skeletal muscle insulin resistance in humans. Diabetes 51 (2002) 599-605
12. Peters A.L., and Davidson M.B. Protein and fat effects on glucose responses and insulin requirements in subjects with insulin-dependent diabetes mellitus. Am J Clin Nutr 58 (1993) 555-560
13. Pisters P.W., Restifo N.P., Cersosimo E., and Brennan M.F. The effects of euglycemic hyperinsulinemia and amino acid infusion on regional and whole body glucose disposal in man. Metabolism 40 (1991) 59-65
14. Buckspan R., Hoxworth B., Cersosimo E., Devlin J., Horton E., and Abumrad N. alpha-Ketoisocaproate is superior to leucine in sparing glucose utilization in humans. Am J Physiol 251 (1986) E648-E653
15. Flakoll P.J., Wentzel L.S., Rice D.E., Hill J.O., and Abumrad N.N. Short-term regulation of insulin-mediated glucose utilization in four-day fasted human volunteers: role of amino acid availability. Diabetologia 35 (1992) 357-366
16. Patti M.E., Brambilla E., Luzi L., Landaker E.J., and Kahn C.R. Bidirectional modulation of insulin action by amino acids. J Clin Invest 101 (1998) 1519-1529
17. Khamzina L., Veilleux A., Bergeron S., and Marette A. Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology 146 (2005) 1473-1481
18. Tremblay F., and Marette A. Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle cells. J Biol Chem 276 (2001) 38052-38060
19. Kimball S.R., Farrell P.A., and Jefferson L.S. Invited Review: Role of insulin in translational control of protein synthesis in skeletal muscle by amino acids or exercise. J Appl Physiol 93 (2002) 1168-1180
20. Kimball S.R., and Jefferson L.S. Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J Nutr 136 (2006) 227S-231S
21. Byfield M.P., Murray J.T., and Backer J.M. hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem 280 (2005) 33076-33082
22. Nobukuni T., Joaquin M., Roccio M., Dann S.G., Kim S.Y., Gulati P., et al. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc Natl Acad Sci USA 102 (2005) 14238-14243
23. Um S.H., Frigerio F., Watanabe M., Picard F., Joaquin M., Sticker M., et al. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431 (2004) 200-205
24. Tremblay F., Krebs M., Dombrowski L., Brehm A., Bernroider E., Roth E., et al. Overactivation of S6 kinase 1 as a cause of human insulin resistance during increased amino acid availability. Diabetes 54 (2005) 2674-2684
25. Bell J.A., Fujita S., Volpi E., Cadenas J.G., and Rasmussen B.B. Short-term insulin and nutritional energy provision do not stimulate muscle protein synthesis if blood amino acid availability decreases. Am J Physiol Endocrinol Metab 289 (2005) E999-E1006
26. Fujita S., Rasmussen B.B., Cadenas J.G., Grady J.J., and Volpi E. Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. Am J Physiol Endocrinol Metab 291 (2006) E745-E754
27. Tessari P., Inchiostro S., Biolo G., Vincenti E., and Sabadin L. Effects of acute systemic hyperinsulinemia on forearm muscle proteolysis in healthy man. J Clin Invest 88 (1991) 27-33
28. Nygren J., and Nair K.S. Differential regulation of protein dynamics in splanchnic and skeletal muscle beds by insulin and amino acids in healthy human subjects. Diabetes 52 (2003) 1377-1385
29. Bell J.A., Volpi E., Fujita S., Cadenas J.G., and Rasmussen B.B. Dysregulation of muscle fatty acid metabolism in type 2 diabetes is independent of malonyl-CoA. Diabetologia 49 (2006) 2144-2152
30. Bell J.A., Volpi E., Fujita S., Cadenas J.G., Sheffield-Moore M., and Rasmussen B.B. Skeletal muscle protein anabolic response to increased energy and insulin is preserved in poorly controlled type 2 diabetes. J Nutr 136 (2006) 1249-1255
31. Wolfe R.R., and Chinkes D.L. Isotope tracers in metabolic research principles and practice of kinetic analysis. 2nd ed. (2005), Wiley-Liss, Hobokon, NJ
32. Wang X., and Proud C.G. The mTOR pathway in the control of protein synthesis. Physiology (Bethesda) 21 (2006) 362-369
33. Volpi E., Sheffield-Moore M., Rasmussen B.B., and Wolfe R.R. Basal muscle amino acid kinetics and protein synthesis in healthy young and older men. JAMA 286 (2001) 1206-1212
34. Cherel Y., Attaix D., Rosolowska-Huszcz D., Belkhou R., Robin J.P., Arnal M., et al. Whole-body and tissue protein synthesis during brief and prolonged fasting in the rat. Clin Sci (Lond) 81 (1991) 611-619
35. Volpi E., Kobayashi H., Sheffield-Moore M., Mittendorfer B., and Wolfe R.R. Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am J Clin Nutr 78 (2003) 250-258
36. Smith K., Reynolds N., Downie S., Patel A., and Rennie M.J. Effects of flooding amino acids on incorporation of labeled amino acids into human muscle protein. Am J Physiol 275 (1998) E73-E78
37. Anthony T.G., Reiter A.K., Anthony J.C., Kimball S.R., and Jefferson L.S. Deficiency of dietary EAA preferentially inhibits mRNA translation of ribosomal proteins in liver of meal-fed rats. Am J Physiol Endocrinol Metab 281 (2001) E430-E439
38. O'Connor P.M., Kimball S.R., Suryawan A., Bush J.A., Nguyen H.V., Jefferson L.S., et al. Regulation of translation initiation by insulin and amino acids in skeletal muscle of neonatal pigs. Am J Physiol Endocrinol Metab 285 (2003) E40-E53
39. Biolo G., Williams B.D., Fleming R.Y., and Wolfe R.R. Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes 48 (1999) 949-957
40. Crozier S.J., Kimball S.R., Emmert S.W., Anthony J.C., and Jefferson L.S. Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J Nutr 135 (2005) 376-382
41. Anthony J.C., Anthony T.G., Kimball S.R., Vary T.C., and Jefferson L.S. Orally administered leucine stimulates protein synthesis in skeletal muscle of postabsorptive rats in association with increased eIF4F formation. J Nutr 130 (2000) 139-145
42. Fujita S., Dreyer H.C., Drummond M.J., Glynn E.L., Cadenas J.G., Yoshizawa F., et al. Nutrient signalling in the regulation of human muscle protein synthesis. J Physiol 582 (2007) 813-823
43. Liberman Z., and Eldar-Finkelman H. Serine 332 phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 attenuates insulin signaling. J Biol Chem 280 (2005) 4422-4428
44. Thong F.S., Bilan P.J., and Klip A. The Rab GTPase-activating protein AS160 integrates Akt, protein kinase C, and AMP-activated protein kinase signals regulating GLUT4 traffic. Diabetes 56 (2007) 414-423
45. Terruzzi I., Allibardi S., Bendinelli P., Maroni P., Piccoletti R., Vesco F., et al. Amino acid- and lipid-induced insulin resistance in rat heart: molecular mechanisms. Mol Cell Endocrinol 190 (2002) 135-145
46. Hillier T.A., Fryburg D.A., Jahn L.A., and Barrett E.J. Extreme hyperinsulinemia unmasks insulin's effect to stimulate protein synthesis in the human forearm. Am J Physiol 274 (1998) E1067-E1074