Stimulation of muscle anabolism by resistance exercise and ingestion of leucine plus protein

Applied Physiology, Nutrition and Metabolism

Volumn 34, Issue 2, 2009, Pages 151-161

  Tipton, Kevin D ^a,b,c   Elliott, Tabatha A ^a,b,d   Ferrando, Arny A ^a,b,d   Aarsland, Asle A ^a,b   Wolfe, Robert R ^a,b,d  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

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

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Area under the curve; Arteriovenous balance; Branched chain amino acids; Muscle biopsies; Net muscle protein synthesis

Indexed keywords

ESSENTIAL AMINO ACID; INSULIN; LEUCINE; MILK PROTEIN; MUSCLE PROTEIN;

ADULT; ARTICLE; BEVERAGE; BIOSYNTHESIS; BLOOD; BLOOD FLOW; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DRUG EFFECT; FEMALE; HUMAN; LEG; MALE; METABOLISM; MUSCLE CONTRACTION; ORAL DRUG ADMINISTRATION; PROTEIN SYNTHESIS; RANDOMIZED CONTROLLED TRIAL; RESISTANCE TRAINING; SKELETAL MUSCLE; TIME; VASCULARIZATION;

ADMINISTRATION, ORAL; ADULT; AMINO ACIDS, ESSENTIAL; BEVERAGES; FEMALE; HUMANS; INSULIN; LEUCINE; LOWER EXTREMITY; MALE; MILK PROTEINS; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SKELETAL; PROTEIN BIOSYNTHESIS; REGIONAL BLOOD FLOW; RESISTANCE TRAINING; TIME FACTORS; YOUNG ADULT;

EID: 66149138401     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H09-006     Document Type: Article

References (55)

1. Anthony, J.C., Anthony, T.G., and Layman, D.K. 1999. Leucine supplementation enhances skeletal muscle recovery in rats following exercise. J. Nutr. 129: 1102-1106. PMID:10356072.
2. Anthony, J.C., Anthony, T.G., Kimball, S.R., Vary, T.C., and Jefferson, L.S. 2000a. Orally administered leucine stimulates protein synthesis in skeletal muscle of postabsorptive rats in association with increased eIF4F formation. J. Nutr. 130: 139-145. PMID:10720160.
3. Anthony, J.C., Yoshizawa, F., Anthony, T.G., Vary, T.C., Jefferson, L.S., and Kimball, S.R. 2000b. Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J. Nutr. 130: 2413-2419. PMID:11015466.
4. Anthony, J.C., Anthony, T.G., Kimball, S.R., and Jefferson, L.S. 2001. Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J. Nutr. 131: 856S-860S. PMID:11238774.
5. Biolo, G., Fleming, R.Y., Maggi, S.P., and Wolfe, R.R. 1995a. Transmembrane transport and intracellular kinetics of amino acids in human skeletal muscle. Am. J. Physiol. 268: E75-E84. PMID:7840186.
6. Biolo, G., Maggi, S.P., Williams, B.D., Tipton, K.D., and Wolfe, R.R. 1995b. Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am. J. Physiol. 268: E514-E520. PMID:7900797.
7. Biolo, G., Tipton, K.D., Klein, S., and Wolfe, R.R. 1997. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am. J. Physiol. 273: E122-E129. PMID:9252488.
8. Block, K.P., Soemitro, S., Heywood, B.W., and Harper, A.E. 1985. Activation of liver branched-chain alpha-keto acid dehydrogenase in rats by excesses of dietary amino acids. J. Nutr. 115: 1550-1561. PMID:3842801.
9. Bohe, J., Low, J.F., Wolfe, R.R., and Rennie, M.J. 2001. Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. J. Physiol. 532: 575-579. doi:10.1111/j.1469-7793.2001.0575f.x. PMID: 11306673.
10. Bohe, J., Low, A., Wolfe, R.R., and Rennie, M.J. 2003. Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: a dose-response study. J. Physiol. 552: 315-324. doi:10.1113/jphysiol.2003.050674. PMID: 12909668.
11. Bolster, D.R., Jefferson, L.S., and Kimball, S.R. 2004a. Regulation of protein synthesis associated with skeletal muscle hypertrophy by insulin-, amino acidand exercise-induced signalling. Proc. Nutr. Soc. 63: 351-356. doi:10.1079/PNS2004355. PMID:15294054.
12. Bolster, D.R., Vary, T.C., Kimball, S.R., and Jefferson, L.S. 2004b. Leucine regulates translation initiation in rat skeletal muscle via enhanced eIF4G phosphorylation. J. Nutr. 134: 1704-1710. PMID:15226457.
13. Borsheim, E., Tipton, K.D., Wolf, S.E., and Wolfe, R.R. 2002. Essential amino acids and muscle protein recovery from resistance exercise. Am. J. Physiol. Endocrinol. Metab. 283: E648-E657. PMID:12217881.
14. Borsheim, E., Bui, Q.U., Tissier, S., Kobayashi, H., Ferrando, A.A., and Wolfe, R.R. 2008. Effect of amino acid supplementation on muscle mass, strength and physical function in elderly. Clin. Nutr. 27: 189-195. doi:10.1016/j.clnu.2008.01.001. PMID: 18294740.
15. Cuthbertson, D., Smith, K., Babraj, J., Leese, G., Waddell, T., Atherton, P., et al. 2005. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 19: 422-424. PMID:15596483.
16. Dardevet, D., Sornet, C., Balage, M., and Grizard, J. 2000. Stimulation of in vitro rat muscle protein synthesis by leucine decreases with age. J. Nutr. 130: 2630-2635. PMID:11053498.
17. Dardevet, D., Sornet, C., Bayle, G., Prugnaud, J., Pouyet, C., and Grizard, J. 2002. Postprandial stimulation of muscle protein synthesis in old rats can be restored by a leucine-supplemented meal. J. Nutr. 132: 95-100. PMID:11773514.
18. Dreyer, H.C., Drummond, M.J., Pennings, B., Fujita, S., Glynn, E.L., Chinkes, D.L., et al. 2008. Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle. Am. J. Physiol. Endocrinol. Metab. 294: E392-E400. doi:10.1152/ajpendo.00582.2007. PMID:18056791.
19. Elliot, T.A., Cree, M.G., Sanford, A.P., Wolfe, R.R., and Tipton, K.D. 2006. Milk ingestion stimulates net muscle protein synthesis following resistance exercise. Med. Sci. Sports Exerc. 38: 667-674. doi:10.1249/01.mss.0000210190.64458.25. PMID: 16679981.
20. Escobar, J., Frank, J.W., Suryawan, A., Nguyen, H.V., Kimball, S.R., Jefferson, L.S., and Davis, T.A. 2005. Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation. Am. J. Physiol. Endocrinol. Metab. 288: E914-E921. doi:10.1152/ ajpendo.00510.2004. PMID:15644455.
21. Escobar, J., Frank, J.W., Suryawan, A., Nguyen, H.V., Kimball, S.R., Jefferson, L.S., and Davis, T.A. 2006. Regulation of cardiac and skeletal muscle protein synthesis by individual branched-chain amino acids in neonatal pigs. Am. J. Physiol. Endocrinol. Metab. 290: E612-E621. doi:10.1152/ajpendo. 00402.2005. PMID:16278252.
22. Escobar, J., Frank, J.W., Suryawan, A., Nguyen, H.V., and Davis, T.A. 2007. Amino acid availability and age affect the leucine stimulation of protein synthesis and eIF4F formation in muscle. Am. J. Physiol. Endocrinol. Metab. 293: E1615-E1621. doi:10. 1152/ajpendo.00302.2007. PMID:17878223.
23. Gautsch, T.A., Anthony, J.C., Kimball, S.R., Paul, G.L., Layman, D.K., and Jefferson, L.S. 1998. Availability of eIF4E regulates skeletal muscle protein synthesis during recovery from exercise. Am. J. Physiol. 274: C406-C414. PMID:9486130.
24. Hagenfeldt, L., and Wahren, J. 1980. Experimental studies on the metabolic effects of branched chain amino acids. Acta Chir. Scand. Suppl. 498: 88-92. PMID:6776744.
25. Hernandez, J.M., Fedele, M.J., and Farrell, P.A. 2000. Time course evaluation of protein synthesis and glucose uptake after acute resistance exercise in rats. J. Appl. Physiol. 88: 1142-1149. PMID:10710414.
26. Karlsson, H.K., Nilsson, P.A., Nilsson, J., Chibalin, A.V., Zierath, J.R., and Blomstrand, E. 2004. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. Am. J. Physiol. Endocrinol. Metab. 287: E1-E7. doi:10.1152/ajpendo.00430.2003. PMID:14998784.
27. Katsanos, C.S., Kobayashi, H., Sheffield-Moore, M., Aarsland, A., and Wolfe, R.R. 2006. A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Am. J. Physiol. Endocrinol. Metab. 291: E381-E387. doi:10.1152/ajpendo.00488.2005. PMID:16507602.
28. Kimball, S.R., and Jefferson, L.S. 2001. Regulation of protein synthesis by branched-chain amino acids. Curr. Opin. Clin. Nutr. Metab. Care, 4: 39-43. doi:10.1097/00075197-20010100000008. PMID:11122558.
29. Kobayashi, H., Borsheim, E., Anthony, T.G., Traber, D.L., Badalamenti, J., Kimball, S.R., et al. 2003. Reduced amino acid availability inhibits muscle protein synthesis and decreases activity of initiation factor eIF2B. Am. J. Physiol. Endocrinol. Metab. 284: E488-E498. PMID:12556349.
30. Koopman, R., Wagenmakers, A.J., Manders, R.J., Zorenc, A.H., Senden, J.M., Gorselink, M., et al. 2005. Combined ingestion of protein and free leucine with carbohydrate increases postexercise muscle protein synthesis in vivo in male subjects. Am. J. Physiol. Endocrinol. Metab. 288: E645-E653. doi:10.1152/ ajpendo.00413.2004. PMID:15562251.
31. Koopman, R., Verdijk, L., Manders, R.J., Gijsen, A.P., Gorselink, M., Pijpers, E., et al. 2006. Coingestion of protein and leucine stimulates muscle protein synthesis rates to the same extent in young and elderly lean men. Am. J. Clin. Nutr. 84: 623-632. PMID:16960178.
32. Koopman, R., Beelen, M., Stellingwerff, T., Pennings, B., Saris, W.H., Kies, A.K., et al. 2007. Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. Am. J. Physiol. Endocrinol. Metab. 293: E833-E842. doi:10.1152/ajpendo.00135.2007. PMID:17609259.
33. Koopman, R., Verdijk, L.B., Beelen, M., Gorselink, M., Kruseman, A.N., Wagenmakers, A.J., et al. 2008. Coingestion of leucine with protein does not further augment post-exercise muscle protein synthesis rates in elderly men. Br. J. Nutr. 99: 571-580. doi:10.1017/S0007114507812013. PMID:17697406.
34. Kubica, N., Bolster, D.R., Farrell, P.A., Kimball, S.R., and Jefferson, L.S. 2005. Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2Bepsilon mRNA in a mammalian target of rapamycin-dependent manner. J. Biol. Chem. 280: 7570-7580. doi:10.1074/jbc. M413732200. PMID:15591312.
35. Louard, R.J., Barrett, E.J., and Gelfand, R.A. 1990. Effect of infused branched-chain amino acids on muscle and whole-body amino acid metabolism in man. Clin. Sci. 79: 457-466. PMID:2174312.
36. Manninen, A.H. 2006. Hyperinsulinaemia, hyperaminoacidaemia and post-exercise muscle anabolism: the search for the optimal recovery drink. Br. J. Sports Med. 40: 900-905. doi:10.1136/ bjsm.2006.030031. PMID:16950882.
37. Matthews, D.E. 2005. Observations of branched-chain amino acid administration in humans. J. Nutr. 135: 1580S-1584S. PMID:15930473.
38. Miller, S.L., Tipton, K.D., Chinkes, D.L., Wolf, S.E., and Wolfe, R.R. 2003. Independent and combined effects of amino acids and glucose after resistance exercise. Med. Sci. Sports Exerc. 35: 449- 455. doi:10.1249/01.MSS.0000053910.63105.45. PMID: 12618575.
39. Nair, K.S., Matthews, D.E., Welle, S.L., and Braiman, T. 1992a. Effect of leucine on amino acid and glucose metabolism in humans. Metabolism, 41: 643-648. doi:10.1016/0026-0495(92) 90057-H. PMID:1640850.
40. Nair, K.S., Schwartz, R.G., and Welle, S. 1992b. Leucine as a regulator of whole body and skeletal muscle protein metabolism in humans. Am. J. Physiol. 263: E928-E934. PMID:1443126.
41. Phillips, S.M., Tipton, K.D., Aarsland, A., Wolf, S.E., and Wolfe, R.R. 1997. Mixed muscle protein synthesis and breakdown following resistance exercise in humans. Am. J. Physiol. 273(1 Pt 1): E99-E107. PMID:9252485.
42. Rasmussen, B.B., Tipton, K.D., Miller, S.L., Wolf, S.E., and Wolfe, R.R. 2000. An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J. Appl. Physiol. 88: 386-392. PMID:10658002.
43. Rennie, M.J., Bohe, J., and Wolfe, R.R. 2002. Latency, duration and dose response relationships of amino acid effects on human muscle protein synthesis. J. Nutr. 132: 3225S-3227S. PMID:12368422.
44. Rennie, M.J., Bohe, J., Smith, K., Wackerhage, H., and Greenhaff, P. 2006. Branched-chain amino acids as fuels and anabolic signals in human muscle. J. Nutr. 136: 264S-268S. PMID:16365095.
45. Rieu, I., Sornet, C., Bayle, G., Prugnaud, J., Pouyet, C., Balage, M., et al. 2003. Leucine-supplemented meal feeding for ten days beneficially affects postprandial muscle protein synthesis in old rats. J. Nutr. 133: 1198-1205. PMID:12672943.
46. Rieu, I., Balage, M., Sornet, C., Giraudet, C., Pujos, E., Grizard, J., et al. 2006. Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidaemia. J. Physiol. 575: 305-315. doi:10.1113/jphysiol.2006.110742. PMID:16777941.
47. Tipton, K.D., and Sharp, C.P. 2005. The response of intracellular signaling and muscle protein metabolism to nutrition and exercise. Eur. J. Sport Sci. 5: 107-121. doi:10.1080/ 17461390500233607.
48. Tipton, K.D., Ferrando, A.A., Phillips, S.M., Doyle, D., Jr., and Wolfe, R.R. 1999. Postexercise net protein synthesis in human muscle from orally administered amino acids. Am. J. Physiol. 276: E628-E634. PMID:10198297.
49. Tipton, K.D., Rasmussen, B.B., Miller, S.L., Wolf, S.E., Owens-Stovall, S.K., Petrini, B.E., and Wolfe, R.R. 2001. Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise. Am. J. Physiol. Endocrinol. Metab. 281: E197-E206. PMID:11440894.
50. Tipton, K.D., Borsheim, E., Wolf, S.E., Sanford, A.P., and Wolfe, R.R. 2003. Acute response of net muscle protein balance reflects 24-h balance after exercise and amino acid ingestion. Am. J. Physiol. Endocrinol. Metab. 284: E76-E89. PMID:12388164.
51. Tipton, K.D., Elliott, T.A., Cree, M.G., Wolf, S.E., Sanford, A.P., and Wolfe, R.R. 2004. Ingestion of casein and whey proteins result in muscle anabolism after resistance exercise. Med. Sci. Sports Exerc. 36: 2073-2081. doi:10.1249/01.MSS.0000147582. 99810.C5. PMID:15570142.
52. Tipton, K.D., Elliott, T.A., Cree, M.G., Aarsland, A.A., Sanford, A.P., and Wolfe, R.R. 2007. Stimulation of net muscle protein synthesis by whey protein ingestion before and after exercise. Am. J. Physiol. Endocrinol. Metab. 292: E71-E76. doi:10.1152/ ajpendo.00166.2006. PMID:16896166.
53. Wilkinson, S.B., Tarnopolsky, M.A., Macdonald, M.J., MacDonald, J.R., Armstrong, D., and Phillips, S.M. 2007. Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am. J. Clin. Nutr. 85: 1031-1040. PMID:17413102.
54. Wolfe, R.R. 2000. Protein supplements and exercise. Am. J. Clin. Nutr. 72: 551S-557S. PMID:10919959.
55. Wolfe, R.R., and Miller, S. 1999. Amino acid availability controls muscle protein metabolism. Diabetes Nutr. Metab. 5: 322-328. PMID:10741346.