Nutritional regulation of muscle protein synthesis with resistance exercise: Strategies to enhance anabolism

Nutrition and Metabolism

Volumn 9, Issue , 2012, Pages

  Churchward Venne, Tyler A ^a   Burd, Nicholas A ^a   Phillips, Stuart M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Anabolic intramuscular signaling; Hypertrophy; Muscle; Nutrition

Indexed keywords

AMINO ACID; BRANCHED CHAIN AMINO ACID; CARBOHYDRATE; LEUCINE; MUSCLE PROTEIN; PHENYLALANINE; THREONINE;

ATHLETE; CALORIC INTAKE; CARBOHYDRATE INTAKE; FEEDING; HUMAN; INGESTION; LEAN BODY WEIGHT; MACRONUTRIENT; MUSCLE MASS; NUTRITION; POSTPRANDIAL STATE; PROTEIN INTAKE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; RESISTANCE TRAINING; REVIEW; SIGNAL TRANSDUCTION;

EID: 84866366247     PISSN: None     EISSN: 17437075     Source Type: Journal    
DOI: 10.1186/1743-7075-9-40     Document Type: Review

References (89)

1. Exercise training and protein metabolism: influences of contraction, protein intake, and sex-based differences. Burd NA, Tang JE, Moore DR, Phillips SM, J Appl Physiol 2009 106 1692 1701 10.1152/japplphysiol.91351.2008 19036897
2. Human muscle protein synthesis and breakdown during and after exercise. Kumar V, Atherton P, Smith K, Rennie MJ, J Appl Physiol 2009 106 2026 2039 10.1152/japplphysiol.91481.2008 19164770
3. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Biolo G, Tipton KD, Klein S, Wolfe RR, Am J Physiol 1997 273 122 E129 9252488
4. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ, The FASEB journal: official publication of the Federation of American Societies for Experimental Biology 2005 19 422 424 (Pubitemid 40316537)
5. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, Prior T, Tarnopolsky MA, Phillips SM, Am J Clin Nutr 2009 89 161 168 19056590
6. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Pennings B, Boirie Y, Senden JM, Gijsen AP, Kuipers H, van Loon LJ, Am J Clin Nutr 2011 93 997 1005 10.3945/ajcn.110.008102 21367943
7. Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Wilkinson SB, Tarnopolsky MA, Macdonald MJ, Macdonald JR, Armstrong D, Phillips SM, Am J Clin Nutr 2007 85 1031 1040 17413102 (Pubitemid 46557918)
8. Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM, J Appl Physiol 2009 107 987 992 10.1152/japplphysiol.00076.2009 19589961
9. Consumption of fat-free fluid milk after resistance exercise promotes greater lean mass accretion than does consumption of soy or carbohydrate in young, novice, male weightlifters. Hartman JW, Tang JE, Wilkinson SB, Tarnopolsky MA, Lawrence RL, Fullerton AV, Phillips SM, Am J Clin Nutr 2007 86 373 381 17684208 (Pubitemid 47256921)
10. Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise. Tipton KD, Rasmussen BB, Miller SL, Wolf SE, Owens-Stovall SK, Petrini BE, Wolfe RR, Am J Physiol Endocrinol Metab 2001 281 197 E206 11440894
11. Essential amino acid and carbohydrate ingestion before resistance exercise does not enhance postexercise muscle protein synthesis. Fujita S, Dreyer HC, Drummond MJ, Glynn EL, Volpi E, Rasmussen BB, J Appl Physiol 2009 106 1730 1739 10.1152/japplphysiol.90395.2008 18535123
12. Stimulation of muscle anabolism by resistance exercise and ingestion of leucine plus protein. Tipton KD, Elliott TA, Ferrando AA, Aarsland AA, Wolfe RR, Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme 2009 34 151 161 10.1139/H09-006 19370045
13. Excess leucine intake enhances muscle anabolic signaling but not net protein anabolism in young men and women. Glynn EL, Fry CS, Drummond MJ, Timmerman KL, Dhanani S, Volpi E, Rasmussen BB, J Nutr 2010 140 1970 1976 10.3945/jn.110.127647 20844186
14. Co-ingestion of leucine with protein does not further augment post-exercise muscle protein synthesis rates in elderly men. Koopman R, Verdijk LB, Beelen M, Gorselink M, Kruseman AN, Wagenmakers AJ, Kuipers H, van Loon LJ, Br J Nutr 2008 99 571 580 17697406 (Pubitemid 351223425)
15. Bolus arginine supplementation affects neither muscle blood flow nor muscle protein synthesis in young men at rest or after resistance exercise. Tang JE, Lysecki PJ, Manolakos JJ, MacDonald MJ, Tarnopolsky MA, Phillips SM, J Nutr 2011 141 195 200 10.3945/jn.110.130138 21191143
16. Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. Glynn EL, Fry CS, Drummond MJ, Dreyer HC, Dhanani S, Volpi E, Rasmussen BB, Am J Physiol Regul Integr Comp Physiol 2010 299 533 R540 10.1152/ajpregu.00077.2010 20519362
17. Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Staples AW, Burd NA, West DW, Currie KD, Atherton PJ, Moore DR, Rennie MJ, Macdonald MJ, Baker SK, Phillips SM, Medicine and science in sports and exercise 2011 43 1154 1161 10.1249/MSS.0b013e31820751cb 21131864
18. Effect of glucose supplement timing on protein metabolism after resistance training. Roy BD, Tarnopolsky MA, MacDougall JD, Fowles J, Yarasheski KE, J Appl Physiol 1997 82 1882 1888 10.1063/1.365993 9173954 (Pubitemid 27248943)
19. Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise. Borsheim E, Cree MG, Tipton KD, Elliott TA, Aarsland A, Wolfe RR, J Appl Physiol 2004 96 674 678 10.1152/japplphysiol.00333. 2003 14594866 (Pubitemid 38140172)
20. Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. Koopman R, Beelen M, Stellingwerff T, Pennings B, Saris WH, Kies AK, Kuipers H, van Loon LJ, Am J Physiol Endocrinol Metab 2007 293 833 E842 10.1152/ajpendo.00135.2007 17609259 (Pubitemid 47358997)
21. Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise. Moore DR, Tang JE, Burd NA, Rerecich T, Tarnopolsky MA, Phillips SM, J Physiol 2009 587 897 904 10.1113/jphysiol.2008.164087 19124543
22. Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Atherton PJ, Etheridge T, Watt PW, Wilkinson D, Selby A, Rankin D, Smith K, Rennie MJ, Am J Clin Nutr 2010 92 1080 1088 10.3945/ajcn.2010.29819 20844073
23. Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. Bohe J, Low JF, Wolfe RR, Rennie MJ, J Physiol 2001 532 575 579 10.1111/j.1469-7793.2001.0575f.x 11306673 (Pubitemid 32390411)
24. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR, Am J Physiol 1997 273 99 E107 9252485
25. Postexercise net protein synthesis in human muscle from orally administered amino acids. Tipton KD, Ferrando AA, Phillips SM, Doyle D, Wolfe RR, Am J Physiol 1999 276 628 E634 10198297
26. Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle. Dreyer HC, Drummond MJ, Pennings B, Fujita S, Glynn EL, Chinkes DL, Dhanani S, Volpi E, Rasmussen BB, Am J Physiol Endocrinol Metab 2008 294 392 E400 18056791
27. Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24h after resistance exercise in young men. Burd NA, West DW, Moore DR, Atherton PJ, Staples AW, Prior T, Tang JE, Rennie MJ, Baker SK, Phillips SM, J Nutr 2011 141 568 573 10.3945/jn.110.135038 21289204
28. Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. Burd NA, West DW, Staples AW, Atherton PJ, Baker JM, Moore DR, Holwerda AM, Parise G, Rennie MJ, Baker SK, Phillips SM, PLoS One 2010 5 12033 10.1371/journal.pone. 0012033 20711498
29. Coingestion of carbohydrate and protein hydrolysate stimulates muscle protein synthesis during exercise in young men, with no further increase during subsequent overnight recovery. Beelen M, Tieland M, Gijsen AP, Vandereyt H, Kies AK, Kuipers H, Saris WH, Koopman R, van Loon LJ, J Nutr 2008 138 2198 2204 10.3945/jn.108.092924 18936219
30. Groen BB, Res PT, Pennings B, Hertle E, Senden JM, Saris WH, van Loon LJ, Intragastric protein administration stimulates overnight muscle protein synthesis in elderly men American journal of physiology, Endocrinology and metabolism 2011
31. Protein Ingestion Prior To Sleep Improves Post-Exercise Overnight Recovery. Res PT, Groen B, Pennings B, Beelen M, Wallis GA, Gijsen AP, Senden JM, van Loon LJ, Medicine and science in sports and exercise 2012 44 4 692 700 10.1249/MSS.0b013e31823a40ef 21986807
32. Control of translation initiation through integration of signals generated by hormones, nutrients, and exercise. Kimball SR, Jefferson LS, J Biol Chem 2010 285 29027 29032 10.1074/jbc.R110.137208 20576612
33. Mammalian target of rapamycin complex 1 activation is required for the stimulation of human skeletal muscle protein synthesis by essential amino acids. Dickinson JM, Fry CS, Drummond MJ, Gundermann DM, Walker DK, Glynn EL, Timmerman KL, Dhanani S, Volpi E, Rasmussen BB, J Nutr 2011 141 856 862 10.3945/jn.111.139485 21430254
34. Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis. Drummond MJ, Fry CS, Glynn EL, Dreyer HC, Dhanani S, Timmerman KL, Volpi E, Rasmussen BB, J Physiol 2009 587 1535 1546 10.1113/jphysiol.2008.163816 19188252
35. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. Karlsson HK, Nilsson PA, Nilsson J, Chibalin AV, Zierath JR, Blomstrand E, Am J Physiol Endocrinol Metab 2004 287 1 E7 10.1152/ajpendo.00430.2003 14998784 (Pubitemid 38856275)
36. Combined ingestion of protein and free leucine with carbohydrate increases postexercise muscle protein synthesis in vivo in male subjects. Koopman R, Wagenmakers AJ, Manders RJ, Zorenc AH, Senden JM, Gorselink M, Keizer HA, van Loon LJ, Am J Physiol Endocrinol Metab 2005 288 645 E653 15562251
37. Resistance exercise enhances mTOR and MAPK signalling in human muscle over that seen at rest after bolus protein ingestion. Moore DR, Atherton PJ, Rennie MJ, Tarnopolsky MA, Phillips SM, Acta Physiol (Oxf) 2011 201 365 372 10.1111/j.1748-1716.2010.02187.x
38. Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Greenhaff PL, Karagounis LG, Peirce N, Simpson EJ, Hazell M, Layfield R, Wackerhage H, Smith K, Atherton P, Selby A, Rennie MJ, Am J Physiol Endocrinol Metab 2008 295 595 E604 10.1152/ajpendo.90411.2008 18577697
39. A MAP4 kinase related to Ste20 is a nutrient-sensitive regulator of mTOR signalling. Findlay GM, Yan L, Procter J, Mieulet V, Lamb RF, Biochem J 2007 403 13 20 10.1042/BJ20061881 17253963 (Pubitemid 46569862)
40. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Nobukuni T, Joaquin M, Roccio M, Dann SG, Kim SY, Gulati P, Byfield MP, Backer JM, Natt F, Bos JL, et al. Proc Natl Acad Sci USA 2005 102 14238 14243 10.1073/pnas.0506925102 16176982 (Pubitemid 41429682)
41. hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. Byfield MP, Murray JT, Backer JM, J Biol Chem 2005 280 33076 33082 10.1074/jbc.M507201200 16049009 (Pubitemid 41368357)
42. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM, Science 2008 320 1496 1501 10.1126/science.1157535 18497260 (Pubitemid 351929429)
43. An increase in essential amino acid availability upregulates amino acid transporter expression in human skeletal muscle. Drummond MJ, Glynn EL, Fry CS, Timmerman KL, Volpi E, Rasmussen BB, Am J Physiol Endocrinol Metab 2010 298 1011 E1018 10.1152/ajpendo.00690.2009 20304764
44. Skeletal muscle amino acid transporter expression is increased in young and older adults following resistance exercise. Drummond MJ, Fry CS, Glynn EL, Timmerman KL, Dickinson JM, Walker DK, Gundermann DM, Volpi E, Rasmussen BB, J Appl Physiol 2011 111 135 142 21527663
45. Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Hundal HS, Taylor PM, Am J Physiol Endocrinol Metab 2009 296 603 E613 10.1152/ajpendo.91002.2008 19158318
46. Resistance exercise volume affects myofibrillar protein synthesis and anabolic signalling molecule phosphorylation in young men. Burd NA, Holwerda AM, Selby KC, West DW, Staples AW, Cain NE, Cashaback JG, Potvin JR, Baker SK, Phillips SM, J Physiol 2010 588 3119 3130 10.1113/jphysiol.2010.192856 20581041
47. Whey and casein labeled with L-[1-13C]leucine and muscle protein synthesis: effect of resistance exercise and protein ingestion. Reitelseder S, Agergaard J, Doessing S, Helmark IC, Lund P, Kristensen NB, Frystyk J, Flyvbjerg A, Schjerling P, van Hall G, et al. Am J Physiol Endocrinol Metab 2011 300 231 E242 10.1152/ajpendo.00513.2010 21045172
48. The anabolic response to resistance exercise and a protein-rich meal is not diminished by age. Symons TB, Sheffield-Moore M, Mamerow MM, Wolfe RR, Paddon-Jones D, J Nutr Health Aging 2011 15 376 381 10.1007/s12603-010-0319-z 21528164
49. A moderate serving of high-quality protein maximally stimulates skeletal muscle protein synthesis in young and elderly subjects. Symons TB, Sheffield-Moore M, Wolfe RR, Paddon-Jones D, J Am Diet Assoc 2009 109 1582 1586 10.1016/j.jada.2009.06.369 19699838
50. The role of milk- and soy-based protein in support of muscle protein synthesis and muscle protein accretion in young and elderly persons. Phillips SM, Tang JE, Moore DR, J Am Coll Nutr 2009 28 343 354 20368372
51. Slow and fast dietary proteins differently modulate postprandial protein accretion. Boirie Y, Dangin M, Gachon P, Vasson MP, Maubois JL, Beaufrere B, Proc Natl Acad Sci USA 1997 94 14930 14935 10.1073/pnas.94.26.14930 9405716 (Pubitemid 28041477)
52. Greater stimulation of myofibrillar protein synthesis with ingestion of whey protein isolate v. micellar casein at rest and after resistance exercise in elderly men. Burd NA, Yang Y, Moore DR, Tang JE, Tarnopolsky MA, Phillips SM, Br J Nutr 2012 1 5 [Epub ahead of print] 22264449
53. Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. West DW, Burd NA, Coffey VG, Baker SK, Burke LM, Hawley JA, Moore DR, Stellingwerff T, Phillips SM, Am J Clin Nutr 2011 94 795 803 10.3945/ajcn.111.013722 21795443
54. The digestion rate of protein is an independent regulating factor of postprandial protein retention. Dangin M, Boirie Y, Garcia-Rodenas C, Gachon P, Fauquant J, Callier P, Ballevre O, Beaufrere B, Am J Physiol Endocrinol Metab 2001 280 340 E348 11158939
55. Influence of the protein digestion rate on protein turnover in young and elderly subjects. Dangin M, Boirie Y, Guillet C, Beaufrere B, J Nutr 2002 132 3228S 3233S 12368423
56. Leucine incorporation into mixed skeletal muscle protein in humans. Nair KS, Halliday D, Griggs RC, Am J Physiol 1988 254 208 E213 3279803
57. Gut mucosal protein synthesis measured using intravenous and intragastric delivery of stable tracer amino acids. Nakshabendi IM, Obeidat W, Russell RI, Downie S, Smith K, Rennie MJ, Am J Physiol 1995 269 996 E999 8572208
58. Whole body and plasma protein synthesis in exercise and recovery in human subjects. Carraro F, Hartl WH, Stuart CA, Layman DK, Jahoor F, Wolfe RR, Am J Physiol 1990 258 821 E831 2333990
59. Effect of food form on postprandial plasma amino acid concentrations in older adults. Conley TB, Apolzan JW, Leidy HJ, Greaves KA, Lim E, Campbell WW, Br J Nutr 2011 106 203 207 10.1017/S0007114511000419 21554804
60. Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: a dose-response study. Bohe J, Low A, Wolfe RR, Rennie MJ, J Physiol 2003 552 315 324 10.1113/jphysiol.2003.050674 12909668 (Pubitemid 37265489)
61. The leucine content of a complete meal directs peak activation but not duration of skeletal muscle protein synthesis and mammalian target of rapamycin signaling in rats. Norton LE, Layman DK, Bunpo P, Anthony TG, Brana DV, Garlick PJ, J Nutr 2009 139 1103 1109 10.3945/jn.108.103853 19403715
62. Branched-chain amino acids as fuels and anabolic signals in human muscle. Rennie MJ, Bohe J, Smith K, Wackerhage H, Greenhaff P, J Nutr 2006 136 264S 268S 16365095 (Pubitemid 43156521)
63. Nonessential amino acids are not necessary to stimulate net muscle protein synthesis in healthy volunteers. Tipton KD, Gurkin BE, Matin S, Wolfe RR, J Nutr Biochem 1999 10 89 95 10.1016/S0955-2863(98)00087-4 15539275 (Pubitemid 29073633)
64. Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Volpi E, Kobayashi H, Sheffield-Moore M, Mittendorfer B, Wolfe RR, Am J Clin Nutr 2003 78 250 258 12885705 (Pubitemid 39655228)
65. Effects of flooding amino acids on incorporation of labeled amino acids into human muscle protein. Smith K, Reynolds N, Downie S, Patel A, Rennie MJ, Am J Physiol 1998 275 73 E78 9688876
66. Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. Anthony JC, Yoshizawa F, Anthony TG, Vary TC, Jefferson LS, Kimball SR, J Nutr 2000 130 2413 2419 11015466
67. Oral leucine administration stimulates protein synthesis in rat skeletal muscle. Crozier SJ, Kimball SR, Emmert SW, Anthony JC, Jefferson LS, J Nutr 2005 135 376 382 15735066 (Pubitemid 40365191)
68. Regulation of cardiac and skeletal muscle protein synthesis by individual branched-chain amino acids in neonatal pigs. Escobar J, Frank JW, Suryawan A, Nguyen HV, Kimball SR, Jefferson LS, Davis TA, Am J Physiol Endocrinol Metab 2006 290 612 E621 16278252
69. Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells. Atherton PJ, Smith K, Etheridge T, Rankin D, Rennie MJ, Amino Acids 2010 38 1533 1539 10.1007/s00726-009-0377-x 19882215
70. A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR, Am J Physiol Endocrinol Metab 2006 291 381 E387 10.1152/ajpendo.00488.2005 16507602 (Pubitemid 44035298)
71. Leucine supplementation improves muscle protein synthesis in elderly men independently of hyperaminoacidaemia. Rieu I, Balage M, Sornet C, Giraudet C, Pujos E, Grizard J, Mosoni L, Dardevet D, J Physiol 2006 575 305 315 10.1113/jphysiol.2006.110742 16777941 (Pubitemid 44182713)
72. Invited review: Aging and sarcopenia. Doherty TJ, J Appl Physiol 2003 95 1717 1727 12970377 (Pubitemid 37169320)
73. The response of muscle protein anabolism to combined hyperaminoacidemia and glucose-induced hyperinsulinemia is impaired in the elderly. Volpi E, Mittendorfer B, Rasmussen BB, Wolfe RR, J Clin Endocrinol Metab 2000 85 4481 4490 10.1210/jc.85.12.4481 11134097 (Pubitemid 32157622)
74. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ, J Physiol 2009 587 211 217 10.1113/jphysiol.2008.164483 19001042
75. Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia. Wilkes EA, Selby AL, Atherton PJ, Patel R, Rankin D, Smith K, Rennie MJ, Am J Clin Nutr 2009 90 1343 1350 10.3945/ajcn.2009.27543 19740975
76. Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Yang Y, Breen L, Burd NA, Hector AJ, Churchward-Venne TA, Josse AR, Tarnopolsky MA, Phillips SM, Br J Nutr 2012 1 9 [Epub ahead of print] 22264449
77. Long-term leucine supplementation does not increase muscle mass or strength in healthy elderly men. Verhoeven S, Vanschoonbeek K, Verdijk LB, Koopman R, Wodzig WK, Dendale P, van Loon LJ, Am J Clin Nutr 2009 89 1468 1475 10.3945/ajcn.2008.26668 19321567
78. Physiological rise in plasma leucine stimulates muscle protein synthesis in neonatal pigs by enhancing translation initiation factor activation. Escobar J, Frank JW, Suryawan A, Nguyen HV, Kimball SR, Jefferson LS, Davis TA, Am J Physiol Endocrinol Metab 2005 288 914 E921 15644455
79. Amino acid availability and age affect the leucine stimulation of protein synthesis and eIF4F formation in muscle. Escobar J, Frank JW, Suryawan A, Nguyen HV, Davis TA, Am J Physiol Endocrinol Metab 2007 293 1615 E1621 10.1152/ajpendo.00302.2007 17878223 (Pubitemid 350255111)
80. Omega-3 polyunsaturated fatty acids augment the muscle protein anabolic response to hyperinsulinaemia-hyperaminoacidaemia in healthy young and middle-aged men and women. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, Mittendorfer B, Clin Sci (Lond) 2011 121 267 278 10.1042/CS20100597
81. Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Smith GI, Atherton P, Reeds DN, Mohammed BS, Rankin D, Rennie MJ, Mittendorfer B, Am J Clin Nutr 2011 93 402 412 10.3945/ajcn.110.005611 21159787
82. Fish-oil supplementation enhances the effects of strength training in elderly women. Rodacki CL, Rodacki AL, Pereira G, Naliwaiko K, Coelho I, Pequito D, Fernandes LC, Am J Clin Nutr 2012 95 428 436 10.3945/ajcn.111.021915 22218156
83. Milk ingestion stimulates net muscle protein synthesis following resistance exercise. Elliot TA, Cree MG, Sanford AP, Wolfe RR, Tipton KD, Medicine and science in sports and exercise 2006 38 667 674 10.1249/01.mss. 0000210190.64458.25 16679981
84. Independent and combined effects of amino acids and glucose after resistance exercise. Miller SL, Tipton KD, Chinkes DL, Wolf SE, Wolfe RR, Medicine and science in sports and exercise 2003 35 449 455 10.1249/01.MSS. 0000053910.63105.45 12618575 (Pubitemid 36278770)
85. Effect of physiologic hyperinsulinemia on skeletal muscle protein synthesis and breakdown in man. Gelfand RA, Barrett EJ, J Clin Invest 1987 80 1 6 10.1172/JCI113033 3298320 (Pubitemid 17097508)
86. Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Biolo G, Williams BD, Fleming RY, Wolfe RR, Diabetes 1999 48 949 957 10.2337/diabetes.48.5.949 10331397 (Pubitemid 29226339)
87. Influence of differing macronutrient intakes on muscle glycogen resynthesis after resistance exercise. Roy BD, Tarnopolsky MA, J Appl Physiol 1998 84 890 896 9480948 (Pubitemid 28110617)
88. Glycogen resynthesis in skeletal muscle following resistive exercise. Pascoe DD, Costill DL, Fink WJ, Robergs RA, Zachwieja JJ, Medicine and science in sports and exercise 1993 25 349 354 8455450 (Pubitemid 23086630)
89. Nutritional modulation of training-induced skeletal muscle adaptations. Hawley JA, Burke LM, Phillips SM, Spriet LL, J Appl Physiol 2011 110 834 845 10.1152/japplphysiol.00949.2010 21030665