Effect of protein/essential amino acids and resistance training on skeletal muscle hypertrophy: A case for whey protein

Nutrition and Metabolism

Volumn 7, Issue , 2010, Pages

  Hulmi, Juha J ^a   Lockwood, Christopher M ^b   Stout, Jeffrey R ^b  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; ESSENTIAL AMINO ACID; MILK PROTEIN;

DIET SUPPLEMENTATION; EXERCISE RECOVERY; HUMAN; MUSCLE HYPERTROPHY; MUSCLE MASS; PROTEIN INTAKE; PROTEIN SYNTHESIS; RESISTANCE TRAINING; REVIEW; SKELETAL MUSCLE; WHEY;

EID: 77953570638     PISSN: None     EISSN: 17437075     Source Type: Journal    
DOI: 10.1186/1743-7075-7-51     Document Type: Review

References (124)

1. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. American College of Sports Medicine, Med Sci Sports Exerc 2009 41 687 708 10.1249/MSS.0b013e3181915670 19204579
2. Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. G Biolo SP Maggi BD Williams KD Tipton RR Wolfe, Am J Physiol 1995 268 514 20 7900797
3. Postexercise net protein synthesis in human muscle from orally administered amino acids. KD Tipton AA Ferrando SM Phillips D Doyle Jr RR Wolfe, Am J Physiol 1999 276 628 34 10198297
4. Free amino acid pool and muscle protein balance after resistance exercise. HT Pitkänen T Nykanen J Knuutinen K Lahti O Keinanen M Alen PV Komi AA Mero, Med Sci Sports Exerc 2003 35 784 792 10.1249/01.MSS.0000064934. 51751.F9 12750588
5. Stimulation of net muscle protein synthesis by whey protein ingestion before and after exercise. KD Tipton TA Elliott MG Cree AA Aarsland AP Sanford RR Wolfe, Am J Physiol Endocrinol Metab 2007 292 71 6 10.1152/ajpendo.00166.2006 16896166
6. Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. SB Wilkinson MA Tarnopolsky MJ Macdonald JR Macdonald D Armstrong SM Phillips, Am J Clin Nutr 2007 85 1031 1040 17413102
7. Combined ingestion of protein and free leucine with carbohydrate increases postexercise muscle protein synthesis in vivo in male subjects. R Koopman AJ Wagenmakers RJ Manders AH Zorenc JM Senden M Gorselink HA Keizer LJ van Loon, Am J Physiol Endocrinol Metab 2005 288 645 53 10.1152/ajpendo.00413. 2004 15562251
8. Minimal whey protein with carbohydrate stimulates muscle protein synthesis following resistance exercise in trained young men. JE Tang JJ Manolakos GW Kujbida PJ Lysecki DR Moore SM Phillips, Appl Physiol Nutr Metab 2007 32 1132 1138 10.1139/H07-076 18059587
9. Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise. DR Moore JE Tang NA Burd T Rerecich MA Tarnopolsky SM Phillips, J Physiol 2009 587 897 904 10.1113/jphysiol.2008.164087 19124543
10. Whey protein ingestion in elderly persons results in greater muscle protein accrual than ingestion of its constituent essential amino acid content. CS Katsanos DL Chinkes D Paddon-Jones XJ Zhang A Aarsland RR Wolfe, Nutr Res 2008 28 651 658 10.1016/j.nutres.2008.06.007 19083472
11. Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. JE Tang DR Moore GW Kujbida MA Tarnopolsky SM Phillips, J Appl Physiol 2009 107 987 992 10.1152/japplphysiol.00076.2009 19589961
12. The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle strength. LL Andersen G Tufekovic MK Zebis RM Crameri G Verlaan M Kjaer C Suetta P Magnusson P Aagaard, Metabolism 2005 54 151 156 10.1016/j.metabol.2004.07.012 15690307
13. Independent and combined effects of liquid carbohydrate/essential amino acid ingestion on hormonal and muscular adaptations following resistance training in untrained men. SP Bird KM Tarpenning FE Marino, Eur J Appl Physiol 2006 97 225 238 10.1007/s00421-005-0127-z 16456674
14. Effects of whey isolate, creatine, and resistance training on muscle hypertrophy. PJ Cribb AD Williams CG Stathis MF Carey A Hayes, Med Sci Sports Exerc 2007 39 298 307 10.1249/01.mss.0000247002.32589.ef 17277594
15. 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. JW Hartman JE Tang SB Wilkinson MA Tarnopolsky RL Lawrence AV Fullerton SM Phillips, Am J Clin Nutr 2007 86 373 381 17684208
16. The effect of whey protein supplementation with and without creatine monohydrate combined with resistance training on lean tissue mass and muscle strength. DG Burke PD Chilibeck KS Davidson DG Candow J Farthing T Smith-Palmer, Int J Sport Nutr Exerc Metab 2001 11 349 364 11591884
17. Effect of whey and soy protein supplementation combined with resistance training in young adults. DG Candow NC Burke T Smith-Palmer DG Burke, Int J Sport Nutr Exerc Metab 2006 16 233 244 16948480
18. The effects of protein and amino acid supplementation on performance and training adaptations during ten weeks of resistance training. CM Kerksick CJ Rasmussen SL Lancaster B Magu P Smith C Melton M Greenwood AL Almada CP Earnest RB Kreider, J Strength Cond Res 2006 20 643 653 10.1519/R-17695.1 16937979
19. Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength. DS Willoughby JR Stout CD Wilborn, Amino Acids 2007 32 467 477 10.1007/s00726-006-0398-7 16988909
20. Acute and long-term effects of resistance exercise with or without protein ingestion on muscle hypertrophy and gene expression. JJ Hulmi V Kovanen H Selänne WJ Kraemer K Häkkinen AA Mero, Amino Acids 2009 37 297 308 10.1007/s00726-008-0150-6 18661258
21. Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. B Esmarck JL Andersen S Olsen EA Richter M Mizuno M Kjaer, J Physiol 2001 535 301 311 10.1111/j.1469-7793.2001. 00301.x 11507179
22. Effects of supplement timing and resistance exercise on skeletal muscle hypertrophy. PJ Cribb A Hayes, Med Sci Sports Exerc 2006 38 1918 1925 10.1249/01.mss.0000233790.08788.3e 17095924
23. Functional properties of whey, whey components, and essential amino acids: mechanisms underlying health benefits for active people (review). E Ha MB Zemel, J Nutr Biochem 2003 14 251 258 10.1016/S0955-2863(03)00030-5 12832028
24. Manufacture and use of dairy protein fractions. MR Etzel, J Nutr 2004 134 996S 1002S 15051860
25. Emerging health properties of whey proteins and their clinical implications. GW Krissansen, J Am Coll Nutr 2007 26 713S 23S 18187438
26. The effect of whey isolate and resistance training on strength, body composition, and plasma glutamine. PJ Cribb AD Williams MF Carey A Hayes, Int J Sport Nutr Exerc Metab 2006 16 494 509 17240782
27. Proteins and amino acid supplements in exercise and sport. L Bucci L Unlu, Energy-Yielding Macronutrients and Energy Metabolism in Sports Nutrition CRC Press: Boca Raton, FL, Driskell L, Wolinsky I, 2000 191 212
28. Selective muscle hypertrophy, changes in EMG and force, and serum hormones during strength training in older women. K Häkkinen A Pakarinen WJ Kraemer A Häkkinen H Valkeinen M Alen, J Appl Physiol 2001 91 569 580 11457767
29. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. WJ Kraemer K Adams E Cafarelli GA Dudley C Dooly MS Feigenbaum SJ Fleck B Franklin AC Fry JR Hoffman RU Newton J Potteiger MH Stone NA Ratamess T Triplett-McBride American College of Sports Medicine, Med Sci Sports Exerc 2002 34 364 380 10.1097/00005768-200205001-00389 11828249
30. Fundamentals of resistance training: progression and exercise prescription. WJ Kraemer NA Ratamess, Med Sci Sports Exerc 2004 36 674 688 10.1249/01.MSS.0000121945.36635.61 15064596
31. Postexercise myostatin and activin IIb mRNA levels: effects of strength training. JJ Hulmi JP Ahtiainen T Kaasalainen E Pöllänen K Häkkinen M Alen H Selänne V Kovanen AA Mero, Med Sci Sports Exerc 2007 39 289 297 10.1249/01.mss.0000241650.15006.6e 17277593
32. Body Composition and Strength Changes in Women with Milk and Resistance Exercise. AR Josse JE Tang MA Tarnopolsky SM Phillips, Med Sci Sports Exerc 2010 42 1122 1130 19997019
33. Creatine supplementation augments the increase in satellite cell and myonuclei number in human skeletal muscle induced by strength training. S Olsen P Aagaard F Kadi G Tufekovic J Verney JL Olesen C Suetta M Kjaer, J Physiol 2006 573 525 534 10.1113/jphysiol.2006.107359 16581862
34. Oral amino-acid provision does not affect muscle strength or size gains in older men. MP Godard DL Williamson SW Trappe, Med Sci Sports Exerc 2002 34 1126 1131 10.1097/00005768-200207000-00012 12131252
35. Protein supplementation before and after resistance training in older men. DG Candow PD Chilibeck M Facci S Abeysekara GA Zello, Eur J Appl Physiol 2006 97 548 556 10.1007/s00421-006-0223-8 16767436
36. Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. LB Verdijk RA Jonkers BG Gleeson M Beelen K Meijer HH Savelberg WK Wodzig P Dendale LJ van Loon, Am J Clin Nutr 2009 89 608 616 10.3945/ajcn.2008.26626 19106243
37. Resistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men. JJ Hulmi J Tannerstedt H Selänne H Kainulainen V Kovanen AA Mero, J Appl Physiol 2009 106 1720 1729 10.1152/japplphysiol.00087.2009 19299575
38. Effects of resistance exercise and fortified milk on skeletal muscle mass, muscle size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial. S Kukuljan CA Nowson K Sanders RM Daly, J Appl Physiol 2009 107 1864 1873 10.1152/japplphysiol.00392.2009 19850735
39. A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. CS Katsanos H Kobayashi M Sheffield-Moore A Aarsland RR Wolfe, Am J Physiol Endocrinol Metab 2006 291 381 7 10.1152/ajpendo.00488.2005 16507602
40. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. D Cuthbertson K Smith J Babraj G Leese T Waddell P Atherton H Wackerhage PM Taylor MJ Rennie, FASEB J 2005 19 422 424 15596483
41. Dietary protein digestion and absorption rates and the subsequent postprandial muscle protein synthetic response do not differ between young and elderly men. R Koopman S Walrand M Beelen AP Gijsen AK Kies Y Boirie WH Saris LJ van Loon, J Nutr 2009 139 1707 1713 10.3945/jn.109.109173 19625697
42. Variability in muscle size and strength gain after unilateral resistance training. MJ Hubal H Gordish-Dressman PD Thompson TB Price EP Hoffman TJ Angelopoulos PM Gordon NM Moyna LS Pescatello PS Visich RF Zoeller RL Seip PM Clarkson, Med Sci Sports Exerc 2005 37 964 972 10.1097/00005768-200505001-00881 15947721
43. Estimating body fat in NCAA Division I female athletes: a five-compartment model validation of laboratory methods. JR Moon JM Eckerson SE Tobkin AE Smith CM Lockwood AA Walter JT Cramer TW Beck JR Stout, Eur J Appl Physiol 2009 105 119 130 10.1007/s00421-008-0881-9 18936958
44. Effects of amino acid supplementation on muscle soreness and damage. K Nosaka P Sacco K Mawatari, Int J Sport Nutr Exerc Metab 2006 16 620 635 17342883
45. Nutraceutical effects of branched-chain amino acids on skeletal muscle. Y Shimomura Y Yamamoto G Bajotto J Sato T Murakami N Shimomura H Kobayashi K Mawatari, J Nutr 2006 136 529S 532S 16424141
46. Supplementation with a whey protein hydrolysate enhances recovery of muscle force-generating capacity following eccentric exercise. JD Buckley RL Thomson AM Coates PR Howe MO DeNichilo MK Rowney, J Sci Med Sport 2010 13 178 181 10.1016/j.jsams.2008.06.007 18768358
47. Acute milk-based protein-CHO supplementation attenuates exercise-induced muscle damage. E Cockburn PR Hayes DN French E Stevenson A St Clair Gibson, Appl Physiol Nutr Metab 2008 33 775 783 10.1139/H08-057 18641722
48. A single protein meal increases recovery of muscle function following an acute eccentric exercise bout. T Etheridge A Philp PW Watt, Appl Physiol Nutr Metab 2008 33 483 488 10.1139/H08-028 18461101
49. Effect of a proprietary protein supplement on recovery indices following resistance exercise in strength/power athletes. JR Hoffman NA Ratamess CP Tranchina SL Rashti J Kang AD Faigenbaum, Amino Acids 2010 38 771 778 10.1007/s00726-009-0283-2 19347247
50. Liquid carbohydrate/essential amino acid ingestion during a short-term bout of resistance exercise suppresses myofibrillar protein degradation. SP Bird KM Tarpenning FE Marino, Metabolism 2006 55 570 577 10.1016/j.metabol.2005.11. 011 16631431
51. Protein ingestion prior to strength exercise affects blood hormones and metabolism. JJ Hulmi JS Volek H Selänne AA Mero, Med Sci Sports Exerc 2005 37 1990 1997 10.1249/01.mss.0000175912.64126.f9 16286871
52. Human insulinotropic response to oral ingestion of native and hydrolysed whey protein. O Power A Hallihan P Jakeman, Amino Acids 2009 37 333 339 10.1007/s00726-008-0156-0 18679613
53. Post-exercise carbohydrate plus whey protein hydrolysates supplementation increases skeletal muscle glycogen level in rats. M Morifuji A Kanda J Koga K Kawanaka M Higuchi, Amino Acids 2010 38 1109 1115 10.1007/s00726-009-0321-0 19593593
54. Branched-chain amino acid-containing dipeptides, identified from whey protein hydrolysates, stimulate glucose uptake rate in L6 myotubes and isolated skeletal muscles. M Morifuji J Koga K Kawanaka M Higuchi, J Nutr Sci Vitaminol (Tokyo) 2009 55 81 86 10.3177/jnsv.55.81 19352067
55. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. HK Karlsson PA Nilsson J Nilsson AV Chibalin JR Zierath E Blomstrand, Am J Physiol Endocrinol Metab 2004 287 1 7 10.1152/ajpendo.00430.2003 14998784
56. Branched-chain amino acids activate key enzymes in protein synthesis after physical exercise. E Blomstrand J Eliasson HK Karlsson R Kohnke, J Nutr 2006 136 269S 73S 16365096
57. Protein ingestion further augments S6K1 phosphorylation in skeletal muscle following resistance type exercise in males. R Koopman B Pennings AH Zorenc LJ van Loon, J Nutr 2007 137 1880 1886 17634259
58. Leucine. A possible regulator of protein turnover in muscle. MG Buse SS Reid, J Clin Invest 1975 56 1250 1261 10.1172/JCI108201 1237498
59. Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. JC Anthony F Yoshizawa TG Anthony TC Vary LS Jefferson SR Kimball, J Nutr 2000 130 2413 2419 11015466
60. New functions for amino acids: effects on gene transcription and translation. SR Kimball LS Jefferson, Am J Clin Nutr 2006 83 500S 507S 16470021
61. Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells. PJ Atherton K Smith T Etheridge D Rankin MJ Rennie, Amino Acids 2010 38 1533 1539 10.1007/s00726-009-0377-x 19882215
62. Amino acids activate mTOR complex 1 via Ca2+/CaM signaling to hVps34. P Gulati LD Gaspers SG Dann M Joaquin T Nobukuni F Natt SC Kozma AP Thomas G Thomas, Cell Metab 2008 7 456 465 10.1016/j.cmet.2008.03.002 18460336
63. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Y Sancak TR Peterson YD Shaul RA Lindquist CC Thoreen L Bar-Peled DM Sabatini, Science 2008 320 1496 1501 10.1126/science.1157535 18497260
64. Regulation of TORC1 by Rag GTPases in nutrient response. E Kim P Goraksha-Hicks L Li TP Neufeld KL Guan, Nat Cell Biol 2008 10 935 945 10.1038/ncb1753 18604198
65. Amino acid regulation of TOR complex 1. J Avruch X Long S Ortiz-Vega J Rapley A Papageorgiou N Dai, Am J Physiol Endocrinol Metab 2009 296 592 602 10.1152/ajpendo.90645.2008 18765678
66. A MAP4 kinase related to Ste20 is a nutrient-sensitive regulator of mTOR signalling. GM Findlay L Yan J Procter V Mieulet RF Lamb, Biochem J 2007 403 13 20 10.1042/BJ20061881 17253963
67. Inadequate protein intake affects skeletal muscle transcript profiles in older humans. AE Thalacker-Mercer JC Fleet BA Craig NS Carnell WW Campbell, Am J Clin Nutr 2007 85 1344 1352 17490972
68. Genetic analysis of mammalian cyclin-dependent kinases and their inhibitors. M Malumbres S Ortega M Barbacid, Biol Chem 2000 381 827 838 10.1515/BC.2000.105 11076015
69. Cdk2 knockout mice are viable. C Berthet E Aleem V Coppola L Tessarollo P Kaldis, Curr Biol 2003 13 1775 1785 10.1016/j.cub.2003.09.024 14561402
70. The effects of whey protein on myostatin and cell cycle-related gene expression responses to a single heavy resistance exercise bout in trained older men. JJ Hulmi V Kovanen I Lisko H Selänne AA Mero, Eur J Appl Physiol 2008 102 205 213 10.1007/s00421-007-0579-4 17924133
71. The effects of amino acid supplementation on muscular performance during resistance training overreaching. NA Ratamess WJ Kraemer JS Volek MR Rubin AL Gomez DN French MJ Sharman MM McGuigan T Scheett K Häkkinen RU Newton F Dioguardi, J Strength Cond Res 2003 17 250 258 10.1519/1533-4287(2003) 017<0250:TEOAAS>2.0.CO;2 12741860
72. International Society of Sports Nutrition position stand: Nutrient timing. C Kerksick T Harvey J Stout B Campbell C Wilborn R Kreider D Kalman T Ziegenfuss H Lopez J Landis JL Ivy J Antonio, J Int Soc Sports Nutr 2008 5 17 10.1186/1550-2783-5-17 18834505
73. Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise. KD Tipton BB Rasmussen SL Miller SE Wolf SK Owens-Stovall BE Petrini RR Wolfe, Am J Physiol Endocrinol Metab 2001 281 197 206 11440894
74. Postexercise nutrient intake timing in humans is critical to recovery of leg glucose and protein homeostasis. DK Levenhagen JD Gresham MG Carlson DJ Maron MJ Borel PJ Flakoll, Am J Physiol Endocrinol Metab 2001 280 982 93 11350780
75. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. G Biolo KD Tipton S Klein RR Wolfe, Am J Physiol 1997 273 122 9 9252488
76. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. SM Phillips KD Tipton A Aarsland SE Wolf RR Wolfe, Am J Physiol 1997 273 99 107 9252485
77. Exercise training and protein metabolism: influences of contraction, protein intake, and sex-based differences. NA Burd JE Tang DR Moore SM Phillips, J Appl Physiol 2009 106 1692 1701 10.1152/japplphysiol.91351.2008 19036897
78. Effect of protein-supplement timing on strength, power, and body-composition changes in resistance-trained men. JR Hoffman NA Ratamess CP Tranchina SL Rashti J Kang AD Faigenbaum, Int J Sport Nutr Exerc Metab 2009 19 172 185 19478342
79. Slow and fast dietary proteins differently modulate postprandial protein accretion. Y Boirie M Dangin P Gachon MP Vasson JL Maubois B Beaufrere, Proc Natl Acad Sci USA 1997 94 14930 14935 10.1073/pnas.94.26.14930 9405716
80. Time-divided ingestion pattern of casein-based protein supplement stimulates an increase in fat-free body mass during resistance training in young untrained men. A Burk S Timpmann L Medijainen M Vahi V Oopik, Nutr Res 2009 29 405 413 10.1016/j.nutres.2009.03.008 19628107
81. Resistance training alters the response of fed state mixed muscle protein synthesis in young men. JE Tang JG Perco DR Moore SB Wilkinson SM Phillips, Am J Physiol Regul Integr Comp Physiol 2008 294 172 8 18032468
82. Coingestion of carbohydrate and protein hydrolysate stimulates muscle protein synthesis during exercise in young men, with no further increase during subsequent overnight recovery. M Beelen M Tieland AP Gijsen H Vandereyt AK Kies H Kuipers WH Saris R Koopman LJ van Loon, J Nutr 2008 138 2198 2204 10.3945/jn.108.092924 18936219
83. Protein coingestion stimulates muscle protein synthesis during resistance-type exercise. M Beelen R Koopman AP Gijsen H Vandereyt AK Kies H Kuipers WH Saris LJ van Loon, Am J Physiol Endocrinol Metab 2008 295 70 7 10.1152/ajpendo.00774.2007 18430966
84. Essential amino acid and carbohydrate ingestion before resistance exercise does not enhance postexercise muscle protein synthesis. S Fujita HC Dreyer MJ Drummond EL Glynn E Volpi BB Rasmussen, J Appl Physiol 2009 106 1730 1739 10.1152/japplphysiol.90395.2008 18535123
85. Contractile and nutritional regulation of human muscle growth. BB Rasmussen SM Phillips, Exerc Sport Sci Rev 2003 31 127 131 10.1097/00003677- 200307000-00005 12882478
86. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. DR Moore MJ Robinson JL Fry JE Tang EI Glover SB Wilkinson T Prior MA Tarnopolsky SM Phillips, Am J Clin Nutr 2009 89 161 168 10.3945/ajcn.2008.26401 19056590
87. A moderate serving of high-quality protein maximally stimulates skeletal muscle protein synthesis in young and elderly subjects. TB Symons M Sheffield-Moore RR Wolfe D Paddon-Jones, J Am Diet Assoc 2009 109 1582 1586 10.1016/j.jada.2009.06.369 19699838
88. Protein pulse feeding improves protein retention in elderly women. MA Arnal L Mosoni Y Boirie ML Houlier L Morin E Verdier P Ritz JM Antoine J Prugnaud B Beaufrere PP Mirand, Am J Clin Nutr 1999 69 1202 1208 10357740
89. The effect of meal frequency on accumulation of muscle mass and strength during 12 weeks of strength training.[abstract]. T Raastad T Fostervold O Hansen EA Hansen I Garthe E Refsnes, Book of abstracts, ICST 5th Congress, Odense 2006
90. Ingestion of casein and whey proteins result in muscle anabolism after resistance exercise. KD Tipton TA Elliott MG Cree SE Wolf AP Sanford RR Wolfe, Med Sci Sports Exerc 2004 36 2073 2081 10.1249/01.MSS.0000147582.99810.C5 15570142
91. Soy versus whey protein bars: effects on exercise training impact on lean body mass and antioxidant status. EC Brown RA DiSilvestro A Babaknia ST Devor, Nutr J 2004 3 22 10.1186/1475-2891-3-22 15588291
92. Effect of protein source and resistance training on body composition and sex hormones. D Kalman S Feldman M Martinez DR Krieger MJ Tallon, J Int Soc Sports Nutr 2007 4 4 10.1186/1550-2783-4-4 17908338
93. The role of milk- and soy-based protein in support of muscle protein synthesis and muscle protein accretion in young and elderly persons. SM Phillips JE Tang DR Moore, J Am Coll Nutr 2009 28 343 354 20368372
94. Peripheral and splanchnic metabolism of dietary nitrogen are differently affected by the protein source in humans as assessed by compartmental modeling. H Fouillet F Mariotti C Gaudichon C Bos D Tome, J Nutr 2002 132 125 133 11773519
95. Ingestion of a protein hydrolysate is accompanied by an accelerated in vivo digestion and absorption rate when compared with its intact protein. R Koopman N Crombach AP Gijsen S Walrand J Fauquant AK Kies S Lemosquet WH Saris Y Boirie LJ van Loon, Am J Clin Nutr 2009 90 106 115 10.3945/ajcn.2009.27474 19474134
96. The digestion rate of protein is an independent regulating factor of postprandial protein retention. M Dangin Y Boirie C Garcia-Rodenas P Gachon J Fauquant P Callier O Ballevre B Beaufrere, Am J Physiol Endocrinol Metab 2001 280 340 8 11158939
97. The rate of protein digestion affects protein gain differently during aging in humans. M Dangin C Guillet C Garcia-Rodenas P Gachon C Bouteloup-Demange K Reiffers-Magnani J Fauquant O Ballevre B Beaufrere, J Physiol 2003 549 635 644 10.1113/jphysiol.2002.036897 12665610
98. Effects of an omnivorous diet compared with a lactoovovegetarian diet on resistance-training-induced changes in body composition and skeletal muscle in older men. WW Campbell ML Barton Jr D Cyr-Campbell SL Davey JL Beard G Parise WJ Evans, Am J Clin Nutr 1999 70 1032 1039 10584048
99. Effect of protein source on resistive-training-induced changes in body composition and muscle size in older men. MD Haub AM Wells MA Tarnopolsky WW Campbell, Am J Clin Nutr 2002 76 511 517 12197993
100. Aging does not impair the anabolic response to a protein-rich meal. TB Symons SE Schutzler TL Cocke DL Chinkes RR Wolfe D Paddon-Jones, Am J Clin Nutr 2007 86 451 456 17684218
101. Re-evaluation of the whey protein/casein ratio of human milk. C Kunz B Lonnerdal, Acta Paediatr 1992 81 107 112 10.1111/j.1651-2227.1992.tb12184.x 1515752
102. Changes in chemical composition of Alxa bactrian camel milk during lactation. H Zhang J Yao D Zhao H Liu J Li M Guo, J Dairy Sci 2005 88 3402 3410 10.3168/jds.S0022-0302(05)73024-1 16162513
103. In-depth exploration of cow's whey proteome via combinatorial peptide ligand libraries. A D'Amato A Bachi E Fasoli E Boschetti G Peltre H Senechal PG Righetti, J Proteome Res 2009 8 3925 3936 10.1021/pr900221x 19499900
104. Emerging therapeutic potential of whey proteins and peptides. AS Yalcin, Curr Pharm Des 2006 12 1637 1643 10.2174/138161206776843296 16729875
105. Increased availability of leucine with leucine-rich whey proteins improves postprandial muscle protein synthesis in aging rats. I Rieu M Balage C Sornet E Debras S Ripes C Rochon-Bonhomme C Pouyet J Grizard D Dardevet, Nutrition 2007 23 323 331 10.1016/j.nut.2006.12.013 17367997
106. 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. LE Norton DK Layman P Bunpo TG Anthony DV Brana PJ Garlick, J Nutr 2009 139 1103 1109 10.3945/jn.108.103853 19403715
107. Postprandial oxidative losses of free and protein-bound amino acids in the diet: interactions and adaptation. JA Nolles AM Verreijen RE Koopmanschap MW Verstegen VV Schreurs, J Anim Physiol Anim Nutr (Berl) 2008
108. Essential amino acids and muscle protein recovery from resistance exercise. E Borsheim KD Tipton SE Wolf RR Wolfe, Am J Physiol Endocrinol Metab 2002 283 648 57 12217881
109. Effects of flooding amino acids on incorporation of labeled amino acids into human muscle protein. K Smith N Reynolds S Downie A Patel MJ Rennie, Am J Physiol 1998 275 73 8 9688876
110. Influence of the protein digestion rate on protein turnover in young and elderly subjects. M Dangin Y Boirie C Guillet B Beaufrere, J Nutr 2002 132 3228S 33S 12368423
111. Effects of high-calcium diets with different whey proteins on weight loss and weight regain in high-fat-fed C57BL/6J mice. TK Pilvi S Harala R Korpela EM Mervaala, Br J Nutr 2009 102 337 341 10.1017/S0007114508199445 19622178
112. Energy nutrients modulate the splanchnic sequestration of dietary nitrogen in humans: a compartmental analysis. H Fouillet C Gaudichon F Mariotti C Bos JF Huneau D Tome, Am J Physiol Endocrinol Metab 2001 281 248 60 11440900
113. Gastric emptying, gastric secretion and enterogastrone response after administration of milk proteins or their peptide hydrolysates in humans. JA Calbet JJ Holst, Eur J Nutr 2004 43 127 139 10.1007/s00394-004-0448-4 15168035
114. Milk ingestion stimulates net muscle protein synthesis following resistance exercise. TA Elliot MG Cree AP Sanford RR Wolfe KD Tipton, Med Sci Sports Exerc 2006 38 667 674 10.1249/01.mss.0000210190.64458.25 16679981
115. Characterization of dried whey protein concentrate and isolate flavor. ME Carunchia Whetstine AE Croissant MA Drake, J Dairy Sci 2005 88 3826 3839 10.3168/jds.S0022-0302(05)73068-X 16230688
116. Protein hydrolysates in sports nutrition. AH Manninen, Nutr Metab (Lond) 2009 6 38 10.1186/1743-7075-6-38 19785737
117. Enzymatic hydrolysis of whey proteins. II. Molecular-weight range. PG Tello F Camacho E Jurado MP Paez EM Guadix, Biotechnol Bioeng 1994 44 529 532 10.1002/bit.260440416 18618787 (Pubitemid 24231208)
118. Differential stimulation of muscle protein synthesis in elderly humans following isocaloric ingestion of amino acids or whey protein. D Paddon-Jones M Sheffield-Moore CS Katsanos XJ Zhang RR Wolfe, Exp Gerontol 2006 41 215 219 10.1016/j.exger.2005.10.006 16310330 (Pubitemid 43165694)
119. Peptide transporters: structure, function, regulation and application for drug delivery. T Terada K Inui, Curr Drug Metab 2004 5 85 94 10.2174/1389200043489153 14965252
120. The role of nutrition in stimulating muscle protein accretion at the molecular level. SR Kimball, Biochem Soc Trans 2007 35 1298 1301 10.1042/BST0351298 17956335
121. Leucine as a regulator of whole body and skeletal muscle protein metabolism in humans. KS Nair RG Schwartz S Welle, Am J Physiol 1992 263 928 34 1443126
122. Co-ingestion of leucine with protein does not further augment post-exercise muscle protein synthesis rates in elderly men. R Koopman LB Verdijk M Beelen M Gorselink AN Kruseman AJ Wagenmakers H Kuipers LJ van Loon, Br J Nutr 2007 1 10
123. Stimulation of muscle anabolism by resistance exercise and ingestion of leucine plus protein. KD Tipton TA Elliott AA Ferrando AA Aarsland RR Wolfe, Appl Physiol Nutr Metab 2009 34 151 161 10.1139/H09-006 19370045
124. Long-term leucine supplementation does not increase muscle mass or strength in healthy elderly men. S Verhoeven K Vanschoonbeek LB Verdijk R Koopman WK Wodzig P Dendale LJ van Loon, Am J Clin Nutr 2009 89 1468 1475 10.3945/ajcn.2008.26668 19321567