Recent perspectives regarding the role of dietary protein for the promotion of muscle hypertrophy with resistance exercise training

Nutrients

Volumn 10, Issue 2, 2018, Pages

  Stokes, Tanner ^a   Hector, Amy J ^a   Morton, Robert W ^a   McGlory, Chris ^a   Phillips, Stuart M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Amino acids; Energy balance; Energy restriction; Muscle hypertrophy; Protein turnover; Resistance exercise; Skeletal muscle

Indexed keywords

AMINO ACID RECEPTOR STIMULATING AGENT; BRANCHED CHAIN AMINO ACID AMINOTRANSFERASE; CASEIN; CHOLECYSTOKININ; DIPEPTIDYL PEPTIDASE IV; GLUCAGON LIKE PEPTIDE 1; GLYCOGEN; GROWTH PROMOTOR; LEUCINE; MUSCLE PROTEIN; PHENYLALANINE; TYROSINE;

AMINOACIDEMIA; AUTOPHAGY; BODY MASS; DIET SUPPLEMENTATION; ENERGY BALANCE; ENERGY YIELD; GENDER; HUMAN; MACROMOLECULE; MUSCLE EXCITATION; MUSCLE HYPERTROPHY; MUSCLE MASS; PROTEIN DEGRADATION; PROTEIN INTAKE; PROTEIN SYNTHESIS; RESISTANCE TRAINING; REVIEW; SIGNAL TRANSDUCTION; SIX MINUTE WALK TEST; SKELETAL MUSCLE; SPLANCHNIC NERVE; ADMINISTRATION AND DOSAGE; GROWTH, DEVELOPMENT AND AGING; HYPERTROPHY; METABOLISM;

DIETARY PROTEINS; HUMANS; HYPERTROPHY; MUSCLE, SKELETAL; RESISTANCE TRAINING;

EID: 85041817049     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu10020180     Document Type: Review

References (100)

1. Thiebaud, D.; Jacot, E.; DeFronzo, R.A.; Maeder, E.; Jequier, E.; Felber, J.P. The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man. Diabetes 1982, 31, 957–963. [CrossRef] [PubMed]
2. Wang, Z.; Ying, Z.; Bosy-Westphal, A.; Zhang, J.; Schautz, B.; Later, W.; Heymsfield, S.B.; Muller, M.J. Specific metabolic rates of major organs and tissues across adulthood: Evaluation by mechanistic model of resting energy expenditure. Am. J. Clin. Nutr. 2010, 92, 1369–1377. [CrossRef] [PubMed]
3. Morton, R.W.; McGlory, C.; Phillips, S.M. Nutritional interventions to augment resistance training-induced skeletal muscle hypertrophy. Front. Physiol. 2015, 6, 245. [CrossRef] [PubMed]
4. Phillips, S.M. A brief review of critical processes in exercise-induced muscular hypertrophy. Sports Med. 2014, 44, S71–S77. [CrossRef] [PubMed]
5. Phillips, S.M.; Tipton, K.D.; Aarsland, A.; Wolf, S.E.; Wolfe, R.R. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am. J. Physiol. 1997, 273, E99–E107. [CrossRef] [PubMed]
6. Biolo, G.; Tipton, K.D.; Klein, S.; Wolfe, R.R. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am. J. Physiol. 1997, 273, E122–E129. [CrossRef] [PubMed]
7. McNurlan, M.A.; Garlick, P.J. Contribution of rat liver and gastrointestinal tract to whole-body protein synthesis in the rat. Biochem. J. 1980, 186, 381–383. [CrossRef] [PubMed]
8. Nakshabendi, I.M.; McKee, R.; Downie, S.; Russell, R.I.; Rennie, M.J. Rates of small intestinal mucosal protein synthesis in human jejunum and ileum. Am. J. Physiol. 1999, 277, E1028–E1031. [CrossRef] [PubMed]
9. Stoll, B.; Henry, J.; Reeds, P.J.; Yu, H.; Jahoor, F.; Burrin, D.G. Catabolism dominates the first-pass intestinal metabolism of dietary essential amino acids in milk protein-fed piglets. J. Nutr. 1998, 128, 606–614. [PubMed]
10. Stoll, B.; Burrin, D.G.; Henry, J.; Yu, H.; Jahoor, F.; Reeds, P.J. Dietary amino acids are the preferential source of hepatic protein synthesis in piglets. J. Nutr. 1998, 128, 1517–1524. [PubMed]
11. Jackman, S.R.; Witard, O.C.; Philp, A.; Wallis, G.A.; Baar, K.; Tipton, K.D. Branched-chain amino acid ingestion stimulates muscle myofibrillar protein synthesis following resistance exercise in humans. Front. Physiol. 2017, 8, 390. [CrossRef] [PubMed]
12. Hutson, S.M. Subcellular distribution of branched-chain aminotransferase activity in rat tissues. J. Nutr. 1988, 118, 1475–1481. [CrossRef] [PubMed]
13. Suryawan, A.; Hawes, J.W.; Harris, R.A.; Shimomura, Y.; Jenkins, A.E.; Hutson, S.M. A molecular model of human branched-chain amino acid metabolism. Am. J. Clin. Nutr. 1998, 68, 72–81. [CrossRef] [PubMed]
14. Wahren, J.; Felig, P.; Hagenfeldt, L. Effect of protein ingestion on splanchnic and leg metabolism in normal man and in patients with diabetes mellitus. J. Clin. Investig. 1976, 57, 987–999. [CrossRef] [PubMed]
15. Groen, B.B.; Horstman, A.M.; Hamer, H.M.; de Haan, M.; van Kranenburg, J.; Bierau, J.; Poeze, M.; Wodzig, W.K.; Rasmussen, B.B.; van Loon, L.J. Post-prandial protein handling: You are what you just ate. PLoS ONE 2015, 10, e0141582. [CrossRef] [PubMed]
16. Dangin, M.; Guillet, C.; Garcia-Rodenas, C.; Gachon, P.; Bouteloup-Demange, C.; Reiffers-Magnani, K.; Fauquant, J.; Ballevre, O.; Beaufrere, B. The rate of protein digestion affects protein gain differently during aging in humans. J. Physiol. 2003, 549, 635–644. [CrossRef] [PubMed]
17. Schadewaldt, P.; Wendel, U. Metabolism of branched-chain amino acids in maple syrup urine disease. Eur. J. Pediatr. 1997, 156, S62–S66. [CrossRef] [PubMed]
18. Fouillet, H.; Mariotti, F.; Gaudichon, C.; Bos, C.; Tome, D. Peripheral and splanchnic metabolism of dietary nitrogen are differently affected by the protein source in humans as assessed by compartmental modeling. J. Nutr. 2002, 132, 125–133. [CrossRef] [PubMed]
19. Devaraj, S.; Hemarajata, P.; Versalovic, J. The human gut microbiome and body metabolism: Implications for obesity and diabetes. Clin. Chem. 2013, 59, 617–628. [CrossRef] [PubMed]
20. Tang, J.E.; Moore, D.R.; Kujbida, G.W.; Tarnopolsky, M.A.; Phillips, S.M. Ingestion of whey hydrolysate, casein, or soy protein isolate: Effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. J. Appl. Physiol. 2009, 107, 987–992. [CrossRef] [PubMed]
21. Gorissen, S.H.; Horstman, A.M.; Franssen, R.; Crombag, J.J.; Langer, H.; Bierau, J.; Respondek, F.; van Loon, L.J. Ingestion of wheat protein increases in vivo muscle protein synthesis rates in healthy older men in a randomized trial. J. Nutr. 2016, 146, 1651–1659. [CrossRef] [PubMed]
22. Reidy, P.T.; Walker, D.K.; Dickinson, J.M.; Gundermann, D.M.; Drummond, M.J.; Timmerman, K.L.; Cope, M.B.; Mukherjea, R.; Jennings, K.; Volpi, E.; et al. Soy-dairy protein blend and whey protein ingestion after resistance exercise increases amino acid transport and transporter expression in human skeletal muscle. J. Appl. Physiol. 2014, 116, 1353–1364. [CrossRef] [PubMed]
23. Drummond, M.J.; Fry, C.S.; Glynn, E.L.; Timmerman, K.L.; Dickinson, J.M.; Walker, D.K.; Gundermann, D.M.; Volpi, E.; Rasmussen, B.B. Skeletal muscle amino acid transporter expression is increased in young and older adults following resistance exercise. J. Appl. Physiol. 2011, 111, 135–142. [CrossRef] [PubMed]
24. Dreyer, H.C.; Drummond, M.J.; Pennings, B.; Fujita, S.; Glynn, E.L.; Chinkes, D.L.; Dhanani, S.; Volpi, E.; Rasmussen, B.B. 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. 2008, 294, E392–E400. [CrossRef] [PubMed]
25. Bohe, J.; Low, J.F.; Wolfe, R.R.; Rennie, M.J. Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. J. Physiol. 2001, 532, 575–579. [CrossRef] [PubMed]
26. Bohe, J.; Low, A.; Wolfe, R.R.; Rennie, M.J. Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: A dose-response study. J. Physiol. 2003, 552, 315–324. [CrossRef] [PubMed]
27. Atherton, P.J.; Etheridge, T.; Watt, P.W.; Wilkinson, D.; Selby, A.; Rankin, D.; Smith, K.; Rennie, M.J. Muscle full effect after oral protein: Time-dependent concordance and discordance between human muscle protein synthesis and mtorc1 signaling. Am. J. Clin. Nutr. 2010, 92, 1080–1088. [CrossRef] [PubMed]
28. Volpi, E.; Kobayashi, H.; Sheffield-Moore, M.; Mittendorfer, B.; 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. 2003, 78, 250–258. [CrossRef] [PubMed]
29. Anthony, J.C.; Lang, C.H.; Crozier, S.J.; Anthony, T.G.; MacLean, D.A.; Kimball, S.R.; Jefferson, L.S. Contribution of insulin to the translational control of protein synthesis in skeletal muscle by leucine. Am. J. Physiol. Endocrinol. Metab. 2002, 282, E1092–E1101. [CrossRef] [PubMed]
30. Crozier, S.J.; Kimball, S.R.; Emmert, S.W.; Anthony, J.C.; Jefferson, L.S. Oral leucine administration stimulates protein synthesis in rat skeletal muscle. J. Nutr. 2005, 135, 376–382. [CrossRef] [PubMed]
31. Norton, L.E.; Layman, D.K.; Bunpo, P.; Anthony, T.G.; Brana, D.V.; Garlick, P.J. 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. J. Nutr. 2009, 139, 1103–1109. [CrossRef] [PubMed]
32. Churchward-Venne, T.A.; Breen, L.; Di Donato, D.M.; Hector, A.J.; Mitchell, C.J.; Moore, D.R.; Stellingwerff, T.; Breuille, D.; Offord, E.A.; Baker, S.K.; et al. Leucine supplementation of a low-protein mixed macronutrient beverage enhances myofibrillar protein synthesis in young men: A double-blind, randomized trial. Am. J. Clin. Nutr. 2014, 99, 276–286. [CrossRef] [PubMed]
33. Moore, D.R.; Churchward-Venne, T.A.; Witard, O.; Breen, L.; Burd, N.A.; Tipton, K.D.; Phillips, S.M. Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J. Gerontol. A Biol. Sci. Med. Sci. 2015, 70, 57–62. [CrossRef] [PubMed]
34. Churchward-Venne, T.A.; Burd, N.A.; Phillips, S.M. Nutritional regulation of muscle protein synthesis with resistance exercise: Strategies to enhance anabolism. Nutr. Metab. 2012, 9, 40. [CrossRef] [PubMed]
35. Witard, O.C.; Jackman, S.R.; Breen, L.; Smith, K.; Selby, A.; Tipton, K.D. Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. Am. J. Clin. Nutr. 2014, 99, 86–95. [CrossRef] [PubMed]
36. Moore, D.R.; Robinson, M.J.; Fry, J.L.; Tang, J.E.; Glover, E.I.; Wilkinson, S.B.; Prior, T.; Tarnopolsky, M.A.; Phillips, S.M. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am. J. Clin. Nutr. 2009, 89, 161–168. [CrossRef] [PubMed]
37. Areta, J.L.; Burke, L.M.; Ross, M.L.; Camera, D.M.; West, D.W.; Broad, E.M.; Jeacocke, N.A.; Moore, D.R.; Stellingwerff, T.; Phillips, S.M.; et al. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. J. Physiol. 2013, 591, 2319–2331. [CrossRef] [PubMed]
38. Macnaughton, L.S.; Wardle, S.L.; Witard, O.C.; McGlory, C.; Hamilton, D.L.; Jeromson, S.; Lawrence, C.E.; Wallis, G.A.; Tipton, K.D. The response of muscle protein synthesis following whole-body resistance exercise is greater following 40 g than 20 g of ingested whey protein. Physiol. Rep. 2016, 4, e128932. [CrossRef] [PubMed]
39. Groen, B.B.; Res, P.T.; Pennings, B.; Hertle, E.; Senden, J.M.; Saris, W.H.; van Loon, L.J. Intragastric protein administration stimulates overnight muscle protein synthesis in elderly men. Am. J. Physiol. Endocrinol. Metab. 2012, 302, E52–E60. [CrossRef] [PubMed]
40. Beelen, M.; Tieland, M.; Gijsen, A.P.; Vandereyt, H.; Kies, A.K.; Kuipers, H.; Saris, W.H.; Koopman, R.; van Loon, L.J. Coingestion of carbohydrate and protein hydrolysate stimulates muscle protein synthesis during exercise in young men, with no further increase during subsequent overnight recovery. J. Nutr. 2008, 138, 2198–2204. [CrossRef] [PubMed]
41. Res, P.T.; Groen, B.; Pennings, B.; Beelen, M.; Wallis, G.A.; Gijsen, A.P.; Senden, J.M.G.; van Loon, L.J. Protein ingestion before sleep improves postexercise overnight recovery. Med. Sci. Sports Exerc. 2012, 44, 1560–1569. [CrossRef] [PubMed]
42. Holwerda, A.M.; Kouw, I.W.; Trommelen, J.; Halson, S.L.; Wodzig, W.K.; Verdijk, L.B.; van Loon, L.J. Physical activity performed in the evening increases the overnight muscle protein synthetic response to presleep protein ingestion in older men. J. Nutr. 2016, 146, 1307–1314. [CrossRef] [PubMed]
43. Trommelen, J.; Holwerda, A.M.; Kouw, I.W.; Langer, H.; Halson, S.L.; Rollo, I.; Verdijk, L.B.; van Loon, L.J. Resistance exercise augments postprandial overnight muscle protein synthesis rates. Med. Sci. Sports Exerc. 2016, 48, 2517–2525. [CrossRef] [PubMed]
44. Snijders, T.; Res, P.T.; Smeets, J.S.; van Vliet, S.; van Kranenburg, J.; Maase, K.; Kies, A.K.; Verdijk, L.B.; van Loon, L.J. Protein ingestion before sleep increases muscle mass and strength gains during prolonged resistance-type exercise training in healthy young men. J. Nutr. 2015, 145, 1178–1184. [CrossRef] [PubMed]
45. Morton, R.W.; Murphy, K.T.; McKellar, S.R.; Schoenfeld, B.J.; Henselmans, M.; Helms, E.; Aragon, A.A.; Devries, M.C.; Banfield, L.; Krieger, J.W.; et al. A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults. Br. J. Sports Med. 2017. [CrossRef] [PubMed]
46. Cermak, N.M.; Res, P.T.; de Groot, L.C.; Saris, W.H.; van Loon, L.J. Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: A meta-analysis. Am. J. Clin. Nutr. 2012, 96, 1454–1464. [CrossRef] [PubMed]
47. Gibala, M.J.; MacDougall, J.D.; Tarnopolsky, M.A.; Stauber, W.T.; Elorriaga, A. Changes in human skeletal muscle ultrastructure and force production after acute resistance exercise. J. Appl. Physiol. 1995, 78, 702–708. [CrossRef] [PubMed]
48. Damas, F.; Phillips, S.M.; Libardi, C.A.; Vechin, F.C.; Lixandrao, M.E.; Jannig, P.R.; Costa, L.A.; Bacurau, A.V.; Snijders, T.; Parise, G.; et al. Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J. Physiol. 2016, 594, 5209–5222. [CrossRef] [PubMed]
49. Hudson, M.B.; Hosick, P.A.; McCaulley, G.O.; Schrieber, L.; Wrieden, J.; McAnulty, S.R.; Triplett, N.T.; McBride, J.M.; Quindry, J.C. The effect of resistance exercise on humoral markers of oxidative stress. Med. Sci. Sports Exerc. 2008, 40, 542–548. [CrossRef] [PubMed]
50. Wolfe, R.R. Tracers in metabolic research: Radioisotope and stable isotope/mass spectrometry methods. Lab. Res. Methods Biol. Med. 1984, 9, 1–287. [CrossRef] [PubMed]
51. Hartman, J.W.; Moore, D.R.; Phillips, S.M. Resistance training reduces whole-body protein turnover and improves net protein retention in untrained young males. Appl. Physiol. Nutr. Metab. 2006, 31, 557–564. [CrossRef] [PubMed]
52. Moore, D.R.; Del Bel, N.C.; Nizi, K.I.; Hartman, J.W.; Tang, J.E.; Armstrong, D.; Phillips, S.M. Resistance training reduces fasted- and fed-state leucine turnover and increases dietary nitrogen retention in previously untrained young men. J. Nutr. 2007, 137, 985–991. [CrossRef] [PubMed]
53. Tang, J.E.; Perco, J.G.; Moore, D.R.; Wilkinson, S.B.; Phillips, S.M. Resistance training alters the response of fed state mixed muscle protein synthesis in young men. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294, R172–R178. [CrossRef] [PubMed]
54. Azizbeigi, K.; Azarbayjani, M.A.; Peeri, M.; Agha-alinejad, H.; Stannard, S. The effect of progressive resistance training on oxidative stress and antioxidant enzyme activity in erythrocytes in untrained men. Int. J. Sport Nutr. Exerc. Metab. 2013, 23, 230–238. [CrossRef] [PubMed]
55. Deutz, N.E.; Wolfe, R.R. Is there a maximal anabolic response to protein intake with a meal? Clin. Nutr. 2013, 32, 309–313. [CrossRef] [PubMed]
56. Kim, I.Y.; Deutz, N.E.P.; Wolfe, R.R. Update on maximal anabolic response to dietary protein. Clin. Nutr. 2017. [CrossRef] [PubMed]
57. Kimball, S.R.; Jurasinski, C.V.; Lawrence, J.C., Jr.; Jefferson, L.S. Insulin stimulates protein synthesis in skeletal muscle by enhancing the association of eIF-4E and eIF-4G. Am. J. Physiol. 1997, 272, C754–C759. [CrossRef] [PubMed]
58. Greenhaff, P.L.; Karagounis, L.G.; Peirce, N.; Simpson, E.J.; Hazell, M.; Layfield, R.; Wackerhage, H.; Smith, K.; Atherton, P.; Selby, A.; et al. Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. Am. J. Physiol. Endocrinol. Metab. 2008, 295, E595–E604. [CrossRef] [PubMed]
59. Abdulla, H.; Smith, K.; Atherton, P.J.; Idris, I. Role of insulin in the regulation of human skeletal muscle protein synthesis and breakdown: A systematic review and meta-analysis. Diabetologia 2016, 59, 44–55. [CrossRef] [PubMed]
60. Wilkes, E.A.; Selby, A.L.; Atherton, P.J.; Patel, R.; Rankin, D.; Smith, K.; Rennie, M.J. Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia. Am. J. Clin. Nutr. 2009, 90, 1343–1350. [CrossRef] [PubMed]
61. Koopman, R.; Beelen, M.; Stellingwerff, T.; Pennings, B.; Saris, W.H.; Kies, A.K.; Kuipers, H.; van Loon, L.J. Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. Am. J. Physiol. Endocrinol. Metab. 2007, 293, E833–E842. [CrossRef] [PubMed]
62. Staples, A.W.; Burd, N.A.; West, D.W.; Currie, K.D.; Atherton, P.J.; Moore, D.R.; Rennie, M.J.; Macdonald, M.J.; Baker, S.K.; Phillips, S.M. Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Med. Sci. Sports Exerc. 2011, 43, 1154–1161. [CrossRef] [PubMed]
63. Glynn, E.L.; Fry, C.S.; Timmerman, K.L.; Drummond, M.J.; Volpi, E.; Rasmussen, B.B. Addition of carbohydrate or alanine to an essential amino acid mixture does not enhance human skeletal muscle protein anabolism. J. Nutr. 2013, 143, 307–314. [CrossRef] [PubMed]
64. Gorissen, S.H.; Burd, N.A.; Hamer, H.M.; Gijsen, A.P.; Groen, B.B.; van Loon, L.J. Carbohydrate coingestion delays dietary protein digestion and absorption but does not modulate postprandial muscle protein accretion. J. Clin. Endocrinol. Metab. 2014, 99, 2250–2258. [CrossRef] [PubMed]
65. Ivy, J.L.; Goforth, H.W., Jr.; Damon, B.M.; McCauley, T.R.; Parsons, E.C.; Price, T.B. Early postexercise muscle glycogen recovery is enhanced with a carbohydrate-protein supplement. J. Appl. Physiol. 2002, 93, 1337–1344. [CrossRef] [PubMed]
66. Berardi, J.M.; Price, T.B.; Noreen, E.E.; Lemon, P.W. Postexercise muscle glycogen recovery enhanced with a carbohydrate-protein supplement. Med. Sci. Sports Exerc. 2006, 38, 1106–1113. [CrossRef] [PubMed]
67. Burke, L.M.; van Loon, L.J.C.; Hawley, J.A. Postexercise muscle glycogen resynthesis in humans. J. Appl. Physiol. 2017, 122, 1055–1067. [CrossRef] [PubMed]
68. Kim, I.Y.; Schutzler, S.; Schrader, A.; Spencer, H.J.; Azhar, G.; Ferrando, A.A.; Wolfe, R.R. The anabolic response to a meal containing different amounts of protein is not limited by the maximal stimulation of protein synthesis in healthy young adults. Am. J. Physiol. Endocrinol. Metab. 2016, 310, E73–E80. [CrossRef] [PubMed]
69. Symons, T.B.; Sheffield-Moore, M.; Wolfe, R.R.; Paddon-Jones, D. A moderate serving of high-quality protein maximally stimulates skeletal muscle protein synthesis in young and elderly subjects. J. Am. Diet. Assoc. 2009, 109, 1582–1586. [CrossRef] [PubMed]
70. Long, C.L.; Birkhahn, R.H.; Geiger, J.W.; Blakemore, W.S. Contribution of skeletal muscle protein in elevated rates of whole body protein catabolism in trauma patients. Am. J. Clin. Nutr. 1981, 34, 1087–1093. [CrossRef] [PubMed]
71. Kim, I.Y.; Schutzler, S.; Schrader, A.; Spencer, H.; Kortebein, P.; Deutz, N.E.; Wolfe, R.R.; Ferrando, A.A. Quantity of dietary protein intake, but not pattern of intake, affects net protein balance primarily through differences in protein synthesis in older adults. Am. J. Physiol. Endocrinol. Metab. 2015, 308, E21–E28. [CrossRef] [PubMed]
72. Masiero, E.; Agatea, L.; Mammucari, C.; Blaauw, B.; Loro, E.; Komatsu, M.; Metzger, D.; Reggiani, C.; Schiaffino, S.; Sandri, M. Autophagy is required to maintain muscle mass. Cell Metab. 2009, 10, 507–515. [CrossRef] [PubMed]
73. Castets, P.; Lin, S.; Rion, N.; Di Fulvio, S.; Romanino, K.; Guridi, M.; Frank, S.; Tintignac, L.A.; Sinnreich, M.; Ruegg, M.A. Sustained activation of mTORC1 in skeletal muscle inhibits constitutive and starvation-induced autophagy and causes a severe, late-onset myopathy. Cell Metab. 2013, 17, 731–744. [CrossRef] [PubMed]
74. Kitajima, Y.; Tashiro, Y.; Suzuki, N.; Warita, H.; Kato, M.; Tateyama, M.; Ando, R.; Izumi, R.; Yamazaki, M.; Abe, M.; et al. Proteasome dysfunction induces muscle growth defects and protein aggregation. J. Cell Sci. 2014, 127, 5204–5217. [CrossRef] [PubMed]
75. Drummond, M.J.; Addison, O.; Brunker, L.; Hopkins, P.N.; McClain, D.A.; LaStayo, P.C.; Marcus, R.L. Downregulation of E3 ubiquitin ligases and mitophagy-related genes in skeletal muscle of physically inactive, frail older women: A cross-sectional comparison. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69, 1040–1048. [CrossRef] [PubMed]
76. Leger, B.; Cartoni, R.; Praz, M.; Lamon, S.; Deriaz, O.; Crettenand, A.; Gobelet, C.; Rohmer, P.; Konzelmann, M.; Luthi, F.; et al. Akt signalling through GSK-3beta, mtor and foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J. Physiol. 2006, 576, 923–933. [CrossRef] [PubMed]
77. Dhurandhar, E.J.; Kaiser, K.A.; Dawson, J.A.; Alcorn, A.S.; Keating, K.D.; Allison, D.B. Predicting adult weight change in the real world: A systematic review and meta-analysis accounting for compensatory changes in energy intake or expenditure. Int. J. Obes. 2015, 39, 1181–1187. [CrossRef] [PubMed]
78. Magkos, F.; Fraterrigo, G.; Yoshino, J.; Luecking, C.; Kirbach, K.; Kelly, S.C.; de Las Fuentes, L.; He, S.; Okunade, A.L.; Patterson, B.W.; et al. Effects of moderate and subsequent progressive weight loss on metabolic function and adipose tissue biology in humans with obesity. Cell Metab. 2016, 23, 591–601. [CrossRef] [PubMed]
79. Wolfe, R.R. The underappreciated role of muscle in health and disease. Am. J. Clin. Nutr. 2006, 84, 475–482. [PubMed]
80. Pasiakos, S.M.; Vislocky, L.M.; Carbone, J.W.; Altieri, N.; Konopelski, K.; Freake, H.C.; Anderson, J.M.; Ferrando, A.A.; Wolfe, R.R.; Rodriguez, N.R. Acute energy deprivation affects skeletal muscle protein synthesis and associated intracellular signaling proteins in physically active adults. J. Nutr. 2010, 140, 745–751. [CrossRef] [PubMed]
81. Areta, J.L.; Burke, L.M.; Camera, D.M.; West, D.W.; Crawshay, S.; Moore, D.R.; Stellingwerff, T.; Phillips, S.M.; Hawley, J.A.; Coffey, V.G. Reduced resting skeletal muscle protein synthesis is rescued by resistance exercise and protein ingestion following short-term energy deficit. Am. J. Physiol. Endocrinol. Metab. 2014, 306, E989–E997. [CrossRef] [PubMed]
82. Villareal, D.T.; Smith, G.I.; Shah, K.; Mittendorfer, B. Effect of weight loss on the rate of muscle protein synthesis during fasted and fed conditions in obese older adults. Obesity (Silver Spring) 2012, 20, 1780–1786. [CrossRef] [PubMed]
83. Carbone, J.W.; Margolis, L.M.; McClung, J.P.; Cao, J.J.; Murphy, N.E.; Sauter, E.R.; Combs, G.F., Jr.; Young, A.J.; Pasiakos, S.M. Effects of energy deficit, dietary protein, and feeding on intracellular regulators of skeletal muscle proteolysis. FASEB J. 2013, 27, 5104–5111. [CrossRef] [PubMed]
84. Carbone, J.W.; Pasiakos, S.M.; Vislocky, L.M.; Anderson, J.M.; Rodriguez, N.R. Effects of short-term energy deficit on muscle protein breakdown and intramuscular proteolysis in normal-weight young adults. Appl. Physiol. Nutr. Metab. 2014, 39, 960–968. [CrossRef] [PubMed]
85. Hector, A.J.; McGlory, C.; Damas, F.; Mazara, N.; Baker, S.K.; Phillips, S.M. Pronounced energy restriction with elevated protein intake results in no change in proteolysis and reductions in skeletal muscle protein synthesis that are mitigated by resistance exercise. FASEB J. 2017. [CrossRef] [PubMed]
86. Peth, A.; Nathan, J.A.; Goldberg, A.L. The atp costs and time required to degrade ubiquitinated proteins by the 26 s proteasome. J. Biol. Chem. 2013, 288, 29215–29222. [CrossRef] [PubMed]
87. Pasiakos, S.M.; Cao, J.J.; Margolis, L.M.; Sauter, E.R.; Whigham, L.D.; McClung, J.P.; Rood, J.C.; Carbone, J.W.; Combs, G.F., Jr.; Young, A.J. Effects of high-protein diets on fat-free mass and muscle protein synthesis following weight loss: A randomized controlled trial. FASEB J. 2013, 27, 3837–3847. [CrossRef] [PubMed]
88. Longland, T.M.; Oikawa, S.Y.; Mitchell, C.J.; Devries, M.C.; Phillips, S.M. Higher compared with lower dietary protein during an energy deficit combined with intense exercise promotes greater lean mass gain and fat mass loss: A randomized trial. Am. J. Clin. Nutr. 2016, 103, 738–746. [CrossRef] [PubMed]
89. Helms, E.R.; Zinn, C.; Rowlands, D.S.; Brown, S.R. A systematic review of dietary protein during caloric restriction in resistance trained lean athletes: A case for higher intakes. Int. J. Sport Nutr. Exerc. Metab. 2014, 24, 127–138. [CrossRef] [PubMed]
90. Hector, A.; Phillips, S.M. Protein recommendations for weight loss in elite athletes: A focus on body composition and performance. Int. J. Sport Nutr. Exerc. Metab. 2017. [CrossRef] [PubMed]
91. Helms, E.R.; Aragon, A.A.; Fitschen, P.J. Evidence-based recommendations for natural bodybuilding contest preparation: Nutrition and supplementation. J. Int. Soc. Sports Nutr. 2014, 11, 20. [CrossRef] [PubMed]
92. Vandewater, K.; Vickers, Z. Higher-protein foods produce greater sensory-specific satiety. Physiol. Behav. 1996, 59, 579–583. [CrossRef]
93. Astrup, A. The satiating power of protein—A key to obesity prevention? Am. J. Clin. Nutr. 2005, 82, 1–2. [PubMed]
94. Veldhorst, M.A.; Nieuwenhuizen, A.G.; Hochstenbach-Waelen, A.; van Vught, A.J.; Westerterp, K.R.; Engelen, M.P.; Brummer, R.J.; Deutz, N.E.; Westerterp-Plantenga, M.S. Dose-dependent satiating effect of whey relative to casein or soy. Physiol. Behav. 2009, 96, 675–682. [CrossRef] [PubMed]
95. Gunnarsson, P.T.; Winzell, M.S.; Deacon, C.F.; Larsen, M.O.; Jelic, K.; Carr, R.D.; Ahren, B. Glucose-induced incretin hormone release and inactivation are differently modulated by oral fat and protein in mice. Endocrinology 2006, 147, 3173–3180. [CrossRef] [PubMed]
96. Hall, W.L.; Millward, D.J.; Long, S.J.; Morgan, L.M. Casein and whey exert different effects on plasma amino acid profiles, gastrointestinal hormone secretion and appetite. Br. J. Nutr. 2003, 89, 239–248. [CrossRef] [PubMed]
97. Burton-Freeman, B.M. Glycomacropeptide (GMP) is not critical to whey-induced satiety, but may have a unique role in energy intake regulation through cholecystokinin (CCK). Physiol. Behav. 2008, 93, 379–387. [CrossRef] [PubMed]
98. Veldhorst, M.A.; Nieuwenhuizen, A.G.; Hochstenbach-Waelen, A.; Westerterp, K.R.; Engelen, M.P.; Brummer, R.J.; Deutz, N.E.; Westerterp-Plantenga, M.S. Effects of complete whey-protein breakfasts versus whey without GMP-breakfasts on energy intake and satiety. Appetite 2009, 52, 388–395. [CrossRef] [PubMed]
99. Acheson, K.J.; Blondel-Lubrano, A.; Oguey-Araymon, S.; Beaumont, M.; Emady-Azar, S.; Ammon-Zufferey, C.; Monnard, I.; Pinaud, S.; Nielsen-Moennoz, C.; Bovetto, L. Protein choices targeting thermogenesis and metabolism. Am. J. Clin. Nutr. 2011, 93, 525–534. [CrossRef] [PubMed]
100. Alfenas Rde, C.; Bressan, J.; Paiva, A.C. Effects of protein quality on appetite and energy metabolism in normal weight subjects. Arq. Bras. Endocrinol. Metabol. 2010, 54, 45–51. [CrossRef] [PubMed]