Maximizing muscle protein anabolism: The role of protein quality

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 12, Issue 1, 2009, Pages 66-71

  Tang, Jason E ^a   Phillips, Stuart M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Casein; Hypertrophy; Muscle mass; Soy; Whey

Indexed keywords

CASEIN; ESSENTIAL AMINO ACID; MUSCLE PROTEIN;

AEROBIC EXERCISE; AGING; AMINOACIDEMIA; ATHLETE; BODY FAT; CALORIC INTAKE; CARBOHYDRATE INTAKE; EXERCISE; HUMAN; LEAN BODY WEIGHT; METABOLIC RATE; MORBIDITY; MUSCLE ATROPHY; MUSCLE CONTRACTION; MUSCLE HYPERTROPHY; MUSCLE METABOLISM; MUSCLE TRAINING; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN INTAKE; PROTEIN SYNTHESIS; REVIEW; SKELETAL MUSCLE; SOYBEAN; WHEY;

AGED; AGING; ANABOLIC AGENTS; DIETARY PROTEINS; HUMANS; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; RESISTANCE TRAINING; WEIGHT LIFTING;

EID: 58149107240     PISSN: 13631950     EISSN: 15353885     Source Type: Journal    
DOI: 10.1097/MCO.0b013e32831cef75     Document Type: Review

References (89)

1. Fry AC. The role of resistance exercise intensity on muscle fibre adaptations. Sports Med 2004; 34:663-679.
2. Kraemer WJ, Adams K, Cafarelli E, et al. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc 2002; 34:364-380.
3. Kraemer WJ, Staron RS, Hagerman FC, et al. The effects of short-term resistance training on endocrine function in men and women. Eur J Appl Physiol Occup Physiol 1998; 78:69-76.
4. Volpi E, Kobayashi H, Sheffield-Moore M, et al. 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.
5. Biolo G, Declan Fleming RY, Wolfe RR. Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J Clin Invest 1995; 95:811 -819.
6. Biolo G, Maggi SP, Williams BD, et al. Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol 1995; 268:E514-E520.
7. Biolo G, Tipton KD, Klein S, et al. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol 1997; 273:E122-E129.
8. Volpi E, Ferrando AA, Yeckel CW, et al. Exogenous amino acids stimulate net muscle protein synthesis in the elderly. J Clin Invest 1998; 101:2000-2007.
9. Wolfe RR. Regulation of muscle protein by amino acids. J Nutr 2002; 132:3219S-3224S.
10. Phillips SM, Tipton KD, Aarsland A, et al. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol 1997; 273:E99-E107.
11. Phillips SM, Tipton KD, Ferrando AA, et al. Resistance training reduces the acute exercise-induced increase in muscle protein turnover. Am J Physiol 1999; 276:E118-E124.
12. Yarasheski KE, Zachwieja JJ, Bier DM. Acute effects of resistance exercise on muscle protein synthesis rate in young and elderly men and women. Am J Physiol 1993; 265:E210-E214.
13. Chesley A, MacDougall JD, Tarnopolsky MA, et al. Changes in human muscle protein synthesis after resistance exercise. J Appl Physiol 1992; 73:1383-1388.
14. Chow LS, Albright RC, Bigelow ML, et al. Mechanism of insulin's anabolic effect on muscle: measurements of muscle protein synthesis and breakdown using aminoacyl-tRNA and other surrogate measures. AJP Endocrinol Metab 2006; 291:E729-E736.
15. Borsheim E, Cree MG, Tipton KD, et al. Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise. J Appl Physiol 2004; 96:674-678.
16. Fujita S, Rasmussen BB, Cadenas JG, et al. Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. AJP Endocrinol Metab 2006; 291:E745-E754.
17. Rennie MJ, Wackerhage H, Spangenburg EE, et al. Control of the size of the human muscle mass. Annu Rev Physiol 2004; 66:799-828.
18. Rasmussen BB, Tipton KD, Miller SL, et al. An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J Appl Physiol 2000; 88:386-392.
19. Tipton KD, Elliott TA, Cree MG, et al. Stimulation of net muscle protein synthesis by whey protein ingestion before and after exercise. Am J Physiol Endocrinol Metab (E) 2006; 292:E71-E76.
20. Tipton KD, Rasmussen BB, Miller SL et al. Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise. Am J Physiol Endocrinol Metab (E) 2001; 281:E197-E206.
21. Boirie Y, Dangin M, Gachon P, et al. Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci U S A 1997; 94:14930-14935.
22. Dangin M, Boirie Y, Garcia-Rodenas C, et al. The digestion rate of protein is an independent regulating factor of postprandial protein retention. Am J Physiol Endocrinol Metab (E) 2001; 280:E340-E348.
23. Dangin M, Boirie Y, Guillet C, et al. Influence of the protein digestion rate on protein turnover in young and elderly subjects. J Nutr 2002; 132:3228S-3233S.
24. Dangin M, Guillet C, Garcia-Rodenas C, et al. The rate of protein digestion affects protein gain differently during aging in humans. J Physiol 2003; 549:635-644.
25. Tipton KD, Ferrando AA, Phillips SM, et al. Postexercise net protein synthesis 7 in human muscle from orally administered amino acids. Am J Physiol 1999; 276:E628-E634.
26. Borsheim E, Tipton KD, Wolf SE, et al. Essential amino acids and muscle protein recovery from resistance exercise. Am J Physiol Endocrinol Metab (E) 2002; 283:E648-E657.
27. Elliot TA, Cree MG, Sanford AP, et al. Milk ingestion stimulates net muscle protein synthesis following resistance exercise. Med Sci Sports Exerc 2006; 38:667-674.
28. Tang JE, Manolakos JJ, Kujbida GW, et al. Minimal whey protein with carbohydrate stimulates muscle protein synthesis following resistance exercise in trained young men. Appl Physiol Nutr Metab 2007; 32:1132-1138.
29. Tipton KD, Elliott TA, Cree MG, et al. Ingestion of casein and whey proteins result in muscle anabolism after resistance exercise. Med Sci Sports Exerc 2004; 36:2073-2081.
30. Wilkinson SB, Tarnopolsky MA, MacDonald MJ, et al. Consumption of fluid skim milk promotes greater muscle protein accretion following resistance exercise than an isonitrogenous and isoenergetic soy protein beverage. Am J Clin Nutr 2007; 85:1031-1040. An important study that showed that when energy, nitrogen and macronutrient-matched soy and milk were consumed, postresistance exercise, that skim milk promoted greater nitrogen retention and greater muscle protein synthesis.
31. Hartman JW, Tang JE, Wilkinson SB, et al. 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. Am J Clin Nutr 2007; 86:373-381. A critical training study in which chronic skim milk consumption following resistance exercise resulted in greater gains in lean mass and loss of fat mass versus matched soy protein or energy as carbohydrate.
32. Hulmi JJ, Kovanen V, Selanne H, et al. Acute and long-term effects of resistance exercise with or without protein ingestion on muscle hypertrophy and gene expression. Amino Acids 2008. doi: 10.1007/s00726-008-0150-6. [Epub ahead of print].
33. Cribb PJ, Hayes A. Effects of supplement timing and resistance exercise on skeletal muscle hypertrophy. Med Sci Sports Exerc 2006; 38:1918-1925.
34. Holm L, Esmarck B, Mizuno M, et al. The effect of protein and carbohydrate supplementation on strength training outcome of rehabilitation in ACL patients. J Orthop Res 2006; 24:2114-2123.
35. Esmarck B, Andersen JL, Olsen S, et al. Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol 2001; 535:301-311.
36. Andersen LL, Tufekovic G, Zebis MK, et al. The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle strength. Metabolism 2005; 54:151-156.
37. Dreyer HC, Fujita S, Cadenas JG, et al. Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J Physiol 2006; 576:613-624.
38. Karisson HK, Nilsson PA, Nilsson J, et al. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. Am J Physiol Endocrinol Metab (E) 2004; 287:E1-E7.
39. Eliasson J, Elfegoun T, Nilsson J, et al. Maximal lengthening contractions increase p70 S6 kinase phosphorylation in human skeletal muscle in the absence of nutritional supply. AJP Endocrinol Metab 2006; 291:E1197-E1205.
40. Bohe J, Low A, Wolfe RR, et al. Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: a dose-response study. J Physiol 2003; 552:315-324.
41. Miller SL, Tipton KD, Chinkes DL, et al. Independent and combined effects of amino acids and glucose after resistance exercise. Med Sci Sports Exerc 2003; 35:449-455.
42. Tipton KD, Gurkin BE, Matin S, et al. Nonessential amino acids are not necessary to stimulate net muscle protein synthesis in healthy volunteers. J Nutr Biochem 1999; 10:89-95.
43. Cuthbertson D, Smith K, Babraj J, et al. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 2005; 19:422-424.
44. Phillips SM, Panse G, Roy BD, et al. Resistance training-induced adaptations in skeletal muscle protein turnover in the fed state. Can J Physiol Pharmacol 2002; 80:1045-1053.
45. Reeds PJ, Garlick PJ. Protein and amino acid requirements and the composition of complementary foods. J Nutr 2003; 133:2953S-2961S.
46. Institute of M. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids. Washington, DC: National Academies Press; 2005.
47. Schaafsma G. The protein digestibility-corrected amino acid score. J Nutr 2000; 130:1865S-1867S.
48. Castellanos VH, Litchford MD, Campbell WW. Modular protein supplements and their application to long-term care. Nutr Clin Pract 2006; 21:485-504.
49. Miller GD, Jarvis JK, McBean LD. Handbook of dairy foods and nutrition. CRC Press: Boca Raton, FL; 2006.
50. Wayler A, Queiroz E, Scrimshaw NS, et al. Nitrogen balance studies in young men to assess the protein quality of an isolated soy protein in relation to meat proteins. J Nutr 1983; 113:2485-2491.
51. Bos C, Juillet B, Fouillet H, et al. Postprandial metabolic utilization of wheat protein in humans. Am J Clin Nutr 2005; 81:87-94.
52. Bos C, Mahe S, Gaudichon C, et al. Assessment of net postprandial protein utilization of 15 N-labelled milk nitrogen in human subjects. Br J Nutr 1999; 81:221-226.
53. Bos C, Metges CC, Gaudichon C, et al. Postprandial kinetics of dietary amino acids are the main determinant of their metabolism after soy or milk protein ingestion in humans. J Nutr 2003; 133:1308-1315.
54. Fouillet H, Mariotti F, Gaudichon C, et al. 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.
55. Phillips SM. Protein requirements and supplementation in strength sports. Nutrition 2004; 20:689-695.
56. Blomstrand E, Eliasson J, Karisson HK, et al. Branched-chain amino acids activate key enzymes in protein synthesis after physical exercise. J Nutr 2006; 136.269S-273S.
57. Blomstrand E, Saltin B. BCAA intake affects protein metabolism in muscle after but not during exercise in humans. Am J Physiol Endocrinol Metab (E) 2001; 281:E365-E374.
58. Candow DG, Burke NC, Smith-Ramer T, et al. Effect of whey and soy protein supplementation combined with resistance training in young adults. Int J Sport Nutr Exerc Metab 2006; 16:233-244.
59. Rankin JW, Goldman LP, Puglisi MJ, et al. Effect of postexercise supplement consumption on adaptations to resistance training. J Am Coll Nutr 2004; 23:322-330.
60. Cribb PJ, Williams AD, Carey MF, et al. The effect of whey isolate and resistance training on strength, body composition, and plasma glutamine. Int J Sport Nutr Exerc Metab 2006; 16:494-509.
61. Cribb PJ, Williams AD, Stathis CG, et al. Effects of whey isolate, creatine, and resistance training on muscle hypertrophy. Med Sci Sports Exerc 2007; 39:298-307.
62. Evans WJ. What is sarcopenia? J Gerontol A Biol Sci Med Sci 1995; 50 (Spec No):5-8.
63. Dorrens J, Rennie MJ. Effects of ageing and human whole body and muscle protein turnover. Scand J Med Sci Sports 2003; 13:26-33.
64. Evans WJ. Protein nutrition, exercise and aging. J Am Coll Nutr 2004; 23:601S-609S.
65. Marsh AP, Miller ME, Saikin AM, et al. Lower extremity strength and power are associated with 400-meter walk time in older adults: the InCHIANTI study. J Gerontol Ser A Biol Sci Med Sci 2006; 61:1186-1193.
66. Forrest KYZ, Zmuda JM, Cauley JA. Correlates of decline in lower extremity performance in older women: a 10-year follow-up study. J Gerontol Ser A Biol Sci Med Sci 2006; 61:1194-1200.
67. DeFronzo RA, Bonadonna RC, Ferrannini E. Pathogenesis of NIDDM. A balanced overview. Diabetes Care 1992; 15:318-368.
68. Johnstone AM, Murison SD, Duncan JS, et al. Factors influencing variation in basal metabolic rate include fat-free mass, fat mass, age, and circulating thyroxine but not sex, circulating leptin, or triiodothyronine. Am J Clin Nutr 2005; 82:941-948.
69. Jurca R, Lamonte MJ, Barlow CE, et al. Association of muscular strength with incidence of metabolic syndrome in men. Med Sci Sports Exerc 2005; 37:1849-1855.
70. Ruiz JR, Sui X, Lobelo F, et al. Association between muscular strength and mortality in men: prospective cohort study. Br Med J 2008; 337:a439.
71. Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr 2006; 84:475-482.
72. Balagopal P, Rooyackers OE, Adey DB, et al. Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am J Physiol 1997; 273:E790-E800.
73. Welle S, Thornton C, Jozefowicz R, et al. Myofibrillar protein synthesis in young and old men. Am J Physiol 1993; 264:E693-E698.
74. Trappe T, Williams R, Carrithers J, et al. Influence of age and resistance exercise on human skeletal muscle proteolysis: a microdialysis approach. J Physiol 2004; 554:803-813.
75. Volpi E, Mittendorfer B, Rasmussen BB, et al. The response of muscle protein anabolism to combined hyperaminoacidemia and glucose-induced hyperinsulinemia is impaired in the elderly. J Clin Endocrinol Metab 2000; 85:4481-4490.
76. Volpi E, Sheffield-Moore M, Rasmussen BB, et al. Basal muscle amino acid kinetics and protein synthesis in healthy young and older men. J Am Med Assoc 2001; 286:1206-1212.
77. Welle S, Thornton CA. High-protein meals do not enhance myofibrillar synthesis after resistance exercise in 62- to 75-yr-old men and women. Am J Physiol 1998; 274:E677-E683.
78. Hunter GR, McCarthy JP, Bamman MM. Effects of resistance training on older adults. Sports Med 2004; 34:329-348.
79. Evans WJ. Reversing sarcopenia: how weight training can build strength and vitality. Geriatrics 1996; 51:51 -53.
80. Evans WJ. Effects of exercise on senescent muscle. Clin Orthop Relat Res 2002; 403:S211-S220.
81. Katsanos CS, Kobayashi H, Sheffield-Moore M, et al. A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. AJP Endocrinol Metab 2006; 291:E381-E387.
82. Drummond MJ, Dreyer HC, Pennings B, et al. Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. J Appl Physiol 2008; 104:1452-1461.
83. Paddon-Jones D, Sheffield-Moore M, Zhang XJ, et al. Amino acid ingestion improves muscle protein synthesis in the young and elderly. Am J Physiol Endocrinol Metab (E) 2004; 286:E321-E328.
84. Dardevet D, Sornet C, Bayle G, et al. Postprandial stimulation of muscle protein synthesis in old rats can be restored by a leucine-supplemented meal. J Nutr 2002; 132:95-100.
85. Rieu I, Sornet C, Bayle G, et al. Leucine-supplemented meal feeding for ten days beneficially affects postprandial muscle protein synthesis in old rats. J Nutr 2003; 133:1198-1205.
86. Beaulieu J, Dubuc R, Beaudet N, et al. Immunomodulation by a malleable matrix composed of fermented whey proteins and lactic acid bacteria. J Med Food 2007; 10:67-72.
87. Beaulieu J, Dupont C, Lemieux P. Anti-inflammatory potential of a malleable matrix composed of fermented whey proteins and lactic acid bacteria in an atopic dermatitis model. J Inflamm (Lond) 2007; 4:6.
88. Westerkamp CM, Gordon SE. Angiotensin-converting enzyme inhibition attenuates myonuclear addition in overloaded slow-twitch skeletal muscle. Am J Physiol Regul Integr Comp Physiol (R) 2005; 289:R1223-R1231.
89. Gordon SE, Davis BS, Carlson CJ, et al. ANG II is required for optimal overload-induced skeletal muscle hypertrophy. Am J Physiol Endocrinol Metab (E) 2001; 280:E150-E159.