Role of protein and amino acids in promoting lean mass accretion with resistance exercise and attenuating lean mass loss during energy deficit in humans

Amino Acids

Volumn 45, Issue 2, 2013, Pages 231-240

  Churchward Venne, Tyler A ^a   Murphy, Caoileann H ^a   Longland, Thomas M ^a   Phillips, Stuart M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Amino acids; Energy deficit; Lean body mass; Protein; Resistance exercise

Indexed keywords

AMINO ACID; MUSCLE PROTEIN; PROTEIN;

AMINOACIDEMIA; BIOSYNTHESIS; CALORIC INTAKE; CATABOLISM; DIET SUPPLEMENTATION; ENERGY; ENERGY RESTRICTION; HUMAN; LEAN BODY WEIGHT; MUSCLE MASS; MUSCLE STRENGTH; NUTRIENT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTAKE; PROTEIN METABOLISM; PROTEIN SYNTHESIS; RESISTANCE TRAINING; REVIEW; SKELETAL MUSCLE;

AMINO ACIDS; CALORIC RESTRICTION; DIET; DIETARY PROTEINS; DIETARY SUPPLEMENTS; EATING; HUMANS; MUSCLE PROTEINS; MUSCLE, SKELETAL; RESISTANCE TRAINING; THINNESS; WEIGHT LOSS;

EID: 84880851856     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-013-1506-0     Document Type: Review

References (71)

1. Abargouei AS, Janghorbani M, Salehi-Marzijarani M, Esmaillzadeh A (2012) Effect of dairy consumption on weight and body composition in adults: a systematic review and meta-analysis of randomized controlled clinical trials. Int J Obes (Lond). doi: 10.1038/ijo.2011.269
2. Abernethy PJ, Jurimae J, Logan PA, Taylor AW, Thayer RE (1994) Acute and chronic response of skeletal muscle to resistance exercise. Sports Med 17(1):22-38
3. Abete I, Parra D, Martinez JA (2009) Legume-, fish-, or high-protein-based hypocaloric diets: effects on weight loss and mitochondrial oxidation in obese men. J Med Food 12(1):100-108. doi: 10.1089/jmf.2007.0700
4. Adechian S, Balage M, Remond D, Migne C, Quignard-Boulange A, Marset-Baglieri A, Rousset S, Boirie Y, Gaudichon C, Dardevet D, Mosoni L (2012) Protein feeding pattern, casein feeding, or milk-soluble protein feeding did not change the evolution of body composition during a short-term weight loss program. Am J Physiol Endocrinol Metab 303(8):E973-E982. doi: 10.1152/ajpendo.00285.2012
5. Almoosawi S, Winter J, Prynne CJ, Hardy R, Stephen AM (2012) Daily profiles of energy and nutrient intakes: are eating profiles changing over time? Eur J Clin Nutr 66(6):678-686. doi: 10.1038/ejcn.2011.210
6. Areta JL, Burke LM, Ross ML, Camera DM, West DW, Broad EM, Jeacocke NA, Moore DR, Stellingwerff T, Phillips SM, Hawley J, Coffey VG (2013) Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. J Physiol. doi: 10.1113/jphysiol.2012.244897
7. Atherton PJ, Smith K (2012) Muscle protein synthesis in response to nutrition and exercise. J Physiol 590(Pt 5):1049-1057. doi: 10.1113/jphysiol. 2011.225003
8. Baumgartner RN (2000) Body composition in healthy aging. Ann N Y Acad Sci 904:437-448
9. Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR (1995) Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol 268(3 Pt 1):E514-E520
10. Biolo G, Tipton KD, Klein S, Wolfe RR (1997) An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol 273(1 Pt 1):E122-E129
11. Bray GA, Smith SR, de Jonge L, Xie H, Rood J, Martin CK, Most M, Brock C, Mancuso S, Redman LM (2012) Effect of dietary protein content on weight gain, energy expenditure, and body composition during overeating: a randomized controlled trial. JAMA 307(1):47-55. doi: 10.1001/jama.2011.1918
12. Burd NA, Yang Y, Moore DR, Tang JE, Tarnopolsky MA, Phillips SM (2012) Greater stimulation of myofibrillar protein synthesis with ingestion of whey protein isolate v. micellar casein at rest and after resistance exercise in elderly men. Br J Nutr 108(6):958-962. doi: 10.1017/S0007114511006271
13. Burk A, Timpmann S, Medijainen L, Vahi M, Oopik V (2009) Time-divided ingestion pattern of casein-based protein supplement stimulates an increase in fat-free body mass during resistance training in young untrained men. Nutr Res 29(6):405-413. doi: 10.1016/j.nutres.2009.03.008
14. Campbell WW, Leidy HJ (2007) Dietary protein and resistance training effects on muscle and body composition in older persons. J Am Coll Nutr 26(6):696S-703S
15. Campbell WW, Barton ML Jr, Cyr-Campbell D, Davey SL, Beard JL, Parise G, Evans WJ (1999) Effects of an omnivorous diet compared with a lactoovovegetarian diet on resistance-training-induced changes in body composition and skeletal muscle in older men. Am J Clin Nutr 70(6):1032-1039
16. Campbell WW, Haub MD, Wolfe RR, Ferrando AA, Sullivan DH, Apolzan JW, Iglay HB (2009) Resistance training preserves fat-free mass without impacting changes in protein metabolism after weight loss in older women. Obesity (Silver Spring) 17(7):1332-1339. doi: 10.1038/oby.2009.2
17. Candow DG, Burke NC, Smith-Palmer T, Burke DG (2006a) Effect of whey and soy protein supplementation combined with resistance training in young adults. Int J Sport Nutr Exerc Metab 16(3):233-244
18. Candow DG, Chilibeck PD, Facci M, Abeysekara S, Zello GA (2006b) Protein supplementation before and after resistance training in older men. Eur J Appl Physiol 97(5):548-556. doi: 10.1007/s00421-006-0223-8
19. Cermak NM, Res PT, de Groot LC, Saris WH, van Loon LJ (2012) Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr. doi: 10.3945/ajcn.112.037556
20. Churchward-Venne TA, Burd NA, Mitchell CJ, West DW, Philp A, Marcotte GR, Baker SK, Baar K, Phillips SM (2012a) Supplementation of a suboptimal protein dose with leucine or essential amino acids: effects on myofibrillar protein synthesis at rest and following resistance exercise in men. J Physiol. doi: 10.1113/jphysiol.2012.228833
21. Churchward-Venne TA, Burd NA, Phillips SM, Research Group EM (2012b) Nutritional regulation of muscle protein synthesis with resistance exercise: strategies to enhance anabolism. Nutr Metab (Lond) 9(1):40. doi: 10.1186/1743-7075-9-40
22. Cribb PJ, Hayes A (2006) Effects of supplement timing and resistance exercise on skeletal muscle hypertrophy. Med Sci Sports Exerc 38(11):1918-1925. doi: 10.1249/01.mss.0000233790.08788.3e
23. Cribb PJ, Williams AD, Carey MF, Hayes A (2006) The effect of whey isolate and resistance training on strength, body composition, and plasma glutamine. Int J Sport Nutr Exerc Metab 16(5):494-509
24. Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M (2001) Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol 535(Pt 1):301-311
25. Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, Singh GM, Gutierrez HR, Lu Y, Bahalim AN, Farzadfar F, Riley LM, Ezzati M, Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (2011) National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet 377(9765):557-567. doi: 10.1016/S0140-6736(10)62037-5
26. Forbes GB, Brown MR, Welle SL, Lipinski BA (1986) Deliberate overfeeding in women and men: energy cost and composition of the weight gain. Br J Nutr 56(1):1-9
27. Frimel TN, Sinacore DR, Villareal DT (2008) Exercise attenuates the weight-loss-induced reduction in muscle mass in frail obese older adults. Med Sci Sports Exerc 40(7):1213-1219. doi: 10.1249/MSS.0b013e31816a85ce
28. Garthe I, Raastad T, Refsnes PE, Koivisto A, Sundgot-Borgen J (2011) Effect of two different weight-loss rates on body composition and strength and power-related performance in elite athletes. Int J Sport Nutr Exerc Metab 21(2):97-104
29. Hartman JW, Tang JE, Wilkinson SB, Tarnopolsky MA, Lawrence RL, Fullerton AV, Phillips SM (2007) 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 86(2):373-381
30. Haub MD, Wells AM, Tarnopolsky MA, Campbell WW (2002) Effect of protein source on resistive-training-induced changes in body composition and muscle size in older men. Am J Clin Nutr 76(3):511-517
31. Heydari M, Freund J, Boutcher SH (2012) The effect of high-intensity intermittent exercise on body composition of overweight young males. J Obes 2012:480467. doi: 10.1155/2012/480467
32. Hoffman JR, Ratamess NA, Tranchina CP, Rashti SL, Kang J, Faigenbaum AD (2009) Effect of protein-supplement timing on strength, power, and body-composition changes in resistance-trained men. Int J Sport Nutr Exerc Metab 19(2):172-185
33. Hubal MJ, Gordish-Dressman H, Thompson PD, Price TB, Hoffman EP, Angelopoulos TJ, Gordon PM, Moyna NM, Pescatello LS, Visich PS, Zoeller RF, Seip RL, Clarkson PM (2005) Variability in muscle size and strength gain after unilateral resistance training. Med Sci Sports Exerc 37(6):964-972
34. Johnstone AM, Murison SD, Duncan JS, Rance KA, Speakman JR (2005) 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 82(5):941-948
35. Josse AR, Tang JE, Tarnopolsky MA, Phillips SM (2010) Body composition and strength changes in women with milk and resistance exercise. Med Sci Sports Exerc 42(6):1122-1130. doi: 10.1249/MSS.0b013e3181c854f6
36. Josse AR, Atkinson SA, Tarnopolsky MA, Phillips SM (2011) Increased consumption of dairy foods and protein during diet- and exercise-induced weight loss promotes fat mass loss and lean mass gain in overweight and obese premenopausal women. J Nutr 141(9):1626-1634. doi: 10.3945/jn.111.141028
37. Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR (2005) Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr 82(5):1065-1073
38. Katzmarzyk PT (2006) A summary of the symposium "Current strategies in the prevention and treatment of obesity". Appl Physiol Nutr Metab 31(6):767-768. doi: 10.1139/h06-049
39. Krieger JW, Sitren HS, Daniels MJ, Langkamp-Henken B (2006) Effects of variation in protein and carbohydrate intake on body mass and composition during energy restriction: a meta-regression 1. Am J Clin Nutr 83(2):260-274
40. Layman DK (2009) Dietary Guidelines should reflect new understandings about adult protein needs. Nutr Metab (Lond) 6:12. doi: 10.1186/1743-7075-6-12
41. Layman DK, Evans E, Baum JI, Seyler J, Erickson DJ, Boileau RA (2005) Dietary protein and exercise have additive effects on body composition during weight loss in adult women. J Nutr 135(8):1903-1910
42. Leidy HJ, Carnell NS, Mattes RD, Campbell WW (2007) Higher protein intake preserves lean mass and satiety with weight loss in pre-obese and obese women. Obesity (Silver Spring) 15(2):421-429. doi: 10.1038/oby.2007.531
43. Lewis GF, Carpentier A, Adeli K, Giacca A (2002) Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr Rev 23(2):201-229
44. Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84(2-3):275-294
45. Li Z, Heber D (2012) Sarcopenic obesity in the elderly and strategies for weight management. Nutr Rev 70(1):57-64. doi: 10.1111/j.1753-4887.2011.00453.x
46. Mettler S, Mitchell N, Tipton KD (2010) Increased protein intake reduces lean body mass loss during weight loss in athletes. Med Sci Sports Exerc 42(2):326-337. doi: 10.1249/MSS.0b013e3181b2ef8e
47. Mojtahedi MC, Thorpe MP, Karampinos DC, Johnson CL, Layman DK, Georgiadis JG, Evans EM (2011) The effects of a higher protein intake during energy restriction on changes in body composition and physical function in older women. J Gerontol A Biol Sci Med Sci 66(11):1218-1225. doi: 10.1093/gerona/glr120
48. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, Prior T, Tarnopolsky MA, Phillips SM (2009a) Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr 89(1):161-168. doi: 10.3945/ajcn.2008.26401
49. Moore DR, Tang JE, Burd NA, Rerecich T, Tarnopolsky MA, Phillips SM (2009b) Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise. J Physiol 587(Pt 4):897-904. doi: 10.1113/jphysiol.2008.164087
50. Paoli A, Grimaldi K, D'Agostino D, Cenci L, Moro T, Bianco A, Palma A (2012) Ketogenic diet does not affect strength performance in elite artistic gymnasts. J Int Soc Sports Nutr 9(1):34. doi: 10.1186/1550-2783-9-34
51. Pennings B, Groen BB, de Lange A, Gijsen AP, Zorenc AH, Senden JM, van Loon LJ (2012) Amino acid absorption and subsequent muscle protein accretion following graded intakes of whey protein in elderly men. Am J Physiol Endocrinol Metab. doi: 10.1152/ajpendo.00517.2011
52. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol 273(1 Pt 1):E99-E107
53. Phillips SM, Hartman JW, Wilkinson SB (2005) Dietary protein to support anabolism with resistance exercise in young men. J Am Coll Nutr 24(2):134S-139S
54. Samuel VT, Petersen KF, Shulman GI (2010) Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375(9733):2267-2277. doi: 10.1016/S0140-6736(10)60408-4
55. Sartor F, de Morree HM, Matschke V, Marcora SM, Milousis A, Thom JM, Kubis HP (2010) High-intensity exercise and carbohydrate-reduced energy-restricted diet in obese individuals. Eur J Appl Physiol 110(5):893-903. doi: 10.1007/s00421-010-1571-y
56. Smith K, Barua JM, Watt PW, Scrimgeour CM, Rennie MJ (1992) Flooding with L-[1-13C]leucine stimulates human muscle protein incorporation of continuously infused L-[1-13C]valine. Am J Physiol 262(3 Pt 1):E372-E376
57. Stiegler P, Cunliffe A (2006) The role of diet and exercise for the maintenance of fat-free mass and resting metabolic rate during weight loss. Sports Med 36(3):239-262
58. Strychar I, Lavoie ME, Messier L, Karelis AD, Doucet E, Prud'homme D, Fontaine J, Rabasa-Lhoret R (2009) Anthropometric, metabolic, psychosocial, and dietary characteristics of overweight/obese postmenopausal women with a history of weight cycling: a MONET (Montreal Ottawa New Emerging Team) study. J Am Diet Assoc 109(4):718-724. doi: 10.1016/j.jada.2008.12.026
59. Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM (2009) 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 107(3):987-992. doi: 10.1152/japplphysiol.00076.2009
60. Tieland M, Dirks ML, van der Zwaluw N, Verdijk LB, van de Rest O, de Groot LC, van Loon LJ (2012) Protein supplementation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly people: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc. doi: 10.1016/j.jamda.2012.05.020
61. Tipton KD, Ferrando AA, Phillips SM, Doyle D Jr, Wolfe RR (1999) Postexercise net protein synthesis in human muscle from orally administered amino acids. Am J Physiol 276(4 Pt 1):E628-E634
62. Trapp EG, Chisholm DJ, Freund J, Boutcher SH (2008) The effects of high-intensity intermittent exercise training on fat loss and fasting insulin levels of young women. Int J Obes (Lond) 32(4):684-691. doi: 10.1038/sj.ijo.0803781
63. Verdijk LB, Jonkers RA, Gleeson BG, Beelen M, Meijer K, Savelberg HH, Wodzig WK, Dendale P, van Loon LJ (2009) Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am J Clin Nutr 89(2):608-616. doi: 10.3945/ajcn.2008.26626
64. Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-Villareal R, Napoli N, Qualls C, Shah K (2011) Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med 364(13):1218-1229. doi: 10.1056/NEJMoa1008234
65. Weinheimer EM, Sands LP, Campbell WW (2010) A systematic review of the separate and combined effects of energy restriction and exercise on fat-free mass in middle-aged and older adults: implications for sarcopenic obesity. Nutr Rev 68(7):375-388. doi: 10.1111/j.1753-4887.2010.00298.x
66. Wilkinson SB, Tarnopolsky MA, Macdonald MJ, Macdonald JR, Armstrong D, Phillips SM (2007) Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am J Clin Nutr 85(4):1031-1040
67. Wolfe RR (2006) The underappreciated role of muscle in health and disease. Am J Clin Nutr 84(3):475-482
68. Wycherley TP, Moran LJ, Clifton PM, Noakes M, Brinkworth GD (2012) Effects of energy-restricted high-protein, low-fat compared with standard-protein, low-fat diets: a meta-analysis of randomized controlled trials. Am J Clin Nutr 96(6):1281-1298. doi: 10.3945/ajcn.112.044321
69. Yamashita T, Sasahara T, Pomeroy SE, Collier G, Nestel PJ (1998) Arterial compliance, blood pressure, plasma leptin, and plasma lipids in women are improved with weight reduction equally with a meat-based diet and a plant-based diet. Metabolism 47(11):1308-1314
70. Yang Y, Breen L, Burd NA, Hector AJ, Churchward-Venne TA, Josse AR, Tarnopolsky MA, Phillips SM (2012a) Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br J Nutr 108(10):1780-1788. doi: 10.1017/S0007114511007422
71. Yang Y, Churchward-Venne TA, Burd NA, Breen L, Tarnopolsky MA, Phillips SM (2012b) Myofibrillar protein synthesis following ingestion of soy protein isolate at rest and after resistance exercise in elderly men. Nutr Metab (Lond) 9(1):57. doi: 10.1186/1743-7075-9-57