Soy-dairy protein blend and whey protein ingestion after resistance exercise increases amino acid transport and transporter expression in human skeletal muscle

Journal of Applied Physiology

Volumn 116, Issue 11, 2014, Pages 1353-1364

  Reidy, P T ^a   Walker, D K ^a   Dickinson, J M ^a   Gundermann, D M ^a   Drummond, M J ^a   Timmerman, K L ^a   Cope, M B ^c   Mukherjea, R ^c   Jennings, K ^b   Volpi, E ^a,b   Rasmussen, B B ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c DUPONT COMPANY   (United States)

Author keywords

Leucine; MTORC1; Muscle protein synthesis; Protein anabolism; Protein metabolism

Indexed keywords

AMINO ACID; AMINO ACID TRANSPORTER; MILK PROTEIN; PROTEIN INTAKE; SOYBEAN PROTEIN; WHEY PROTEIN;

ADMINISTRATION AND DOSAGE; ADULT; BIOSYNTHESIS; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; EATING; FEMALE; HUMAN; MALE; METABOLISM; ORAL DRUG ADMINISTRATION; PHYSIOLOGY; PROCEDURES; PROTEIN INTAKE; RANDOMIZED CONTROLLED TRIAL; RESISTANCE TRAINING; SKELETAL MUSCLE; UPREGULATION; YOUNG ADULT;

ADMINISTRATION, ORAL; ADULT; AMINO ACID TRANSPORT SYSTEMS; AMINO ACIDS; DIETARY PROTEINS; DOUBLE-BLIND METHOD; EATING; FEMALE; HUMANS; MALE; MILK PROTEINS; MUSCLE, SKELETAL; RESISTANCE TRAINING; SOYBEAN PROTEINS; UP-REGULATION; YOUNG ADULT;

EID: 84902472412     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01093.2013     Document Type: Article

References (67)

1. Adams CM. Role of the transcription factor ATF4 in the anabolic actions of insulin and the anti-anabolic actions of glucocorticoids. J Biol Chem 282: 16744-16753, 2007.
2. Bell JA, Fujita S, Volpi E, Cadenas JG, Rasmussen BB. Short-term insulin and nutritional energy provision do not stimulate muscle protein synthesis if blood amino acid availability decreases. Am J Physiol Endocrinol Metab 289: E999-E1006, 2005.
3. Biolo G, Fleming RY, Maggi SP, Wolfe RR. Transmembrane transport and intracellular kinetics of amino acids in human skeletal muscle. Am J Physiol Endocrinol Metab 268: E75-E84, 1995.
4. Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR. Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol Endocrinol Metab 268: E514-E520, 1995.
5. Biolo G, Tipton KD, Klein S, Wolfe RR. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol Endocrinol Metab 273: E122-E129, 1997.
6. Biolo G, Williams BD, Fleming RY, Wolfe RR. Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes 48: 949-957, 1999.
7. Borsheim E, Aarsland A, Wolfe RR. Effect of an amino acid, protein, and carbohydrate mixture on net muscle protein balance after resistance exercise. Int J Sport Nutr Exerc Metab 14: 255-271, 2004.
8. Borsheim E, Cree MG, Tipton KD, Elliott TA, Aarsland A, Wolfe RR. Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise. J Appl Physiol 96: 674-678, 2004.
9. Borsheim E, Tipton KD, Wolf SE, Wolfe RR. Essential amino acids and muscle protein recovery from resistance exercise. Am J Physiol Endocrinol Metab 283: E648-E657, 2002.
10. Burd NA, Tang JE, Moore DR, Phillips SM. Exercise training and protein metabolism: influences of contraction, protein intake, and sexbased differences. J Appl Physiol 106: 1692-1701, 2009.
11. Calder AG, Anderson SE, Grant I, McNurlan MA, Garlick PJ. The determination of low d5-phenylalanine enrichment (0.002-009 atom percent excess), after conversion to phenylethylamine, in relation to protein turnover studies by gas chromatography/electron ionization mass spectrometry. Rapid Commun Mass Spectrom 6: 421-424, 1992.
12. Churchward-Venne TA, Breen L, Di Donato DM, Hector AJ, Mitchell CJ, Moore DR, Stellingwerff T, Breuille D, Offord EA, Baker SK, Phillips SM. 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 99: 276-86, 2014.
13. Churchward-Venne TA, Burd NA, Mitchell CJ, West DW, Philp A, Marcotte GR, Baker SK, Baar K, Phillips SM. 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 590: 2751-2765, 2012.
14. Dickinson JM, Drummond MJ, Coben JR, Volpi E, Rasmussen BB. Aging differentially affects human skeletal muscle amino acid transporter expression when essential amino acids are ingested after exercise. Clin Nutr 32: 273-280, 2013.
15. Dickinson JM, Rasmussen BB. Essential amino acid sensing, signaling, and transport in the regulation of human muscle protein metabolism. Curr Opin Clin Nutr Metab Care 14: 83-88, 2011.
16. Dreyer HC, Drummond MJ, Pennings B, Fujita S, Glynn EL, Chinkes DL, Dhanani S, Volpi E, Rasmussen BB. 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 294: E392-E400, 2008.
17. Dreyer HC, Fujita S, Cadenas JG, Chinkes DL, Volpi E, Rasmussen BB. Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. J Physiol 576: 613-624, 2006.
18. Drummond MJ, Bell JA, Fujita S, Dreyer HC, Glynn EL, Volpi E, Rasmussen BB. Amino acids are necessary for the insulin-induced activation of mTOR/S6K1 signaling and protein synthesis in healthy and insulin resistant human skeletal muscle. Clin Nutr 27: 447-456, 2008.
19. Drummond MJ, Dickinson JM, Fry CS, Walker DK, Gundermann DM, Reidy PT, Timmerman KL, Markofski MM, Paddon-Jones D, Rasmussen BB, Volpi E. Bed rest impairs skeletal muscle amino acid transporter expression, mTORC1 signaling, and protein synthesis in response to essential amino acids in older adults. Am J Physiol Endocrinol Metab 302: E1113-E1122, 2012.
20. Drummond MJ, Dreyer HC, Fry CS, Glynn EL, Rasmussen BB. Nutritional and contractile regulation of human skeletal muscle protein synthesis and mTORC1 signaling. J Appl Physiol 106: 1374-1384, 2009.
21. Drummond MJ, Fry CS, Glynn EL, Timmerman KL, Dickinson JM, Walker DK, Gundermann DM, Volpi E, Rasmussen BB. Skeletal muscle amino acid transporter expression is increased in young and older adults following resistance exercise. J Appl Physiol 111: 135-142, 2011.
22. Drummond MJ, Glynn EL, Fry CS, Timmerman KL, Volpi E, Rasmussen BB. An increase in essential amino acid availability upregulates amino acid transporter expression in human skeletal muscle. Am J Physiol Endocrinol Metab 298: E1011-E1018, 2010.
23. Drummond MJ, Rasmussen BB. Leucine-enriched nutrients and the regulation of mammalian target of rapamycin signaling and human skeletal muscle protein synthesis. Curr Opin Clin Nutr Metab Care 11: 222-226, 2008.
24. Elliot TA, Cree MG, Sanford AP, Wolfe RR, Tipton KD. Milk ingestion stimulates net muscle protein synthesis following resistance exercise. Med Sci Sports Exerc 38: 667-674, 2006.
25. Evans K, Nasim Z, Brown J, Butler H, Kauser S, Varoqui H, Erickson JD, Herbert TP, Bevington A. Acidosis-sensing glutamine pump SNAT2 determines amino acid levels and mammalian target of rapamycin signalling to protein synthesis in L6 muscle cells. J Am Soc Nephrol 18: 1426-1436, 2007.
26. Fry CS, Drummond MJ, Glynn EL, Dickinson JM, Gundermann DM, Timmerman KL, Walker DK, Dhanani S, Volpi E, Rasmussen BB. Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis. Skelet Muscle 1: 11, 2011.
27. Fry CS, Drummond MJ, Glynn EL, Dickinson JM, Gundermann DM, Timmerman KL, Walker DK, Volpi E, Rasmussen BB. Skeletal muscle autophagy and protein breakdown following resistance exercise are similar in younger and older adults. J Gerontol A Biol Sci Med Sci 68: 599-607, 2013.
28. Fujita S, Rasmussen BB, Bell JA, Cadenas JG, Volpi E. Basal muscle intracellular amino acid kinetics in women and men. Am J Physiol Endocrinol Metab 292: E77-E83, 2007.
29. Gislason SR, Hassenkam T, Nedel S, Bovet N, Eiriksdottir ES, Alfredsson HA, Hem CP, Balogh ZI, Dideriksen K, Oskarsson N, Sigfusson B, Larsen G, Stipp SL. Characterization of Eyjafjallajokull volcanic ash particles and a protocol for rapid risk assessment. Proc Natl Acad Sci U S A 108: 7307-7312, 2011.
30. Glover EI, Oates BR, Tang JE, Moore DR, Tarnopolsky MA, Phillips SM. Resistance exercise decreases eIF2B epsilon phosphorylation and potentiates the feeding-induced stimulation of p70S6K1 and rpS6 in young men. Am J Physiol Regul Integr Comp Physiol 295: R604-R610, 2008.
31. Glynn EL, Fry CS, Timmerman KL, Drummond MJ, Volpi E, Rasmussen BB. Addition of carbohydrate or alanine to an essential amino acid mixture does not enhance human skeletal muscle protein anabolism. J Nutr 143: 307-314, 2013.
32. Goberdhan DC. Intracellular amino acid sensing and mTORC1-regulated growth: new ways to block an old target? Curr Opin Investig Drugs 11: 1360-1367, 2010.
33. Goberdhan DC, Meredith D, Boyd CA, Wilson C. PAT-related amino acid transporters regulate growth via a novel mechanism that does not require bulk transport of amino acids. Development 132: 2365-2375, 2005.
34. Harber MP, Konopka AR, Jemiolo B, Trappe SW, Trappe TA, Reidy PT. Muscle protein synthesis and gene expression during recovery from aerobic exercise in the fasted and fed states. Am J Physiol Regul Integr Comp Physiol 299: R1254-R1262, 2010.
35. Heublein S, Kazi S, Ogmundsdottir MH, Attwood EV, Kala S, Boyd CA, Wilson C, Goberdhan DC. Proton-assisted amino-acid transporters are conserved regulators of proliferation and amino-acid-dependent mTORC1 activation. Oncogene 29: 4068-4079, 2010.
36. Hulmi JJ, Kovanen V, Selanne H, Kraemer WJ, Hakkinen K, Mero AA. Acute and long-term effects of resistance exercise with or without protein ingestion on muscle hypertrophy and gene expression. Amino Acids 37: 297-308, 2009.
37. Hundal HS, Taylor PM. Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Am J Physiol Endocrinol Metab 296: E603-E613, 2009.
38. Hyde R, Hajduch E, Powell DJ, Taylor PM, Hundal HS. Ceramide down-regulates System A amino acid transport and protein synthesis in rat skeletal muscle cells. FASEB J 19: 461-463, 2005.
39. Jorfeldt L, Juhlin-Dannfelt A. The influence of ethanol on splanchnic and skeletal muscle metabolism in man. Metabolism 27: 97-106, 1978.
40. Jorfeldt L, Wahren J. Leg blood flow during exercise in man. Clin Sci 41: 459-473, 1971.
41. Kraemer WJ, Hatfield DL, Volek JS, Fragala MS, Vingren JL, Anderson JM, Spiering BA, Thomas GA, Ho JY, Quann EE, Izquierdo M, Hakkinen K, Maresh CM. Effects of amino acids supplement on physiological adaptations to resistance training. Med Sci Sports Exerc 41: 1111-1121, 2009.
42. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25: 402-408, 2001.
43. Lopez AB, Wang C, Huang CC, Yaman I, Li Y, Chakravarty K, Johnson PF, Chiang CM, Snider MD, Wek RC, Hatzoglou M. A feedback transcriptional mechanism controls the level of the arginine/ lysine transporter cat-1 during amino acid starvation. Biochem J 402: 163-173, 2007.
44. Luo JQ, Chen DW, Yu B. Upregulation of amino acid transporter expression induced by L-leucine availability in L6 myotubes is associated with ATF4 signaling through mTORC1-dependent mechanism. Nutrition 29: 284-290, 2013.
45. Malmberg SE, Adams CM. Insulin signaling and the general amino acid control response. Two distinct pathways to amino acid synthesis and uptake. J Biol Chem 283: 19229-19234, 2008.
46. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, Prior T, Tarnopolsky MA, Phillips SM. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr 89: 161-168, 2009.
47. Moore DR, Tang JE, Burd NA, Rerecich T, Tarnopolsky MA, Phillips SM. Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise. J Physiol 587: 897-904, 2009.
48. Paul GL. The rationale for consuming protein blends in sports nutrition. J Am Coll Nutr 28, Suppl: 464S-472S, 2009.
49. Poncet N, Taylor PM. The role of amino acid transporters in nutrition. Curr Opin Clin Nutr Metab Care 16: 57-65, 2013.
50. Rasmussen BB, Tipton KD, Miller SL, Wolf SE, Wolfe RR. An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J Appl Physiol 88: 386-392, 2000.
51. Reidy PT, Walker DK, Dickinson JM, Gundermann DM, Drummond MJ, Timmerman KL, Fry CS, Borack MS, Cope MB, Mukherjea R, Jennings K, Volpi E, Rasmussen BB. Protein blend ingestion following resistance exercise promotes human muscle protein synthesis. J Nutr 143: 410-416, 2013.
52. Reitelseder S, Agergaard J, Doessing S, Helmark IC, Lund P, Kristensen NB, Frystyk J, Flyvbjerg A, Schjerling P, van Hall G, Kjaer M, Holm L. Whey and casein labeled with L-[1-13C]leucine and muscle protein synthesis: effect of resistance exercise and protein ingestion. Am J Physiol Endocrinol Metab 300: E231-E242, 2011.
53. Reitelseder S, Agergaard J, Doessing S, Helmark IC, Schjerling P, van Hall G, Kjaer M, Holm L. Positive muscle protein net balance and differential regulation of atrogene expression after resistance exercise and milk protein supplementation. Eur J Nutr 53: 321-33, 2014.
54. Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM. 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: 987-992, 2009.
55. Tang JE, Phillips SM. Maximizing muscle protein anabolism: the role of protein quality. Curr Opin Clin Nutr Metab Care 12: 66-71, 2009.
56. Taylor PM. Role of amino acid transporters in amino acid sensing. Am J Clin Nutr 99: 223S-230S, 2014.
57. Tipton KD, Elliott TA, Cree MG, Aarsland AA, Sanford AP, Wolfe RR. Stimulation of net muscle protein synthesis by whey protein ingestion before and after exercise. Am J Physiol Endocrinol Metab 292: E71-E76, 2007.
58. Tipton KD, Elliott TA, Cree MG, Wolf SE, Sanford AP, Wolfe RR. Ingestion of casein and whey proteins result in muscle anabolism after resistance exercise. Med Sci Sports Exerc 36: 2073-2081, 2004.
59. Tipton KD, Elliott TA, Ferrando AA, Aarsland AA, Wolfe RR. Stimulation of muscle anabolism by resistance exercise and ingestion of leucine plus protein. Appl Physiol Nutr Metab 34: 151-161, 2009.
60. Tipton KD, Ferrando AA, Phillips SM, Doyle D Jr, Wolfe RR. Postexercise net protein synthesis in human muscle from orally administered amino acids. Am J Physiol Endocrinol Metab 276: E628-E634, 1999.
61. Tipton KD, Rasmussen BB, Miller SL, Wolf SE, Owens-Stovall SK, Petrini BE, Wolfe RR. Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise. Am J Physiol Endocrinol Metab 281: E197-E206, 2001.
62. Volpi E, Kobayashi H, Sheffield-Moore M, Mittendorfer B, Wolfe RR. Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am J Clin Nutr 78: 250-258, 2003.
63. Walker DK, Dickinson JM, Timmerman KL, Drummond MJ, Reidy PT, Fry CS, Gundermann DM, Rasmussen BB. Exercise, Amino Acids and Aging in the Control of Human Muscle Protein Synthesis. Med Sci Sports Exerc 43: 2249-2258, 2011.
64. Wilkinson SB, Tarnopolsky MA, Macdonald MJ, Macdonald JR, Armstrong D, Phillips SM. 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: 1031-1040, 2007.
65. Willoughby DS, Stout JR, Wilborn CD. Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength. Amino Acids 32: 467-477, 2007.
66. Wolfe RR, Chinkes DL. Isotope Tracers in Metabolic Research: Principles and Practice of Kinetic Analysis. Hoboken, NJ: Wiley-Liss, 2005, p. vii, 474.
67. Yanagida O, Kanai Y, Chairoungdua A, Kim DK, Segawa H, Nii T, Cha SH, Matsuo H, Fukushima J, Fukasawa Y, Tani Y, Taketani Y, Uchino H, Kim JY, Inatomi J, Okayasu I, Miyamoto K, Takeda E, Goya T, Endou H. Human L-type amino acid transporter 1 (LAT1): characterization of function and expression in tumor cell lines. Biochim Biophys Acta 1514: 291-302, 2001.