Consumption of milk protein or whey protein results in a similar increase in muscle protein synthesis in middle aged men

Nutrients

Volumn 7, Issue 10, 2015, Pages 8685-8699

  Mitchell, Cameron J ^a   McGregor, Robin A ^b,c   D’Souza, Randall F ^a   Thorstensen, Eric B ^a   Markworth, James F ^a   Fanning, Aaron C ^d   Poppitt, Sally D ^b   Cameron Smith, David ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c Inje University   (South Korea)

^d FONTERRA RESEARCH CENTRE   (New Zealand)

Author keywords

Amino acids; Fractional synthetic rate; Milk protein; Muscle; Stable isotopes; Whey protein

Indexed keywords

HIGH DENSITY LIPOPROTEIN; LEUCINE; LOW DENSITY LIPOPROTEIN; MILK PROTEIN; MUSCLE PROTEIN; PHENYLALANINE; WHEY PROTEIN;

ADULT; ARTICLE; BLOOD BIOCHEMISTRY; CONTROLLED STUDY; DIGESTION; DOUBLE BLIND PROCEDURE; DUAL ENERGY X RAY ABSORPTIOMETRY; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; INSULIN RESISTANCE; MALE; MIDDLE AGED; MUSCLE; MUSCLE BIOPSY; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MUSCLE MASS; MUSCLE STRENGTH; NORMAL HUMAN; PHYSICAL ACTIVITY; PROTEIN INTAKE; SARCOPENIA; CLINICAL TRIAL; COMPARATIVE STUDY; DRUG EFFECTS; METABOLISM; MUSCLE FIBRIL; PROTEIN SYNTHESIS;

HUMANS; MALE; MIDDLE AGED; MILK PROTEINS; MUSCLE PROTEINS; MUSCLES; MYOFIBRILS; PROTEIN BIOSYNTHESIS; WHEY PROTEINS;

EID: 84945126640     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu7105420     Document Type: Article

References (53)

1. Lauretani, F.; Russo, C.R.; Bandinelli, S.; Bartali, B.; Cavazzini, C.; di Iorio, A.; Corsi, A.M.; Rantanen, T.; Guralnik, J.M.; Ferrucci, L. Age-associated changes in skeletal muscles and their effect on mobility: An operational diagnosis of sarcopenia. J. Appl. Physiol. 2003, 95, 1851–1860. [CrossRef] [PubMed]
2. Von Haehling, S.; Morley, J.E.; Anker, S.D. An overview of sarcopenia: Facts and numbers on prevalence and clinical impact. J. Cachexia Sarcopenia Muscle 2010, 1, 129–133. [CrossRef] [PubMed]
3. McGregor, R.A.; Cameron-Smith, D.; Poppitt, S.D. It is not just muscle mass: A review of muscle quality, composition and metabolism during ageing as determinants of muscle function and mobility in later life. Longev. Healthspan 2014, 3, 9. [CrossRef] [PubMed]
4. Cruz-Jentoft, A.J.; Baeyens, J.P.; Bauer, J.M.; Boirie, Y.; Cederholm, T.; Landi, F.; Martin, F.C.; Michel, J.P.; Rolland, Y.; Schneider, S.M.; et al. Sarcopenia: European consensus on definition and diagnosis: Report of the european working group on sarcopenia in older people. Age Ageing 2010, 39, 412–423. [CrossRef] [PubMed]
5. Rennie, M.J. Exercise- and nutrient-controlled mechanisms involved in maintenance of the musculoskeletal mass. Biochem. Soc. Trans. 2007, 35, 1302–1305. [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. [PubMed]
7. Cuthbertson, D.; Smith, K.; Babraj, J.; Leese, G.; Waddell, T.; Atherton, P.; Wackerhage, H.; Taylor, P.M.; Rennie, M.J. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 2005, 19, 422–424. [CrossRef] [PubMed]
8. Burd, N.A.; Gorissen, S.H.; van Loon, L.J. Anabolic resistance of muscle protein synthesis with aging. Exerc. Sport Sci. Rev. 2013, 41, 169–173. [CrossRef] [PubMed]
9. 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]
10. Reitelseder, S.; Agergaard, J.; Doessing, S.; Helmark, I.C.; Lund, P.; Kristensen, N.B.; Frystyk, J.; Flyvbjerg, A.; Schjerling, P.; Van Hall, G.; et al. 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. 2011, 300, E231–E242. [CrossRef] [PubMed]
11. 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]
12. Wilkinson, S.B.; Tarnopolsky, M.A.; Macdonald, M.J.; Macdonald, J.R.; Armstrong, D.; Phillips, S.M. 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. 2007, 85, 1031–1040. [PubMed]
13. Yang, Y.; Churchward-Venne, T.A.; Burd, N.A.; Breen, L.; Tarnopolsky, M.A.; Phillips, S.M. Myofibrillar protein synthesis following ingestion of soy protein isolate at rest and after resistance exercise in elderly men. Nutr. Metab. 2012, 9, 57. [CrossRef] [PubMed]
14. Dideriksen, K.J.; Reitelseder, S.; Petersen, S.G.; Hjort, M.; Helmark, I.C.; Kjaer, M.; Holm, L. Stimulation of muscle protein synthesis by whey and caseinate ingestion after resistance exercise in elderly individuals. Scand. J. Med. Sci. Sports 2011, 21, e372–e383. [CrossRef] [PubMed]
15. Pennings, B.; Boirie, Y.; Senden, J.M.; Gijsen, A.P.; Kuipers, H.; Van Loon, L.J. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am.J. Clin. Nutr. 2011, 93, 997–1005. [CrossRef] [PubMed]
16. Robinson, M.J.; Burd, N.A.; Breen, L.; Rerecich, T.; Yang, Y.; Hector, A.J.; Baker, S.K.; Phillips, S.M. Dose-dependent responses of myofibrillar protein synthesis with beef ingestion are enhanced with resistance exercise in middle-aged men. Appl. Physiol. Nutr. Metab. 2013, 38, 120–125. [CrossRef] [PubMed]
17. Tang, J.E.; Manolakos, J.J.; Kujbida, G.W.; Lysecki, P.J.; Moore, D.R.; Phillips, S.M. Minimal whey protein with carbohydrate stimulates muscle protein synthesis following resistance exercise in trained young men. Appl. Physiol. Nutr. Metab. 2007, 32, 1132–1138. [CrossRef] [PubMed]
18. Mitchell, C.J.; Della Gatta, P.A.; Petersen, A.C.; Cameron-Smith, D.; Markworth, J.F. Soy protein ingestion results in less prolonged p70s6 kinase phosphorylation compared to whey protein after resistance exercise in older men. J. Int. Soc. Sports Nutr. 2015, 12, 6. [CrossRef] [PubMed]
19. 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]
20. Smithers, G.W. Whey and whey proteins—from “gutter-to-gold”. Int. Dairy J. 2008, 18, 695–704. [CrossRef]
21. Severin, S.; Wenshui, X. Milk biologically active components as nutraceuticals: Review. Crit. Rev. Food Sci. Nutr. 2005, 45, 645–656. [CrossRef] [PubMed]
22. Drummond, M.J.; Dreyer, H.C.; Fry, C.S.; Glynn, E.L.; Rasmussen, B.B. Nutritional and contractile regulation of human skeletal muscle protein synthesis and mTORC1 signaling. J. Appl. Physiol. 2009, 106, 1374–1384. [CrossRef] [PubMed]
23. Zoncu, R.; Bar-Peled, L.; Efeyan, A.; Wang, S.; Sancak, Y.; Sabatini, D.M. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar h(+)-atpase. Science 2011, 334, 678–683. [CrossRef] [PubMed]
24. Han, J.M.; Jeong, S.J.; Park, M.C.; Kim, G.; Kwon, N.H.; Kim, H.K.; Ha, S.H.; Ryu, S.H.; Kim, S. Leucyl-trna synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 2012, 149, 410–424. [CrossRef] [PubMed]
25. 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]
26. 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]
27. Breen, L.; Churchward-Venne, T.A. Leucine: A nutrient “trigger” for muscle anabolism, but what more? J. Physiol. 2012, 590, 2065–2066. [CrossRef] [PubMed]
28. Matthews, D.R.; Hosker, J.P.; Rudenski, A.S.; Naylor, B.A.; Treacher, D.F.; Turner, R.C. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28, 412–419. [CrossRef] [PubMed]
29. Roza, A.M.; Shizgal, H.M. The harris benedict equation reevaluated: Resting energy requirements and the body cell mass. Am. J. Clin. Nutr. 1984, 40, 168–182. [PubMed]
30. Burd, N.A.; West, D.W.; Staples, A.W.; Atherton, P.J.; Baker, J.M.; Moore, D.R.; Holwerda, A.M.; Parise, G.; Rennie, M.J.; Baker, S.K.; et al. Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS ONE 2010, 5, e12033. [CrossRef] [PubMed]
31. Churchward-Venne, T.A.; Cotie, L.M.; MacDonald, M.J.; Mitchell, C.J.; Prior, T.; Baker, S.K.; Phillips, S.M. Citrulline does not enhance blood flow, microvascular circulation, or myofibrillar protein synthesis in elderly men at rest or following exercise. Am. J. Physiol. Endocrinol. Metab. 2014, 307, E71–E83. [CrossRef] [PubMed]
32. March, J.F. A modified technique for the quantitative analysis of amino acids by gas chromatography using heptafluorobutyric n-propyl derivatives. Anal. Biochem. 1975, 69, 420–442. [CrossRef]
33. Matthews, D.E.; Pesola, G.; Campbell, R.G. Effect of epinephrine on amino acid and energy metabolism in humans. Am. J. Physiol. 1990, 258, E948–E956. [PubMed]
34. Tang, J.E.; Phillips, S.M. Maximizing muscle protein anabolism: The role of protein quality. Curr. Opin. Clin. Nutr. Metab. Care 2009, 12, 66–71. [CrossRef] [PubMed]
35. Atherton, P.J.; Smith, K.; Etheridge, T.; Rankin, D.; Rennie, M.J. Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells. Amino Acids 2010, 38, 1533–1539. [CrossRef] [PubMed]
36. Burd, N.A.; Yang, Y.; Moore, D.R.; Tang, J.E.; Tarnopolsky, M.A.; Phillips, S.M. 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. 2012, 108, 958–962. [CrossRef] [PubMed]
37. West, D.W.; Burd, N.A.; Coffey, V.G.; Baker, S.K.; Burke, L.M.; Hawley, J.A.; Moore, D.R.; Stellingwerff, T.; Phillips, S.M. Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. Am. J. Clin. Nutr. 2011, 94, 795–803. [CrossRef] [PubMed]
38. 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]
39. Mitchell, W.K.; Phillips, B.E.; Williams, J.P.; Rankin, D.; Lund, J.N.; Smith, K.; Atherton, P.J. A dose- rather than delivery profile-dependent mechanism regulates the “muscle-full” effect in response to oral essential amino acid intake in young men. J. Nutr. 2015, 145, 207–214. [CrossRef] [PubMed]
40. Mitchell, W.K.; Phillips, B.E.; Williams, J.P.; Rankin, D.; Lund, J.N.; Wilkinson, D.J.; Smith, K.; Atherton, P.J. The impact of delivery profile of essential amino acids upon skeletal muscle protein synthesis in older men: Clinical efficacy of pulse vs. bolus supply. Am. J. Physiol. Endocrinol. Metab. 2015, 309, E450–E457. [CrossRef] [PubMed]
41. Elliot, T.A.; Cree, M.G.; Sanford, A.P.;Wolfe, R.R.; Tipton, K.D. Milk ingestion stimulates net muscle protein synthesis following resistance exercise. Med. Sci. Sports Exerc. 2006, 38, 667–674. [CrossRef] [PubMed]
42. Churchward-Venne, T.A.; Burd, N.A.; Mitchell, C.J.; West, D.W.; Philp, A.; Marcotte, G.R.; Baker, S.K.; Baar, K.; Phillips, S.M. 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. 2012, 590, 2751–2765. [CrossRef] [PubMed]
43. Reidy, P.T.; Walker, D.K.; Dickinson, J.M.; Gundermann, D.M.; Drummond, M.J.; Timmerman, K.L.; Fry, C.S.; Borack, M.S.; Cope, M.B.; Mukherjea, R.; et al. Protein blend ingestion following resistance exercise promotes human muscle protein synthesis. J. Nutr. 2013, 143, 410–416. [CrossRef] [PubMed]
44. Yang, Y.; Breen, L.; Burd, N.A.; Hector, A.J.; Churchward-Venne, T.A.; Josse, A.R.; Tarnopolsky, M.A.; Phillips, S.M. Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. Br. J. Nutr. 2012, 108, 1780–1788. [CrossRef] [PubMed]
45. 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]
46. Pennings, B.; Groen, B.; de Lange, A.; Gijsen, A.P.; Zorenc, A.H.; Senden, J.M.; van Loon, L.J. Amino acid absorption and subsequent muscle protein accretion following graded intakes of whey protein in elderly men. Am. J. Physiol. Endocrinol. Metab. 2012, 302, E992–E999. [CrossRef] [PubMed]
47. Timmerman, K.L.; Dhanani, S.; Glynn, E.L.; Fry, C.S.; Drummond, M.J.; Jennings, K.; Rasmussen, B.B.; Volpi, E. A moderate acute increase in physical activity enhances nutritive flow and the muscle protein anabolic response to mixed nutrient intake in older adults. Am. J. Clin. Nutr. 2012, 95, 1403–1412. [CrossRef] [PubMed]
48. Breen, L.; Phillips, S.M. Skeletal muscle protein metabolism in the elderly: Interventions to counteract the “anabolic resistance” of ageing. Nutr. Metab. 2011, 8, 68. [CrossRef] [PubMed]
49. Farnfield, M.M.; Carey, K.A.; Gran, P.; Trenerry, M.K.; Cameron-Smith, D. Whey protein ingestion activates mtor-dependent signalling after resistance exercise in young men: Adouble-blinded randomized controlled trial. Nutrients 2009, 1, 263–275. [CrossRef] [PubMed]
50. D’Souza, R.F.; Marworth, J.F.; Figueiredo, V.C.; Della Gatta, P.A.; Petersen, A.C.; Mitchell, C.J.; Cameron-Smith, D. Dose-dependent increases in p70S6K phosphorylation and intramuscular branched-chain amino acids in older men following resistance exercise and protein intake. Physiol. Rep. 2014, 2. [CrossRef] [PubMed]
51. Mitchell, C.J.; Churchward-Venne, T.A.; Parise, G.; Bellamy, L.; Baker, S.K.; Smith, K.; Atherton, P.J.; Phillips, S.M. Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PLoS ONE 2014, 9, e89431. [CrossRef] [PubMed]
52. Burd, N.A.; Groen, B.B.; Beelen, M.; Senden, J.M.; Gijsen, A.P.; van Loon, L.J. The reliability of using the single-biopsy approach to assess basal muscle protein synthesis rates in vivo in humans. Metab. 2012, 61, 931–936. [CrossRef] [PubMed]
53. Murphy, C.H.; Churchward-Venne, T.A.; Mitchell, C.J.; Kolar, N.M.; Kassis, A.; Karagounis, L.G.; Burke, L.M.; Hawley, J.A.; Phillips, S.M. Hypoenergetic diet-induced reductions in myofibrillar protein synthesis are restored with resistance training and balanced daily protein ingestion in older men. Am. J. Physiol. Endocrinol. Metab. 2015, 308, E734–E743. [CrossRef] [PubMed]