Whey Protein Augments Leucinemia and Postexercise p70S6K1 Activity Compared With a Hydrolyzed Collagen Blend When in Recovery From Training With Low Carbohydrate Availability

in International Journal of Sport Nutrition and Exercise Metabolism
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We examined the effects of whey versus collagen protein on skeletal muscle cell signaling responses associated with mitochondrial biogenesis and protein synthesis in recovery from an acute training session completed with low carbohydrate availability. In a repeated-measures design (after adhering to a 36-hr exercise–dietary intervention to standardize preexercise muscle glycogen), eight males completed a 75-min nonexhaustive cycling protocol and consumed 22 g of a hydrolyzed collagen blend (COLLAGEN) or whey (WHEY) protein 45 min prior to exercise, 22 g during exercise, and 22 g immediately postexercise. Exercise decreased (p < .05) muscle glycogen content by comparable levels from pre- to postexercise in both trials (≈300–150 mmol/kg·dry weight). WHEY protein induced greater increases in plasma branched chain amino acids (p = .03) and leucine (p = .02) than COLLAGEN. Exercise induced (p < .05) similar increases in PGC-1α (fivefold) mRNA at 1.5 hr postexercise between conditions, although no effect of exercise (p > .05) was observed for p53, Parkin, and Beclin1 mRNA. Exercise suppressed (p < .05) p70S6K1 activity in both conditions immediately postexercise (≈25 fmol·min−1·mg−1). Postexercise feeding increased p70S6K1 activity at 1.5 hr postexercise (p < .05), the magnitude of which was greater (p < .05) in WHEY (180 ± 105 fmol·min−1·mg−1) versus COLLAGEN (73 ± 42 fmol·min−1·mg−1). We conclude that protein composition does not modulate markers of mitochondrial biogenesis when in recovery from a training session deliberately completed with low carbohydrate availability. By contrast, whey protein augments postexercise p70S6K activity compared with hydrolyzed collagen, as likely mediated via increased leucine availability.

Impey, Hammond, Naughton, Langan-Evans, Shepherd, Sharples, Close, and Morton are with the Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, United Kingdom. Cegielski and Smith are with the Division of Medical Sciences and Graduate Entry Medicine, MRC-ARUK Centre for Musculoskeletal Ageing Research, School of Medicine, Faculty of Medicine and Health Sciences, University of Nottingham, Derby, United Kingdom. Jeromson and Hamilton are with Health and Exercise Sciences Research Group, University of Stirling, Stirling, United Kingdom.

Address author correspondence to James P. Morton at J.P.Morton@ljmu.ac.uk.
  • Apró, W., Moberg, M., Hamilton, D.L., Ekblom, B., Rooyackers, O., Holmberg, H.C., & Blomstrand, E. (2015a). Resistance exercise-induced S6K1 kinase activity is not inhibited in human skeletal muscle despite prior activation of AMPK by high-intensity interval cycling. American Journal of Physiology-Endocrinology and Metabolism, 308, 470–481. doi:10.1152/ajpendo.00486.2014

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Apró, W., Moberg, M., Hamilton, D.L., Ekblom, B., Rooyackers, O., Holmberg, H.C., & Blomstrand, E. (2015b). Leucine does not affect mechanistic target of rapamycin complex 1 assembly but is required for maximal ribosomal protein s6 kinase 1 activity in human skeletal muscle following resistance exercise. The FASEB Journal, 29, 4358–4373. doi:10.1096/fj.15-273474

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Areta, J.L., Burke, L.M., Ross, M.L., Camera, D.M., West, D.W., Broad, E.M., … Coffey, V.G. (2013). Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. The Journal of Physiology, 591, 2319–2331. PubMed ID: 23459753 doi:10.1113/jphysiol.2012.244897

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bartlett, J.D., Hawley, J.A., & Morton, J.P. (2015). Carbohydrate availability and exercise training adaptation: Too much of a good thing? European Journal of Sport Science, 15, 3–12. PubMed ID: 24942068 doi:10.1080/17461391.2014.920926

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Breen, L., Philp, A., Witard, O.C., Jackman, S.R., Selby, A., Smith, K., … Tipton, K.D. (2011). The influence of carbohydrate–protein co-ingestion following endurance exercise on myofibrillar and mitochondrial protein synthesis. The Journal of Physiology, 589, 4011–4025. PubMed ID: 21746787 doi:10.1113/jphysiol.2011.211888

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Burke, L.M., Winter, J.A., Cameron-Smith, D., Enslen, M., Farnfield, M., & Decombaz, J. (2012). Effect of intake of different dietary protein sources on plasma amino acid profiles at rest and after exercise. International Journal of Sport Nutrition and Exercise Metabolism, 22, 452–462. PubMed ID: 22807528 doi:10.1123/ijsnem.22.6.452

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Camera, D.M., West, D.W., Burd, N.A., Phillips, S.M., Garnham, A.P., Hawley, J.A., & Coffey, V.G. (2012). Low muscle glycogen concentration does not suppress the anabolic response to resistance exercise. Journal of Applied Physiology, 113, 206–214. PubMed ID: 22628371 doi:10.1152/japplphysiol.00395.2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Castellanos, V.H., Litchford, M.D., & Campbell, W.W. (2006). Modular protein supplements and their application to long-term care. Nutrition in Clinical Practice, 21, 485–504. PubMed ID: 16998147 doi:10.1177/0115426506021005485

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Churchward-Venne, T.A., Breen, L., DiDonato, D.M., Hector, A.J., Mitchell, C.J., Moore, D.R., … Phillips, S.M. (2013) Leucine supplementation of low-protein mixed macronutrient beverage enhances myofibrillar protein synthesis in young men: a double-blind, randomized trial. The American Journal of Clinical Nutrition, 99(2), 276–286.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Coffey, V.G., Moore, D.R., Burd, N.A., Rerecich, T., Stellingwerff, T., Garnham, A.P., … Hawley, J.A. (2011). Nutrient provision increases signalling and protein synthesis in human skeletal muscle after repeated sprints. European Journal of Applied Physiology, 111(7), 1473–1483. doi:10.1007/s00421-010-1768-0

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Coffey, V.G., Zhong, Z., Shield, A., Canny, B.J., Chilbalin, A.V., Zierath, J.R., & Hawley, J.A. (2006). Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. The FASEB Journal, 20, 190–192. PubMed ID: 16267123 doi:10.1096/fj.05-4809fje

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hammond, K.M., Impey, S.G., Currell, K., Mitchell, N., Shepherd, S.O., Jeromson, S., … Morton, J.P. (2016). Postexercise high-fat feeding suppresses p70S6K1 activity in human skeletal muscle. Medicine & Science in Sports & Exercise, 48, 2108–2117. PubMed ID: 27327024 doi:10.1249/MSS.0000000000001009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hawley, J.A., & Morton, J.P. (2014). Ramping up the signal: Promoting endurance training adaptation in skeletal muscle by nutritional manipulation. Clinical and Experimental Pharmacology and Physiology, 41, 608–613. PubMed ID: 25142094 doi:10.1111/1440-1681.12246

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Howarth, K.R., Phillips, S.M., MacDonald, M.J., Richards, D., Moreau, N.A., & Gibala, M.J. (2010). Effect of glycogen availability on human skeletal muscle protein turnover during exercise and recovery. Journal of Applied Physiology, 109, 431–438. doi:10.1152/japplphysiol.00108.2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hulston, C.J., Wolsk, E., Grondahl, T.S., Yfanti, C., & Van Hall, G. (2011). Protein intake does not increase vastus lateralis muscle protein synthesis during cycling. Medicine & Science in Sports & Exercise, 43, 1635–1642. doi:10.1249/MSS.0b013e31821661ab

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Impey, S.G., Hammond, K.M., Shepherd, S.O., Sharples, A.P., Stewart, C., Limb, M., … Morton, J.P. (2016). Fuel for the work required: A practical approach to amalgamating train-low paradigms for endurance athletes. Physiological Reports, 4, e12803. doi:10.14814/phy2.12803

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Impey, S.G., Hearris, M., Hammond, K.M., Bartlett, J.D., Louis, J.L., Close, G.L., & Morton, J.P. (2018). Fuel for the work required: A theoretical framework for carbohydrate periodization and the glycogen threshold hypothesis. Sports Medicine, 48(5), 1031–1048. PubMed ID: 29453741 doi:10.1007/s40279-018-0867-7

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Impey, S.G., Smith, D., Robinson, A.L., Owens, D.J., Bartlett, J.D., Smith, K., … Morton, J.P. (2015). Leucine-enriched protein feeding does not impair exercise-induced free fatty acid availability and lipid oxidation: Beneficial implications for training in carbohydrate-restricted states. Amino Acids, 47, 407–416. PubMed ID: 25471599 doi:10.1007/s00726-014-1876-y

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Jeukendrup, A.E., & Wallis, G.A. (2005). Measurement of substrate oxidation during exercise by means of gas exchange measurements. International Journal of Sports Medicine, 26, S28–S37. doi:10.1055/s-2004-830512

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kimball, S.R., Ravi, S., Gordon, B.R., Dennis, M.D., & Jefferson, L.S. (2015). Amino acid-induced activation of mTORC1 in rat liver is attenuated by short-term consumption of a high-fat diet. The Journal of Nutrition, 145, 2496–2502. PubMed ID: 26400964 doi:10.3945/jn.115.215491

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lemon, P.W., & Mullin, J.P. (1980). Effect of initial muscle glycogen levels on protein catabolism during exercise. Journal of Applied Physiology, 48, 624–629. PubMed ID: 7380688 doi:10.1152/jappl.1980.48.4.624

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Loucks, A.B., Kiens, B., & Wright, H.H. (2011). Energy availability in athletes. Journal of Sports Sciences, 29(Suppl 1), S7–S15. doi:10.1080/02640414.2011.588958

    • Crossref
    • Search Google Scholar
    • Export Citation
  • MacNaughton, L.S., Wardle, S.L., Witard, O.C., McGlory, C., Hamilton, D.L., Jeromson, S., … Tipton, K.D. (2016). The response of muscle protein synthesis following whole-body resistance exercise is greater following 40 g than 20 g of ingested whey protein. Physiological Reports, 4(15), e12893. doi:10.14814/phy2.12893

    • Crossref
    • Search Google Scholar
    • Export Citation
  • McGlory, C., White, A., Treins, C., Drust, B., Close, G.L., Maclaren, D.P., … Hamilton, D.L. (2014). Application of the [γ-32p] ATP kinase assay to study anabolic signalling in human skeletal muscle. Journal of Applied Physiology, 116, 504–513. doi:10.1152/japplphysiol.01072.2013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Moberg, M., Apró, W., Ohlsson, I., Pontén, M., Villanueva, A., Ekblom, B., & Blomstrand, E. (2014). Absence of leucine in an essential amino acid supplement reduces activation of mTORC1 signalling following resistance exercise in young females. Applied Physiology, Nutrition, and Metabolism, 39, 183–194. doi:10.1139/apnm-2013-0244

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Moore, D.R., Camera, D.M., Areta, J.L., & Hawley, J.A. (2014). Beyond muscle hypertrophy: Why dietary protein is important for endurance athletes. Applied Physiology, Nutrition, and Metabolism, 39, 987–997. doi:10.1139/apnm-2013-0591

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Moore, D.R., Robinson, M.J., Fry, J.L., Tang, J.E., Glover, E.I., Wilkinson, S.B., … Phillips, S.M. (2009). Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. The American Journal of Clinical Nutrition, 89, 161–168. PubMed ID: 19056590 doi:10.3945/ajcn.2008.26401

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pasiakos, S.M., McClung, H.L., McClung, J.P., Margolis, L.M., Andersen, N.E., Gloutier, G.J., … Young, A.J. (2011). Leucine-enriched essential amino acid supplementation during moderate steady state exercise enhances postexercise muscle protein synthesis. The American Journal of Clinical Nutrition, 94, 809–818. PubMed ID: 21775557 doi:10.3945/ajcn.111.017061

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Phillips, S.M. (2016). The impact of protein quality on the promotion of resistance exercise-induced changes in muscle mass. Nutrition & Metabolism, 13, 64. doi:10.1186/s12986-016-0124-8

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rowlands, D.S., Nelson, A.R., Phillips, S.M., Faulkner, J.A., Clarke, J., Burd, N.A., … Stellingwerff, T. (2015). Protein-leucine fed dose effects on muscle protein synthesis after endurance exercise. Medicine & Science in Sports & Exercise, 47, 547–555. doi:10.1249/MSS.0000000000000447

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rowlands, D.S., Thomson, J.S., Timmons, B.W., Raymond, F., Fuerholz, A., Mansourian, R., … Tarnopolsky, M.A. (2011). Transcriptome and translational signaling following endurance exercise in trained skeletal muscle: Impact of dietary protein. Physiological Genomics, 43, 1004–1020. PubMed ID: 21730029 doi:10.1152/physiolgenomics.00073.2011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Stephens, F.B., Chee, C., Wall, B.J., Murton, A.J., Shannon, C.E., van Loon, L.J., & Tsintzas, K. (2015). Lipid-induced insulin resistance is associated with an impaired skeletal muscle protein synthetic response to amino acid ingestion in healthy young men. Diabetes, 64, 1615–1620. PubMed ID: 25524913 doi:10.2337/db14-0961

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Stokes, T., Hector, A.J., Morton, R.W., McGlory, C., & Phillips, S.M. (2018). Recent perspectives regarding the role of dietary protein for the promotion of muscle hypertrophy with resistance exercise training. Nutrients, 10, E180. doi:10.3390/nu10020180

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tang, J.E., Moore, D.R., Kujbida, G.W., Tarnopolsky, M.A., & Phillips, S.M. (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. Journal of Applied Physiology, 107, 987–992. PubMed ID: 19589961 doi:10.1152/japplphysiol.00076.2009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Taylor, C., Bartlett, J.D., van de Graaf, C.S., Louhelainen, J., Coyne, V., Iqbal, Z., … Morton, J.P. (2013). Protein ingestion does not impair exercise-induced AMPK signalling when in a glycogen-depleted state: Implications for train-low compete-high. European Journal of Applied Physiology, 113, 1457–1468. PubMed ID: 23263742 doi:10.1007/s00421-012-2574-7

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Thomas, D.T., Erdman, K.A., & Burke, L.M. (2016). Position of the Academy of Nutrition and Dietetics, Dietitians of Canada, and the American College of Sports Medicine: Nutrition and athletic performance. Journal of the Academy of Nutrition and Dietetics, 116, 501–528. doi:10.1016/j.jand.2015.12.006

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Vogt, S., Heinrich, L., Schumacher, Y.O., Grosshauser, M., Blum, A., Koing, D., … Schmid, A. (2005). Energy intake and energy expenditure of elite cyclists during preseason training. International Journal of Sports Medicine, 26, 701–706. doi:10.1055/s-2004-830438

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wagenmakers, A.J., Beckers, E.J., Brouns, F., Kuipers, H., Soeters, P.B., Moore, D.R., van der Vusse, & Saris, W.H. (1991) Carbohydrate supplementation, glycogen deletion, and amino acid metabolism during exercise. Journal of Physiology Endocrinology And Metabolism, 260(6 Pt 1), E883–890.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • West, D.W., Burd, N.A., Coffey, V.G., Baker, S.K., Burke, L.M., Hawley, J.A., … Phillips, S.M. (2011). Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. The American Journal of Clinical Nutrition, 94, 795–803. PubMed ID: 21795443 doi:10.3945/ajcn.111.013722

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wilkinson, S.B., Tarnopolsky, M.A., Macdonald, M.J., Macdonald, J.R., Armstrong, D., & Philips, S.M. (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. The American Journal of Clinical Nutrition, 85, 1031–1040. PubMed ID: 17413102 doi:10.1093/ajcn/85.4.1031

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Witard, O.C., Jackman, S.R., Breen, L., Smith, K., Selby, A., & Tipton, K.D. (2014) Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. The American Journal of Clinical Nutrition, 99, 86–95. PubMed ID: 24257722 doi:10.3945/ajcn.112.055517

    • Crossref
    • Search Google Scholar
    • Export Citation
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