The metabolic and temporal basis of muscle hypertrophy in response to resistance exercise

References

• Aagaard, P., Andersen, J. L., Dyhre-Poulsen, P., Leffers, A. M., Wagner, A., Magnusson, S. P., … Simonsen, E. B. (2001). A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. The Journal of Physiology, 534(Pt 2), 613–623. doi: 10.1111/j.1469-7793.2001.t01-1-00613.x
   PubMed Web of Science ®Google Scholar
• Atherton, P. J., Etheridge, T., Watt, P. W., Wilkinson, D., Selby, A., Rankin, D., … Rennie, M. J. (2010). Muscle full effect after oral protein: Time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. The American Journal of Clinical Nutrition, 92(5), 1080–1088. http://doi.org/10.3945/ajcn.2010.29819 doi: 10.3945/ajcn.2010.29819
   PubMed Web of Science ®Google Scholar
• Atherton, P. J., Phillips, B. E., Brook, M. S., Wilkinson, D. J., Smith, K., Etheridge, T. E., … Vagula, M. C. (2015). Commentaries on Viewpoint: What is the relationship between acute measure of muscle protein synthesis and changes in muscle mass? Journal of Applied Physiology (Bethesda, Md. : 1985), 118(4), 498–503. http://doi.org/10.1152/japplphysiol.01069.2014
   Web of Science ®Google Scholar
• Atherton, P. J., & Smith, K. (2012). Muscle protein synthesis in response to nutrition and exercise. The Journal of Physiology, 590(Pt 5), 1049–1057. http://doi.org/10.1113/jphysiol.2011.225003 doi: 10.1113/jphysiol.2011.225003
   PubMed Web of Science ®Google Scholar
• Atherton, P. J., Smith, K., Etheridge, T., Rankin, D., & Rennie, M. J. (2010). Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells. Amino Acids, 38(5), 1533–1539. http://doi.org/10.1007/s00726-009-0377-x doi: 10.1007/s00726-009-0377-x
   PubMed Web of Science ®Google Scholar
• Babraj, J. a., Cuthbertson, D. J. R., Smith, K., Langberg, H., Miller, B., Krogsgaard, M. R., … Rennie, M. J. (2005). Collagen synthesis in human musculoskeletal tissues and skin. American Journal of Physiology. Endocrinology and Metabolism, 289(5), E864–E869. http://doi.org/10.1152/ajpendo.00243.2005 doi: 10.1152/ajpendo.00243.2005
   PubMed Web of Science ®Google Scholar
• Baroni, B. M., Geremia, J. M., Rodrigues, R., De Azevedo Franke, R., Karamanidis, K., & Vaz, M. A. (2013). Muscle architecture adaptations to knee extensor eccentric training: Rectus femoris vs. vastus lateralis. Muscle & Nerve, 48(4), 498–506. http://doi.org/10.1002/mus.23785 doi: 10.1002/mus.23785
   PubMed Web of Science ®Google Scholar
• Bederman, I. R., Foy, S., Chandramouli, V., Alexander, J. C., & Previs, S. F. (2009). Triglyceride synthesis in epididymal adipose tissue: Contribution of glucose and non-glucose carbon sources. The Journal of Biological Chemistry, 284(10), 6101–6108. http://doi.org/10.1074/jbc.M808668200 doi: 10.1074/jbc.M808668200
   PubMed Web of Science ®Google Scholar
• Bennet, W. M., Connacher, A. A., Scrimgeour, C. M., Smith, K., & Rennie, M. J. (1989). Increase in anterior tibialis muscle protein synthesis in healthy man during mixed amino acid infusion: Studies of incorporation of [1-13C]leucine. Clinical Science (London, England : 1979), 76(4), 447–454. doi: 10.1042/cs0760447
   PubMed Web of Science ®Google Scholar
• Biolo, G., Maggi, S. P., Williams, B. D., Tipton, K. D., & Wolfe, R. R. (1995). Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans I. The American Journal of Physiology, 268(3 Pt 1), E514–E520.
   PubMed Web of Science ®Google Scholar
• Biolo, G., Tipton, K. D., Klein, S., & Wolfe, R. R. (1997). An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. The American Journal of Physiology, 273(1 Pt 1), E122–E129.
   PubMed Web of Science ®Google Scholar
• Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., … Yancopoulos, G. D. (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nature Cell Biology, 3(11), 1014–1019. http://doi.org/10.1038/ncb1101-1014 doi: 10.1038/ncb1101-1014
   PubMed Web of Science ®Google Scholar
• Bohé, J., Low, J. F., Wolfe, R. R., & Rennie, M. J. (2001). Latency and duration of stimulation of human muscle protein synthesis during continuous infusion of amino acids. The Journal of Physiology, 532(Pt 2), 575–579. doi: 10.1111/j.1469-7793.2001.0575f.x
   PubMed Web of Science ®Google Scholar
• Bohé, J., Low, A., Wolfe, R. R., & Rennie, M. J. (2003). Human muscle protein synthesis is modulated by extracellular, not intramuscular amino acid availability: A dose-response study. The Journal of Physiology, 552(Pt 1), 315–324. http://doi.org/10.1113/jphysiol.2003.050674 doi: 10.1113/jphysiol.2003.050674
   PubMed Web of Science ®Google Scholar
• Bonfils, G., Jaquenoud, M., Bontron, S., Ostrowicz, C., Ungermann, C., & De Virgilio, C. (2012). Leucyl-tRNA synthetase controls TORC1 via the EGO complex. Molecular Cell, 46(1), 105–110. http://doi.org/10.1016/j.molcel.2012.02.009 doi: 10.1016/j.molcel.2012.02.009
   PubMed Web of Science ®Google Scholar
• Breen, L., Stokes, K. a., Churchward-Venne, T. a., Moore, D. R., Baker, S. K., Smith, K., … Phillips, S. M. (2013). Two weeks of reduced activity decreases leg lean mass and induces “anabolic resistance” of myofibrillar protein synthesis in healthy elderly. The Journal of Clinical Endocrinology and Metabolism, 98(6), 2604–2612. http://doi.org/10.1210/jc.2013-1502 doi: 10.1210/jc.2013-1502
   PubMed Web of Science ®Google Scholar
• Bukhari, S. S., Phillips, B. E., Wilkinson, D. J., Limb, M. C., Rankin, D., Mitchell, W. K., … Atherton, P. J. (2015). Intake of low-dose leucine-rich essential amino acids stimulates muscle anabolism equivalently to bolus whey protein in older women, at rest and after exercise. American Journal of Physiology – Endocrinology and Metabolism, ajpendo.00481.2014. http://doi.org/10.1152/ajpendo.00481.2014
   PubMed Web of Science ®Google Scholar
• Burd, N. A., Holwerda, A. M., Selby, K. C., West, D. W. D., Staples, A. W., Cain, N. E., … Phillips, S. M. (2010). Resistance exercise volume affects myofibrillar protein synthesis and anabolic signalling molecule phosphorylation in young men. The Journal of Physiology, 588(Pt 16), 3119–3130. http://doi.org/10.1113/jphysiol.2010.192856 doi: 10.1113/jphysiol.2010.192856
   PubMed Web of Science ®Google Scholar
• Burd, N. A., West, D. W. D., Moore, D. R., Atherton, P. J., Staples, A. W., Prior, T., … Phillips, S. M. (2011). Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24 h after resistance exercise in young men. The Journal of Nutrition, 141(4), 568–573. http://doi.org/10.3945/jn.110.135038 doi: 10.3945/jn.110.135038
   PubMed Web of Science ®Google Scholar
• Busch, R., Kim, Y., Neese, R. A., Schade-Serin, V., Collins, M., Awada, M., … Hellerstein, M. K. (2006). Measurement of protein turnover rates by heavy water labeling of nonessential amino acids. Biochimica et Biophysica Acta (BBA) – General Subjects, 1760(5), 730–744. http://doi.org/10.1016/j.bbagen.2005.12.023 doi: 10.1016/j.bbagen.2005.12.023
   PubMed Web of Science ®Google Scholar
• Chesley, A., MacDougall, J. D., Tarnopolsky, M. A., Atkinson, S. A., & Smith, K. (1992). Changes in human muscle protein synthesis after resistance exercise. Journal of Applied Physiology (Bethesda, Md. : 1985), 73(4), 1383–1388.
   PubMed Web of Science ®Google Scholar
• Constantin, D., Menon, M. K. M., Houchen-Wolloff, L., Morgan, M. D., Singh, S. J., Greenhaff, P., & Steiner, M. C. (2013). Skeletal muscle molecular responses to resistance training and dietary supplementation in COPD. Thorax, 68(7), 625–633. http://doi.org/10.1136/thoraxjnl-2012-202764 doi: 10.1136/thoraxjnl-2012-202764
   PubMed Web of Science ®Google Scholar
• Cuthbertson, D., Smith, K., Babraj, J., Leese, G., Waddell, T., Atherton, P., … Rennie, M. J. (2005). Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB Journal : Official Publication of the Federation of American Societies for Experimental Biology, 19(3), 422–424. http://doi.org/10.1096/fj.04-2640fje
   PubMed Web of Science ®Google Scholar
• Cuthbertson, D. J., Babraj, J., Smith, K., Wilkes, E., Fedele, M. J., Esser, K., & Rennie, M. (2006). Anabolic signaling and protein synthesis in human skeletal muscle after dynamic shortening or lengthening exercise. American Journal of Physiology. Endocrinology and Metabolism, 290(4), E731–E738. http://doi.org/10.1152/ajpendo.00415.2005 doi: 10.1152/ajpendo.00415.2005
   PubMed Web of Science ®Google Scholar
• D'Antona, G., Lanfranconi, F., Pellegrino, M. A., Brocca, L., Adami, R., Rossi, R., … Bottinelli, R. (2006). Skeletal muscle hypertrophy and structure and function of skeletal muscle fibres in male body builders. The Journal of Physiology, 570(Pt 3), 611–627. http://doi.org/10.1113/jphysiol.2005.101642 doi: 10.1113/jphysiol.2005.101642
   PubMed Web of Science ®Google Scholar
• De Boer, M. D., Selby, A., Atherton, P., Smith, K., Seynnes, O. R., Maganaris, C. N., … Rennie, M. J. (2007). The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse. The Journal of Physiology, 585(Pt 1), 241–251. http://doi.org/10.1113/jphysiol.2007.142828 doi: 10.1113/jphysiol.2007.142828
   PubMed Web of Science ®Google Scholar
• Decaris, M. L., Emson, C. L., Li, K., Gatmaitan, M., Luo, F., Cattin, J., … Hellerstein, M. K. (2015). Turnover Rates of Hepatic Collagen and Circulating Collagen-Associated Proteins in Humans with Chronic Liver Disease. PloS One, 10(4), e0123311. http://doi.org/10.1371/journal.pone.0123311 doi: 10.1371/journal.pone.0123311
   PubMed Web of Science ®Google Scholar
• DeFreitas, J. M., Beck, T. W., Stock, M. S., Dillon, M. a., & Kasishke, P. R. (2011). An examination of the time course of training-induced skeletal muscle hypertrophy. European Journal of Applied Physiology, 111(11), 2785–2790. http://doi.org/10.1007/s00421-011-1905-4 doi: 10.1007/s00421-011-1905-4
   PubMed Web of Science ®Google Scholar
• Dreyer, H. C., Fujita, S., Cadenas, J. G., Chinkes, D. L., Volpi, E., & Rasmussen, B. B. (2006). Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle. The Journal of Physiology, 576(Pt 2), 613–624. http://doi.org/10.1113/jphysiol.2006.113175 doi: 10.1113/jphysiol.2006.113175
   PubMed Web of Science ®Google Scholar
• Drummond, M. J., Fry, C. S., Glynn, E. L., Dreyer, H. C., Dhanani, S., Timmerman, K. L., … Rasmussen, B. B. (2009). Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis. The Journal of Physiology, 587(Pt 7), 1535–1546. http://doi.org/10.1113/jphysiol.2008.163816 doi: 10.1113/jphysiol.2008.163816
   PubMed Web of Science ®Google Scholar
• Drummond, M. J., Miyazaki, M., Dreyer, H. C., Pennings, B., Dhanani, S., Volpi, E., … Rasmussen, B. B. (2009). Expression of growth-related genes in young and older human skeletal muscle following an acute stimulation of protein synthesis. Journal of Applied Physiology (Bethesda, Md. : 1985), 106(4), 1403–1411. http://doi.org/10.1152/japplphysiol.90842.2008
   PubMed Web of Science ®Google Scholar
• Dufner, D. a., Bederman, I. R., Brunengraber, D. Z., Rachdaoui, N., Ismail-Beigi, F., Siegfried, B. a., … Previs, S. F. (2005). Using 2H2O to study the influence of feeding on protein synthesis: Effect of isotope equilibration in vivo vs. in cell culture. American Journal of Physiology. Endocrinology and Metabolism, 288(6), E1277–E1283. http://doi.org/10.1152/ajpendo.00580.2004 doi: 10.1152/ajpendo.00580.2004
   PubMed Web of Science ®Google Scholar
• Escobar, J., Frank, J. W., Suryawan, A., Nguyen, H. V., Horn, C. G., Van Hutson, S. M., & Davis, T. A. (2010). Leucine and a-Ketoisocaproic Acid, but Not Norleucine, Stimulate Skeletal Muscle Protein Synthesis in Neonatal Pigs 1–3. http://doi.org/10.3945/jn.110.123042.mechanisms
   Google Scholar
• Felig, P., Owen, O. E., Wahren, J., & Cahill, G. F. (1969). Amino acid metabolism during prolonged starvation. The Journal of Clinical Investigation, 48(3), 584–594. http://doi.org/10.1172/JCI106017 doi: 10.1172/JCI106017
   PubMed Web of Science ®Google Scholar
• Folland, J. P., & Williams, A. G. (2007). The adaptations to strength training : Morphological and neurological contributions to increased strength. Sports Medicine (Auckland, N.Z.), 37(2), 145–168. doi: 10.2165/00007256-200737020-00004
   PubMed Web of Science ®Google Scholar
• Franchi, M. V., Atherton, P. J., Reeves, N. D., Flück, M., Williams, J., Mitchell, W. K., … Narici, M. V. (2014). Architectural, functional and molecular responses to concentric and eccentric loading in human skeletal muscle. Acta Physiologica (Oxford, England), 210(3), 642–654. http://doi.org/10.1111/apha.12225 doi: 10.1111/apha.12225
   PubMed Web of Science ®Google Scholar
• Fujita, T., Brechue, W. F., Kurita, K., Sato, Y., & Abe, T. (2008). Increased muscle volume and strength following six days of low-intensity resistance training with restricted muscle blood flow. International Journal of KAATSU Training Research, 4(1), 1–8. http://doi.org/10.3806/ijktr.4.1 doi: 10.3806/ijktr.4.1
   Google Scholar
• Gasier, H. G., Fluckey, J. D., Previs, S. F., Wiggs, M. P., & Riechman, S. E. (2012). Acute resistance exercise augments integrative myofibrillar protein synthesis. Metabolism: Clinical and Experimental, 61(2), 153–156. http://doi.org/10.1016/j.metabol.2011.07.001 doi: 10.1016/j.metabol.2011.07.001
   PubMed Web of Science ®Google Scholar
• Glynn, E. L., Fry, C. S., Drummond, M. J., Dreyer, H. C., Dhanani, S., Volpi, E., … Dhanani, S. (2010). Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise, 533–540. http://doi.org/10.1152/ajpregu.00077.2010.
   Google Scholar
• Gorissen, S. H. M., Burd, N. a., Hamer, H. M., Gijsen, A. P., Groen, B. B., & van Loon, L. J. C. (2014). Carbohydrate coingestion delays dietary protein digestion and absorption but does not modulate postprandial muscle protein accretion. The Journal of Clinical Endocrinology and Metabolism, 99(6), 2250–2258. http://doi.org/10.1210/jc.2013-3970 doi: 10.1210/jc.2013-3970
   PubMed Web of Science ®Google Scholar
• Green, H., Goreham, C., Ouyang, J., Ranney, D., & Ball-Burnett, M. (1999). Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. The American Journal of Physiology, 276(Pt 2), R591–R596.
   PubMedGoogle Scholar
• Greenhaff, P. L., Karagounis, L. G., Peirce, N., Simpson, E. J., Hazell, M., Layfield, R., … Rennie, M. J. (2008). Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle. American Journal of Physiology. Endocrinology and Metabolism, 295(3), E595–E604. http://doi.org/10.1152/ajpendo.90411.2008 doi: 10.1152/ajpendo.90411.2008
   PubMed Web of Science ®Google Scholar
• Han, J. M., Jeong, S. J., Park, M. C., Kim, G., Kwon, N. H., Kim, H. K., … Kim, S. (2012). Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell, 149(2), 410–424. http://doi.org/10.1016/j.cell.2012.02.044 doi: 10.1016/j.cell.2012.02.044
   PubMed Web of Science ®Google Scholar
• Hellerstein, M. K. (1999). De novo lipogenesis in humans: Metabolic and regulatory aspects. European Journal of Clinical Nutrition, 53(Suppl. 1), S53–S65. doi: 10.1038/sj.ejcn.1600744
   PubMed Web of Science ®Google Scholar
• Heymsfield, S. B., Smith, R., Aulet, M., Bensen, B., Lichtman, S., Wang, J., & Pierson, R. N. (1990). Appendicular skeletal muscle mass: Measurement by dual-photon absorptiometry. The American Journal of Clinical Nutrition, 52(2), 214–218.
   PubMed Web of Science ®Google Scholar
• Heymsfield, S. B., Wang, Z., Baumgartner, R. N., & Ross, R. (1997). Human body composition: Advances in models and methods. Annual Review of Nutrition, 17, 527–558. http://doi.org/10.1146/annurev.nutr.17.1.527 doi: 10.1146/annurev.nutr.17.1.527
   PubMed Web of Science ®Google Scholar
• Holm, L., O'Rourke, B., Ebenstein, D., Toth, M. J., Bechshoeft, R., Holstein-Rathlou, N. H., … Matthews, D. E. (2013). Determination of steady-state protein breakdown rate in vivo by the disappearance of protein-bound tracer-labeled amino acids: A method applicable in humans. American Journal of Physiology. Endocrinology and Metabolism, 304(8), E895–E907. http://doi.org/10.1152/ajpendo.00579.2012 doi: 10.1152/ajpendo.00579.2012
   PubMed Web of Science ®Google Scholar
• Hornberger, T. a. (2011). Mechanotransduction and the regulation of mTORC1 signaling in skeletal muscle. The International Journal of Biochemistry & Cell Biology, 43(9), 1267–1276. http://doi.org/10.1016/j.biocel.2011.05.007 doi: 10.1016/j.biocel.2011.05.007
   PubMed Web of Science ®Google Scholar
• Hulmi, J. J., Kovanen, V., Selänne, H., Kraemer, W. J., Häkkinen, K., & Mero, A. a. (2009). Acute and long-term effects of resistance exercise with or without protein ingestion on muscle hypertrophy and gene expression. Amino Acids, 37(2), 297–308. http://doi.org/10.1007/s00726-008-0150-6 doi: 10.1007/s00726-008-0150-6
   PubMed Web of Science ®Google Scholar
• Janssen, I., Heymsfield, S. B., & Ross, R. (2002). Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. Journal of the American Geriatrics Society, 50(5), 889–896. doi: 10.1046/j.1532-5415.2002.50216.x
   PubMed Web of Science ®Google Scholar
• Jones, K. I., Doleman, B., Scott, S., Lund, J. N., & Williams, J. P. (2015). Simple psoas cross-sectional area measurement is a quick and easy method to assess sarcopenia and predicts major surgical complications. Colorectal Disease: The Official Journal of the Association of Coloproctology of Great Britain and Ireland, 17(1), O20–O26. http://doi.org/10.1111/codi.12805 doi: 10.1111/codi.12805
   PubMed Web of Science ®Google Scholar
• Kasumov, T., Dabkowski, E. R., Shekar, K. C., Li, L., Ribeiro, R. F., Walsh, K., … Stanley, W. C. (2013). Assessment of cardiac proteome dynamics with heavy water: Slower protein synthesis rates in interfibrillar than subsarcolemmal mitochondria. American Journal of Physiology. Heart and Circulatory Physiology, 304(9), H1201–H1214. http://doi.org/10.1152/ajpheart.00933.2012 doi: 10.1152/ajpheart.00933.2012
   PubMed Web of Science ®Google Scholar
• Kim, J. E., & Chen, J. (2000). Cytoplasmic-nuclear shuttling of FKBP12-rapamycin-associated protein is involved in rapamycin-sensitive signaling and translation initiation. Proceedings of the National Academy of Sciences of the United States of America, 97(26), 14340–14345. http://doi.org/10.1073/pnas.011511898 doi: 10.1073/pnas.011511898
   PubMed Web of Science ®Google Scholar
• Kim, P. L., Staron, R. S., & Phillips, S. M. (2005). Fasted-state skeletal muscle protein synthesis after resistance exercise is altered with training. The Journal of Physiology, 568(Pt1), 283–290. http://doi.org/10.1113/jphysiol.2005.093708 doi: 10.1113/jphysiol.2005.093708
   PubMed Web of Science ®Google Scholar
• Koopman, R., Zorenc, A. H. G., Gransier, R. J. J., Cameron-Smith, D., & van Loon, L. J. C. (2006). Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers. American Journal of Physiology. Endocrinology and Metabolism, 290(6), E1245–E1252. http://doi.org/10.1152/ajpendo.00530.2005 doi: 10.1152/ajpendo.00530.2005
   PubMed Web of Science ®Google Scholar
• Kumar, V., Selby, A., Rankin, D., Patel, R., Atherton, P., Hildebrandt, W., … Rennie, M. J. (2009). Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. The Journal of Physiology, 587(Pt 1), 211–217. http://doi.org/10.1113/jphysiol.2008.164483 doi: 10.1113/jphysiol.2008.164483
   PubMed Web of Science ®Google Scholar
• Lexell, J., & Taylor, C. C. (1989a). Variability in muscle fibre areas in whole human quadriceps muscle: How to reduce sampling errors in biopsy techniques. Clinical Physiology (Oxford, England), 9(4), 333–343. doi: 10.1111/j.1475-097X.1989.tb00987.x
   PubMedGoogle Scholar
• Lexell, J., & Taylor, C. C. (1989b). Variability in muscle fibre areas in whole human quadriceps muscle. How much and why? Acta Physiologica Scandinavica, 136(4), 561–568. http://doi.org/10.1111/j.1748-1716.1989.tb08702.x doi: 10.1111/j.1748-1716.1989.tb08702.x
   PubMedGoogle Scholar
• Louis, M., & Poortmans, J. (2003). No effect of creatine supplementation on human myofibrillar and sarcoplasmic protein synthesis after resistance exercise. American Journal of Physiology. Endocrinology and Metabolism, 285(5), 1089–1094. doi: 10.1152/ajpendo.00195.2003
   PubMed Web of Science ®Google Scholar
• MacDonald, A. J., Small, A. C., Greig, C. A., Husi, H., Ross, J. A., Stephens, N. A., … Preston, T. (2013). A novel oral tracer procedure for measurement of habitual myofibrillar protein synthesis. Rapid Communications in Mass Spectrometry: RCM, 27(15), 1769–1777. http://doi.org/10.1002/rcm.6622 doi: 10.1002/rcm.6622
   PubMed Web of Science ®Google Scholar
• Maden-Wilkinson, T. M., Degens, H., Jones, D. A., & McPhee, J. S. (2013). Comparison of MRI and DXA to measure muscle size and age-related atrophy in thigh muscles. Journal of Musculoskeletal & Neuronal Interactions, 13(3), 320–328.
   PubMed Web of Science ®Google Scholar
• Mayhew, T. P., Rothstein, J. M., Finucane, S. D., & Lamb, R. L. (1995). Muscular adaptation to concentric and eccentric exercise at equal power levels. Medicine and Science in Sports and Exercise, 27(6), 868–873. doi: 10.1249/00005768-199506000-00011
   PubMed Web of Science ®Google Scholar
• Mccall, G. E., Byrnes, W. C., Dickinson, A., Pattany, P. M., Fleck, S. J., Mula, J., … Zentner, A. (1996). Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training 2004–2012.
   Google Scholar
• Metter, E. J., Talbot, L. a., Schrager, M., & Conwit, R. (2002). Skeletal muscle strength as a predictor of all-cause mortality in healthy men. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 57(10), B359–B365. doi: 10.1093/gerona/57.10.B359
   PubMed Web of Science ®Google Scholar
• Miller, B. F., Olesen, J. L., Hansen, M., Døssing, S., Crameri, R. M., Welling, R. J., … Rennie, M. J. (2005). Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. The Journal of Physiology, 567(Pt 3), 1021–1033. http://doi.org/10.1113/jphysiol.2005.093690 doi: 10.1113/jphysiol.2005.093690
   PubMed Web of Science ®Google Scholar
• Miller, B. F., Robinson, M. M., Bruss, M. D., Hellerstein, M., & Hamilton, K. L. (2012). A comprehensive assessment of mitochondrial protein synthesis and cellular proliferation with age and caloric restriction. Aging Cell, 11(1), 150–161. http://doi.org/10.1111/j.1474-9726.2011.00769.x doi: 10.1111/j.1474-9726.2011.00769.x
   PubMed Web of Science ®Google Scholar
• Mitchell, C. J., Churchward-Venne, T. a., Parise, G., Bellamy, L., Baker, S. K., Smith, K., … Phillips, S. M. (2014). Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PloS One, 9(2), e89431. http://doi.org/10.1371/journal.pone.0089431 doi: 10.1371/journal.pone.0089431
   PubMed Web of Science ®Google Scholar
• Mitsiopoulos, N., Baumgartner, R. N., Heymsfield, S. B., Lyons, W., Gallagher, D., & Ross, R. (1998). Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. Journal of Applied Physiology (Bethesda, Md. : 1985), 85(1), 115–122.
   PubMed Web of Science ®Google Scholar
• 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(1), 161–168. http://doi.org/10.3945/ajcn.2008.26401 doi: 10.3945/ajcn.2008.26401
   PubMed Web of Science ®Google Scholar
• Moore, D. R., Tang, J. E., Burd, N. a., Rerecich, T., Tarnopolsky, M. a., & Phillips, S. M. (2009). Differential stimulation of myofibrillar and sarcoplasmic protein synthesis with protein ingestion at rest and after resistance exercise. The Journal of Physiology, 587(Pt 4), 897–904. http://doi.org/10.1113/jphysiol.2008.164087 doi: 10.1113/jphysiol.2008.164087
   PubMed Web of Science ®Google Scholar
• Moritani, T., & DeVries, H. A. (1979). Neural factors versus hypertrophy in the time course of muscle strength gain. American Journal of Physical Medicine, 58(3), 115–130.
   PubMedGoogle Scholar
• Murton, a. J., Billeter, R., Stephens, F. B., Des Etages, S. G., Graber, F., Hill, R. J., … Greenhaff, P. L. (2014). Transient transcriptional events in human skeletal muscle at the outset of concentric resistance exercise training. Journal of Applied Physiology (Bethesda, Md. : 1985), 116(1), 113–125. http://doi.org/10.1152/japplphysiol.00426.2013
   PubMed Web of Science ®Google Scholar
• Narici, M. V., Hoppeler, H., Kayser, B., Landoni, L., Claassen, H., Gavardi, C., … Cerretelli, P. (1996). Human quadriceps cross-sectional area, torque and neural activation during 6 months strength training. Acta Physiologica Scandinavica, 157(2), 175–186. http://doi.org/10.1046/j.1365-201X.1996.483230000.x doi: 10.1046/j.1365-201X.1996.483230000.x
   PubMedGoogle Scholar
• Narici, M. V., & Kayser, B. (1995). Hypertrophic response of human skeletal muscle to strength training in hypoxia and normoxia. European Journal of Applied Physiology and Occupational Physiology, 70(3), 213–219. doi: 10.1007/BF00238566
   PubMed Web of Science ®Google Scholar
• Neese, R. a., Misell, L. M., Turner, S., Chu, a., Kim, J., Cesar, D., … Hellerstein, M. K. (2002). Nonlinear partial differential equations and applications: Measurement in vivo of proliferation rates of slow turnover cells by 2H2O labeling of the deoxyribose moiety of DNA. Proceedings of the National Academy of Sciences of the United States of America, 99(24), 15345–15350. http://doi.org/10.1073/pnas.232551499 doi: 10.1073/pnas.232551499
   PubMed Web of Science ®Google Scholar
• Nindl, B. C., Harman, E. A., Marx, J. O., Gotshalk, L. A., Frykman, P. N., Lammi, E., … Kraemer, W. J. (2000). Regional body composition changes in women after 6 months of periodized physical training. Journal of Applied Physiology (Bethesda, Md. : 1985), 88(6), 2251–2259.
   PubMed Web of Science ®Google Scholar
• Norrbrand, L., Pozzo, M., & Tesch, P. a. (2010). Flywheel resistance training calls for greater eccentric muscle activation than weight training. European Journal of Applied Physiology, 110(5), 997–1005. http://doi.org/10.1007/s00421-010-1575-7 doi: 10.1007/s00421-010-1575-7
   PubMed Web of Science ®Google Scholar
• Ogasawara, R., Yasuda, T., Ishii, N., & Abe, T. (2013). Comparison of muscle hypertrophy following 6-month of continuous and periodic strength training. European Journal of Applied Physiology, 113(4), 975–985. http://doi.org/10.1007/s00421-012-2511-9 doi: 10.1007/s00421-012-2511-9
   PubMed Web of Science ®Google Scholar
• Olsen, S., Aagaard, P., Kadi, F., Tufekovic, G., Verney, J., Olesen, J. L., … Kjaer, M. (2006). Creatine supplementation augments the increase in satellite cell and myonuclei number in human skeletal muscle induced by strength training. The Journal of Physiology, 573(Pt 2), 525–534. http://doi.org/10.1113/jphysiol.2006.107359 doi: 10.1113/jphysiol.2006.107359
   PubMed Web of Science ®Google Scholar
• Owen, O. E., Smalley, K. J., D'Alessio, D. A., Mozzoli, M. A., & Dawson, E. K. (1998). Protein, fat, and carbohydrate requirements during starvation: Anaplerosis and cataplerosis. The American Journal of Clinical Nutrition, 68(1), 12–34.
   PubMed Web of Science ®Google Scholar
• Pedersen, B. K. (2013). Muscle as a secretory organ. Comprehensive Physiology, 3(3), 1337–1362. http://doi.org/10.1002/cphy.c120033
   PubMed Web of Science ®Google Scholar
• Pennings, B., Koopman, R., Beelen, M., Senden, J. M. G., Saris, W. H. M., & van Loon, L. J. C. (2011). Exercising before protein intake allows for greater use of dietary protein-derived amino acids for de novo muscle protein synthesis in both young and elderly men. The American Journal of Clinical Nutrition, 93(2), 322–331. http://doi.org/10.3945/ajcn.2010.29649 doi: 10.3945/ajcn.2010.29649
   PubMed Web of Science ®Google Scholar
• Phillips, B. E., Williams, J. P., Gustafsson, T., Bouchard, C., Rankinen, T., Knudsen, S., … Atherton, P. J. (2013). Molecular networks of human muscle adaptation to exercise and age. PLoS Genetics, 9(3), e1003389. http://doi.org/10.1371/journal.pgen.1003389 doi: 10.1371/journal.pgen.1003389
   PubMed Web of Science ®Google Scholar
• Phillips, S. M., Glover, E. I., & Rennie, M. J. (2009). Alterations of protein turnover underlying disuse atrophy in human skeletal muscle. Journal of Applied Physiology (Bethesda, Md. : 1985), 107(3), 645–654. http://doi.org/10.1152/japplphysiol.00452.2009
   PubMed Web of Science ®Google Scholar
• Phillips, S. M., Parise, G., Roy, B. D., Tipton, K. D., Wolfe, R. R., & Tamopolsky, M. A. (2002). Resistance-training-induced adaptations in skeletal muscle protein turnover in the fed state. Canadian Journal of Physiology and Pharmacology, 80(11), 1045–1053. doi: 10.1139/y02-134
   PubMed Web of Science ®Google Scholar
• Phillips, S. M., Tipton, K. D., Aarsland, A., Wolf, S. E., Wolfe, R. R., & Wolf, E. (1997). Mixed muscle protein synthesis and breakdown after resistance exercise in humans. The American Journal of Physiology, 273(1 Pt 1), E99–107.
   PubMed Web of Science ®Google Scholar
• Phillips, S. M., Tipton, K. D., Ferrando, a. a., & Wolfe, R. R. (1999). Resistance training reduces the acute exercise-induced increase in muscle protein turnover. The American Journal of Physiology, 276(1 Pt 1), E118–E124.
   PubMedGoogle Scholar
• Pozefsky, T., Tancredi, R. G., Moxley, R. T., Dupre, J., & Tobin, J. D. (1976). Effects of brief starvation on muscle amino acid metabolism in nonobese man. The Journal of Clinical Investigation, 57(2), 444–449. http://doi.org/10.1172/JCI108295 doi: 10.1172/JCI108295
   PubMed Web of Science ®Google Scholar
• Previs, S. F., Fatica, R., Chandramouli, V., Alexander, J. C., Brunengraber, H., & Landau, B. R. (2004). Quantifying rates of protein synthesis in humans by use of 2H2O: Application to patients with end-stage renal disease. American Journal of Physiology. Endocrinology and Metabolism, 286(4), E665–E672. http://doi.org/10.1152/ajpendo.00271.2003 doi: 10.1152/ajpendo.00271.2003
   PubMed Web of Science ®Google Scholar
• Proud, C. G. (2009). mTORC1 signalling and mRNA translation. Biochemical Society Transactions, 37(Pt 1), 227–231. http://doi.org/10.1042/BST0370227 doi: 10.1042/BST0370227
   PubMed Web of Science ®Google Scholar
• Rand, W. M., Pellett, P. L., & Young, V. R. (2003). Meta-analysis of nitrogen balance studies for estimating protein requirements in healthy adults. The American Journal of Clinical Nutrition, 77(1), 109–127.
   PubMed Web of Science ®Google Scholar
• Rennie, M. J., Edwards, R. H., Halliday, D., Matthews, D. E., Wolman, S. L., & Millward, D. J. (1982). Muscle protein synthesis measured by stable isotope techniques in man: The effects of feeding and fasting. Clinical Science (London, England : 1979), 63(6), 519–523. doi: 10.1042/cs0630519
   PubMed Web of Science ®Google Scholar
• Rennie, M. J., Wackerhage, H., Spangenburg, E. E., & Booth, F. W. (2004). Control of the size of the human muscle mass. Annual Review of Physiology, 66(9), 799–828. http://doi.org/10.1146/annurev.physiol.66.052102.134444 doi: 10.1146/annurev.physiol.66.052102.134444
   PubMed Web of Science ®Google Scholar
• Robinson, M. M., Turner, S. M., Hellerstein, M. K., Hamilton, K. L., & Miller, B. F. (2011). Long-term synthesis rates of skeletal muscle DNA and protein are higher during aerobic training in older humans than in sedentary young subjects but are not altered by protein supplementation. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 25(9), 3240–3249. http://doi.org/10.1096/fj.11-186437 doi: 10.1096/fj.11-186437
   PubMed Web of Science ®Google Scholar
• Sancak, Y., Bar-peled, L., Zoncu, R., Markhard, A. L., Nada, S., & Sabatini, D. M. (2011). NIH Public Access, 141(2), 290–303. http://doi.org/10.1016/j.cell.2010.02.024.Ragulator-Rag
   Google Scholar
• Sancak, Y., Peterson, T. R., Shaul, Y. D., Lindquist, R. A., Thoreen, C. C., Bar-peled, L., & Sabatini, D. M. (2008). NIH Public Access, 320(5882), 1496–1501. http://doi.org/10.1126/science.1157535.The
   Google Scholar
• Scalzo, R. L., Peltonen, G. L., Binns, S. E., Shankaran, M., Giordano, G. R., Hartley, D. a., … Miller, B. F. (2014). Greater muscle protein synthesis and mitochondrial biogenesis in males compared with females during sprint interval training. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 28(6), 2705–2714. http://doi.org/10.1096/fj.13-246595 doi: 10.1096/fj.13-246595
   PubMed Web of Science ®Google Scholar
• Schoenheimer, R., & Rittenberg, D. (1936). Deuterium as an indicator in the study of intermediary metabolism VI. Synthesis and destruction of fatty acids in the organism. Journal of Biological Chemistry, 114, 381–396.
   Google Scholar
• Seynnes, O. R., de Boer, M., & Narici, M. V. (2007). Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. Journal of Applied Physiology (Bethesda, Md. : 1985), 102(1), 368–373. http://doi.org/10.1152/japplphysiol.00789.2006
   PubMed Web of Science ®Google Scholar
• Sheffield-Moore, M., Yeckel, C. W., Volpi, E., Wolf, S. E., Morio, B., Chinkes, D. L., … Wolfe, R. R. (2004). Postexercise protein metabolism in older and younger men following moderate-intensity aerobic exercise. American Journal of Physiology. Endocrinology and Metabolism, 287(3), E513–E522. http://doi.org/10.1152/ajpendo.00334.2003 doi: 10.1152/ajpendo.00334.2003
   PubMed Web of Science ®Google Scholar
• Shulman, G. I., Rothman, D. L., Jue, T., Stein, P., DeFronzo, R. A., & Shulman, R. G. (1990). Quantitation of muscle glycogen synthesis in normal subjects and subjects with non-insulin-dependent diabetes by 13C nuclear magnetic resonance spectroscopy. The New England Journal of Medicine, 322(4), 223–228. http://doi.org/10.1056/NEJM199001253220403 doi: 10.1056/NEJM199001253220403
   PubMed Web of Science ®Google Scholar
• Smith, K., Reynolds, N., Downie, S., Patel, A., & Rennie, M. J. (1998). Effects of flooding amino acids on incorporation of labeled amino acids into human muscle protein. American Journal of Physiology, 275, 73–78.
   PubMedGoogle Scholar
• Staples, A. W., Burd, N. a., West, D. W. D., Currie, K. D., Atherton, P. J., Moore, D. R., … Phillips, S. M. (2011). Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Medicine and Science in Sports and Exercise, 43(7), 1154–1161. http://doi.org/10.1249/MSS.0b013e31820751cb doi: 10.1249/MSS.0b013e31820751cb
   PubMed Web of Science ®Google Scholar
• Staron, R. S., Karapondo, D. L., Kraemer, W. J., Fry, A. C., Gordon, S. E., Falkel, J. E., … Hikida, R. S. (1994). Skeletal muscle adaptations during early phase of heavy-resistance training in men and women. Journal of Applied Physiology (Bethesda, Md. : 1985), 76(3), 1247–1255.
   PubMed Web of Science ®Google Scholar
• Tang, J. E., Perco, J. G., Moore, D. R., Wilkinson, S. B., & Phillips, S. M. (2008). Resistance training alters the response of fed state mixed muscle protein synthesis in young men. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 294(1), R172–R178. http://doi.org/10.1152/ajpregu.00636.2007 doi: 10.1152/ajpregu.00636.2007
   PubMed Web of Science ®Google Scholar
• Tesch, P. A., Ekberg, A., Lindquist, D. M., & Trieschmann, J. T. (2004). Muscle hypertrophy following 5-week resistance training using a non-gravity-dependent exercise system. Acta Physiologica Scandinavica, 180(1), 89–98. http://doi.org/10.1046/j.0001-6772.2003.01225.x doi: 10.1046/j.0001-6772.2003.01225.x
   PubMedGoogle Scholar
• Viitasalo, J. T., Saukkonen, S., & Komi, P. V. (1980). Reproducibility of measurements of selected neuromuscular performance variables in man. Electromyography and Clinical Neurophysiology, 20(6), 487–501.
   PubMedGoogle Scholar
• Volek, J. S., Volk, B. M., Gómez, A. L., Kunces, L. J., Kupchak, B. R., Freidenreich, D. J., … Kraemer, W. J. (2013). Whey protein supplementation during resistance training augments lean body mass. Journal of the American College of Nutrition, 32(2), 122–135. http://doi.org/10.1080/07315724.2013.793580 doi: 10.1080/07315724.2013.793580
   PubMed Web of Science ®Google Scholar
• Wernbom, M., Augustsson, J., & Thomeé, R. (2007). The influence of frequency, intensity, volume and mode of strength training on whole muscle cross-sectional area in humans. Sports Medicine (Auckland, N.Z.), 37(3), 225–264. doi: 10.2165/00007256-200737030-00004
   PubMed Web of Science ®Google Scholar
• 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. American Journal of Clinical Nutrition, 94, 795–803. doi: 10.3945/ajcn.111.013722
   PubMed Web of Science ®Google Scholar
• West, D. W. D., Kujbida, G. W., Moore, D. R., Atherton, P., Burd, N. a., Padzik, J. P., … Phillips, S. M. (2009). Resistance exercise-induced increases in putative anabolic hormones do not enhance muscle protein synthesis or intracellular signalling in young men. The Journal of Physiology, 587(Pt 21), 5239–5247. http://doi.org/10.1113/jphysiol.2009.177220 doi: 10.1113/jphysiol.2009.177220
   PubMed Web of Science ®Google Scholar
• Wilkinson, D. J., Franchi, M. V., Brook, M. S., Narici, M. V., Williams, J. P., Mitchell, W. K., … Smith, K. (2014). A validation of the application of D(2)O stable isotope tracer techniques for monitoring day-to-day changes in muscle protein subfraction synthesis in humans. American Journal of Physiology. Endocrinology and Metabolism, 306(5), E571–E579. http://doi.org/10.1152/ajpendo.00650.2013 doi: 10.1152/ajpendo.00650.2013
   PubMed Web of Science ®Google Scholar
• Wilkinson, D. J., Hossain, T., Hill, D. S., Phillips, B. E., Crossland, H., Williams, J., … Atherton, P. J. (2013). Effects of leucine and its metabolite β-hydroxy-β-methylbutyrate on human skeletal muscle protein metabolism. The Journal of Physiology, 591(Pt 11), 2911–2923. http://doi.org/10.1113/jphysiol.2013.253203 doi: 10.1113/jphysiol.2013.253203
   PubMed Web of Science ®Google Scholar
• Wilkinson, S. B., Phillips, S. M., Atherton, P. J., Patel, R., Yarasheski, K. E., Tarnopolsky, M. a., & Rennie, M. J. (2008). Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. The Journal of Physiology, 586(Pt 15), 3701–3717. http://doi.org/10.1113/jphysiol.2008.153916 doi: 10.1113/jphysiol.2008.153916
   PubMed Web of Science ®Google Scholar
• Williams, J. P., Phillips, B. E., Smith, K., Atherton, P. J., Rankin, D., Selby, A. L., … Rennie, M. J. (2012). Effect of tumor burden and subsequent surgical resection on skeletal muscle mass and protein turnover in colorectal cancer patients. The American Journal of Clinical Nutrition, 96(5), 1064–1070. http://doi.org/10.3945/ajcn.112.045708 doi: 10.3945/ajcn.112.045708
   PubMed Web of Science ®Google Scholar
• Willoughby, D., & Taylor, L. (2004). Effects of sequential bouts of resistance exercise on androgen receptor expression. Medicine and Science in Sports and Excercise, 36(9), 1499–1506. http://doi.org/10.1249/01.MSS.0000139795.83030.DI doi: 10.1249/01.MSS.0000139795.83030.D1
   PubMed Web of Science ®Google Scholar
• 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(1), 86–95. http://doi.org/10.3945/ajcn.112.055517 doi: 10.3945/ajcn.112.055517
   PubMed Web of Science ®Google Scholar
• Woolstenhulme, M. T., Conlee, R. K., Drummond, M. J., Stites, A. W., & Parcell, A. C. (2006). Temporal response of desmin and dystrophin proteins to progressive resistance exercise in human skeletal muscle. Journal of Applied Physiology (Bethesda, Md. : 1985), 100(6), 1876–1882. http://doi.org/10.1152/japplphysiol.01592.2005
   PubMed Web of Science ®Google Scholar
• Yang, R. D., Matthews, D. E., Bier, D. M., Lo, C., & Young, V. R. (1984). Alanine kinetics in humans: Influence of different isotopic tracers Alanine kinetics in humans: Influence of different isotopic tracers.
   Google Scholar
• Zhang, X., Chinkes, D. L., Wolfe, R. R., & Robert, R. (2002). Breakdown rates from a pulse tracer injection, 753–764.
   Google Scholar
• Zurlo, F., Larson, K., Bogardus, C., & Ravussin, E. (1990). Skeletal muscle metabolism is a major determinant of resting energy expenditure. The Journal of Clinical Investigation, 86(5), 1423–1427. http://doi.org/10.1172/JCI114857 doi: 10.1172/JCI114857
   PubMed Web of Science ®Google Scholar