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Protein Availability and Satellite Cell Dynamics in Skeletal Muscle

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Abstract

Human skeletal muscle satellite cells are activated in response to both resistance and endurance exercise. It was initially proposed that satellite cell proliferation and differentiation were only required to support resistance exercise-induced hypertrophy. However, satellite cells may also play a role in muscle fibre remodelling after endurance-based exercise and extracellular matrix regulation. Given the importance of dietary protein, particularly branched chain amino acids, in supporting myofibrillar and mitochondrial adaptations to both resistance and endurance-based training, a greater understanding of how protein intake impacts satellite cell activity would provide further insight into the mechanisms governing skeletal muscle remodelling with exercise. While many studies have investigated the capacity for protein ingestion to increase post-exercise rates of muscle protein synthesis, few investigations have examined the role for protein ingestion to modulate satellite cell activity. Here we review the molecular mechanisms controlling the activation of satellite cells in response to mechanical stress and protein intake in both in vitro and in vivo models. We provide a mechanistic framework that describes how protein ingestion may enhance satellite activity and promote exercise adaptations in human skeletal muscle.

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References

  1. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961;9:493–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Crameri RM, Langberg H, Magnusson P, Jensen CH, Schrøder HD, Olesen JL, et al. Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol. 2004;558:333–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Dreyer HC, Blanco CE, Sattler FR, Schroeder ET, Wiswell RA. Satellite cell numbers in young and older men 24 hours after eccentric exercise. Muscle Nerve. 2006;33:242–53.

    Article  PubMed  Google Scholar 

  4. Babcock L, Escano M, D’Lugos A, Todd K, Murach K, Luden N. Concurrent aerobic exercise interferes with the satellite cell response to acute resistance exercise. AJP Regul Integr Comp Physiol. 2012;302:R1458–65.

    Article  CAS  Google Scholar 

  5. Joanisse S, Gillen JB, Bellamy LM, McKay BR, Tarnopolsky MA, Gibala MJ, et al. Evidence for the contribution of muscle stem cells to nonhypertrophic skeletal muscle remodeling in humans. FASEB J. 2013;27:4596–605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Farup J, Rahbek SK, Knudsen IS, de Paoli F, Mackey AL, Vissing K. Whey protein supplementation accelerates satellite cell proliferation during recovery from eccentric exercise. Amino Acids. 2014;46:2503–16.

    Article  CAS  PubMed  Google Scholar 

  7. Snijders T, Verdijk LB, McKay BR, Smeets JSJ, van Kranenburg J, Groen BBB, et al. Acute dietary protein intake restriction is associated with changes in myostatin expression after a single bout of resistance exercise in healthy young men. J Nutr. 2014;144:137–45.

    Article  CAS  PubMed  Google Scholar 

  8. Blaauw B, Reggiani C. The role of satellite cells in muscle hypertrophy. J Muscle Res Cell Motil. 2014;35:3–10.

    Article  CAS  PubMed  Google Scholar 

  9. McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, et al. Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development. 2011;138:3657–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Egner IM, Bruusgaard JC, Gundersen K. Satellite cell depletion prevents fiber hypertrophy in skeletal muscle. Development. 2016;143:2898–906.

    Article  CAS  PubMed  Google Scholar 

  11. Fry CS, Lee JD, Jackson JR, Kirby TJ, Stasko SA, Liu H, et al. Regulation of the muscle fiber microenvironment by activated satellite cells during hypertrophy. FASEB J. 2014;28:1654–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Petrella JK, Kim J, Cross JM, Kosek DJ, Bamman MM. Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women. Am J Physiol Endocrinol Metab. 2006;291:E937–46.

    Article  CAS  PubMed  Google Scholar 

  13. Petrella JK, Kim J, Mayhew DL, Cross JM, Bamman MM. Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol. 2008;104:1736–42.

    Article  PubMed  Google Scholar 

  14. Verdijk LB, Gleeson BG, Jonkers RAM, Meijer K, Savelberg HHCM, Dendale P, et al. Skeletal muscle hypertrophy following resistance training is accompanied by a fiber type-specific increase in satellite cell content in elderly men. J Gerontol A Biol Sci Med Sci. 2009;64A:332–9.

    Article  CAS  PubMed Central  Google Scholar 

  15. Verdijk LB, Snijders T, Drost M, Delhaas T, Kadi F, van Loon LJC. Satellite cells in human skeletal muscle; from birth to old age. Age. 2014;36:545–57.

    Article  CAS  PubMed  Google Scholar 

  16. Bellamy LM, Joanisse S, Grubb A, Mitchell CJ, McKay BR, Phillips SM, et al. The acute satellite cell response and skeletal muscle hypertrophy following resistance training. PLoS One. 2014;9:e109739 (Asakura A, editor).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Dirks ML, Tieland M, Verdijk LB, Losen M, Nilwik R, Mensink M, et al. Protein supplementation augments muscle fiber hypertrophy but does not modulate satellite cell content during prolonged resistance-type exercise training in frail elderly. J Am Med Dir Assoc. 2017;18:608–15.

    Article  PubMed  Google Scholar 

  18. Reidy PT, Fry CS, Igbinigie S, Deer RR, Jennings K, Cope MB, et al. Protein supplementation does not affect myogenic adaptations to resistance training. Med Sci Sports Exerc. 2017; 49:1197–208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. McCarthy JJ, Dupont-Versteegden EE, Fry CS, Murach KA, Peterson CA. Methodological issues limit interpretation of negative effects of satellite cell depletion on adult muscle hypertrophy. Development. 2017;144:1363–5.

    Article  CAS  PubMed  Google Scholar 

  20. Karlsen A, Couppé C, Andersen JL, Mikkelsen UR, Nielsen RH, Magnusson SP, et al. Matters of fiber size and myonuclear domain: does size matter more than age? Muscle Nerve. 2015;52:1040–6.

    Article  CAS  PubMed  Google Scholar 

  21. Murach KA, White SH, Wen Y, Ho A, Dupont-Versteegden EE, McCarthy JJ, et al. Differential requirement for satellite cells during overload-induced muscle hypertrophy in growing versus mature mice. Skelet Muscle. 2017;7:14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Nederveen JP, Joanisse S, Snijders T, Ivankovic V, Baker SK, Phillips SM, et al. Skeletal muscle satellite cells are located at a closer proximity to capillaries in healthy young compared with older men. J Cachexia Sarcopenia Muscle. 2016;7:547–54.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Nederveen JP, Snijders T, Joanisse S, Wavell CG, Mitchell CJ, Johnston LM, et al. Altered muscle satellite cell activation following 16 wk of resistance training in young men. Am J Physiol Regul Integr Comp Physiol. 2017;312:R85–92.

    Article  PubMed  Google Scholar 

  24. McKay BR, O’Reilly CE, Phillips SM, Tarnopolsky MA, Parise G. Co-expression of IGF-1 family members with myogenic regulatory factors following acute damaging muscle-lengthening contractions in humans. J Physiol. 2008;586:5549–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. McKay BR, De Lisio M, Johnston APW, O’Reilly CE, Phillips SM, Tarnopolsky MA, et al. Association of interleukin-6 signalling with the muscle stem cell response following muscle-lengthening contractions in humans. PLoS One. 2009;4:e6027.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 2005;433:760–4.

    Article  CAS  PubMed  Google Scholar 

  27. Merritt EK, Stec MJ, Thalacker-Mercer A, Windham ST, Cross JM, Shelley DP, et al. Heightened muscle inflammation susceptibility may impair regenerative capacity in aging humans. J Appl Physiol. 2013;115:937–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Corrick KL, Stec MJ, Merritt EK, Windham ST, Thomas SJ, Cross JM, et al. Serum from human burn victims impairs myogenesis and protein synthesis in primary myoblasts. Front Physiol. 2015;6:184.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Rodgers JT, Schroeder MD, Ma C, Rando TA. HGFA is an injury-regulated systemic factor that induces the transition of stem cells into G alert. Cell Rep. 2017;19:479–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Cermak NM, Res PT, de Groot LC, Saris WH, van Loon LJ. Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr. 2012;96:1454–64.

    Article  CAS  PubMed  Google Scholar 

  31. Morton RW, Murphy KT, McKellar SR, Schoenfeld BJ, Henselmans M, Helms E, et al. A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults. Br J Sports Med. 2018;52:376–84.

    PubMed  Google Scholar 

  32. Averous J, Gabillard JC, Seiliez I, Dardevet D. Leucine limitation regulates myf5 and myoD expression and inhibits myoblast differentiation. Exp Cell Res. 2012;318:217–27.

    Article  CAS  PubMed  Google Scholar 

  33. Dai J-M, Yu M-X, Shen Z-Y, Guo C-Y, Zhuang S-Q, Qiu X-S. Leucine promotes proliferation and differentiation of primary preterm rat satellite cells in part through mTORC1 signaling pathway. Nutrients. 2015;7:3387–400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chen X, Huang Z, Chen D, Yang T, Liu G. MicroRNA-27a is induced by leucine and contributes to leucine-induced proliferation promotion in C2C12 cells. Int J Mol Sci. 2013;14:14076–84.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Duan Y, Zeng L, Li F, Wang W, Li Y, Guo Q, et al. Effect of branched-chain amino acid ratio on the proliferation, differentiation, and expression levels of key regulators involved in protein metabolism of myocytes. Nutrition. 2017;36:8–16.

    Article  CAS  PubMed  Google Scholar 

  36. Coffey VG, Hawley JA. Concurrent exercise training: do opposites distract? J Physiol. 2017;595:2883–96.

    Article  CAS  PubMed  Google Scholar 

  37. Hawley JA, Hargreaves M, Joyner MJ, Zierath JR. Integrative biology of exercise. Cell. 2014;159:738–49.

    Article  CAS  PubMed  Google Scholar 

  38. Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol. 1984;56:831–8.

    Article  CAS  PubMed  Google Scholar 

  39. Hawley JA. Adaptations of skeletal muscle to prolonged, intense endurance training. Clin Exp Pharmacol Physiol. 2002;29:218–22.

    Article  CAS  PubMed  Google Scholar 

  40. Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA, et al. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle: Protein synthesis, resistance and endurance exercise. J Physiol. 2008;586:3701–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. McDonagh MJN, Davies CTM. Adaptive response of mammalian skeletal muscle to exercise with high loads. Eur J Appl Physiol. 1984;52:139–55.

    Article  CAS  Google Scholar 

  42. Cheek DB. The control of cell mass and replication. The DNA unit—a personal 20-year study. Early Hum Dev. 1985;12:211–39.

    Article  CAS  PubMed  Google Scholar 

  43. Kadi F, Schjerling P, Andersen LL, Charifi N, Madsen JL, Christensen LR, et al. The effects of heavy resistance training and detraining on satellite cells in human skeletal muscles. J Physiol. 2004;558:1005–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Snijders T, Smeets JSJ, van Kranenburg J, Kies AK, van Loon LJC, Verdijk LB. Changes in myonuclear domain size do not precede muscle hypertrophy during prolonged resistance-type exercise training. Acta Physiol. 2016;216:231–9.

    Article  CAS  Google Scholar 

  45. Fry CS, Noehren B, Mula J, Ubele MF, Westgate PM, Kern PA, et al. Fibre type-specific satellite cell response to aerobic training in sedentary adults. J Physiol. 2014;592:2625–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Mackey AL, Holm L, Reitelseder S, Pedersen TG, Doessing S, Kadi F, et al. Myogenic response of human skeletal muscle to 12 weeks of resistance training at light loading intensity: Increased CD56+ cells with low muscle loading. Scand J Med Sci Sports. 2011;21:773–82.

    Article  CAS  PubMed  Google Scholar 

  47. Snijders T, Verdijk LB, Beelen M, McKay BR, Parise G, Kadi F, et al. A single bout of exercise activates skeletal muscle satellite cells during subsequent overnight recovery: satellite cell activation following exercise. Exp Physiol. 2012;97:762–73.

    Article  CAS  PubMed  Google Scholar 

  48. Snijders T, Verdijk LB, Smeets JSJ, McKay BR, Senden JMG, Hartgens F, et al. The skeletal muscle satellite cell response to a single bout of resistance-type exercise is delayed with aging in men. Age (Dordrecht, Netherlands). 2014;36:9699.

    Article  PubMed Central  Google Scholar 

  49. Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HHCM, van Loon LJC. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab. 2007;292:E151–7.

    Article  CAS  PubMed  Google Scholar 

  50. Olsen S, Aagaard P, Kadi F, Tufekovic G, Verney J, Olesen JL, et al. Creatine supplementation augments the increase in satellite cell and myonuclei number in human skeletal muscle induced by strength training. J Physiol. 2006;573:525–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Snijders T, Nederveen JP, McKay BR, Joanisse S, Verdijk LB, van Loon LJC, et al. Satellite cells in human skeletal muscle plasticity. Front Physiol. 2015;6:283.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Rodgers JT, King KY, Brett JO, Cromie MJ, Charville GW, Maguire KK, et al. mTORC1 controls the adaptive transition of quiescent stem cells from G0 to GAlert. Nature. 2014;510:393–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Charville GW, Cheung TH, Yoo B, Santos PJ, Lee GK, Shrager JB, et al. Ex vivo expansion and in vivo self-renewal of human muscle stem cells. Stem Cell Rep. 2015;5:621–32.

    Article  CAS  Google Scholar 

  54. Verdijk LB, Snijders T, Beelen M, Savelberg HHCM, Meijer K, Kuipers H, et al. Characteristics of muscle fiber type are predictive of skeletal muscle mass and strength in elderly men. J Am Geriatr Soc. 2010;58:2069–75.

    Article  PubMed  Google Scholar 

  55. Mackey AL, Kjaer M, Charifi N, Henriksson J, Bojsen-Moller J, Holm L, et al. Assessment of satellite cell number and activity status in human skeletal muscle biopsies. Muscle Nerve. 2009;40:455–65.

    Article  PubMed  Google Scholar 

  56. Charifi N, Kadi F, Féasson L, Denis C. Effects of endurance training on satellite cell frequency in skeletal muscle of old men. Muscle Nerve. 2003;28:87–92.

    Article  PubMed  Google Scholar 

  57. Joanisse S, McKay BR, Nederveen JP, Scribbans TD, Gurd BJ, Gillen JB, et al. Satellite cell activity, without expansion, after nonhypertrophic stimuli. Am J Physiol Regul Integr Comp Physiol. 2015;309:R1101–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Snijders T, Verdijk LB, Hansen D, Dendale P, van Loon LJC. Continuous endurance-type exercise training does not modulate satellite cell content in obese type 2 diabetes patients. Muscle Nerve. 2011;43:393–401.

    Article  PubMed  Google Scholar 

  59. Verney J, Kadi F, Charifi N, Féasson L, Saafi MA, Castells J, et al. Effects of combined lower body endurance and upper body resistance training on the satellite cell pool in elderly subjects. Muscle Nerve. 2008;38:1147–54.

    Article  PubMed  Google Scholar 

  60. McKenzie AI, D’Lugos AC, Saunders MJ, Gworek KD, Luden ND. Fiber type-specific satellite cell content in cyclists following heavy training with carbohydrate and carbohydrate-protein supplementation. Front Physiol. 2016;7:550.

    Article  PubMed  PubMed Central  Google Scholar 

  61. McLoon LK, Rowe J, Wirtschafter J, McCormick KM. Continuous myofiber remodeling in uninjured extraocular myofibers: myonuclear turnover and evidence for apoptosis. Muscle Nerve. 2004;29:707–15.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Fry CS, Kirby TJ, Kosmac K, McCarthy JJ, Peterson CA. Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy. Cell Stem Cell. 2017;20:56–69.

    Article  CAS  PubMed  Google Scholar 

  63. Hood DA. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl Physiol Nutr Metab Physiol Appl Nutr Metab. 2009;34:465–72.

    Article  CAS  Google Scholar 

  64. Gilde AJ, Van Bilsen M. Peroxisome proliferator-activated receptors (PPARS): regulators of gene expression in heart and skeletal muscle. Acta Physiol Scand. 2003;178:425–34.

    Article  CAS  PubMed  Google Scholar 

  65. Dinulovic I, Furrer R, Beer M, Ferry A, Cardel B, Handschin C. Muscle PGC-1α modulates satellite cell number and proliferation by remodeling the stem cell niche. Skelet Muscle. 2016;6:39.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, Harrison BC, et al. A PGC-1α isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell. 2012;151:1319–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kivelä R, Salmela I, Nguyen YH, Petrova TV, Koistinen HA, Wiener Z, et al. The transcription factor Prox1 is essential for satellite cell differentiation and muscle fibre-type regulation. Nat Commun. 2016;7:13124.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. 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. 2009;587:897–904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Breen L, Philp A, Witard OC, Jackman SR, Selby A, Smith K, et al. The influence of carbohydrate–protein co-ingestion following endurance exercise on myofibrillar and mitochondrial protein synthesis. J Physiol. 2011;589:4011–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Camera DM, West DWD, Phillips SM, Rerecich T, Stellingwerff T, Hawley JA, et al. Protein ingestion increases myofibrillar protein synthesis after concurrent exercise. Med Sci Sports Exerc. 2015;47:82–91.

    Article  CAS  PubMed  Google Scholar 

  71. Burd NA, De Lisio M. Skeletal muscle remodeling: interconnections between stem cells and protein turnover. Exerc Sport Sci Rev. 2017;45:187–91.

    Article  PubMed  Google Scholar 

  72. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, et al. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr. 2009;89:161–8.

    Article  CAS  PubMed  Google Scholar 

  73. 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. 2009;107:987–92.

    Article  CAS  PubMed  Google Scholar 

  74. Res PT, Groen B, Pennings B, Beelen M, Wallis GA, Gijsen AP, et al. Protein ingestion before sleep improves postexercise overnight recovery. Med Sci Sports Exerc. 2012;44:1560–9.

    Article  CAS  PubMed  Google Scholar 

  75. Morton RW, McGlory C, Phillips SM. Nutritional interventions to augment resistance training-induced skeletal muscle hypertrophy. Front Physiol. 2015;6:245.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Areta JL, Burke LM, Ross ML, Camera DM, West DWD, Broad EM, et al. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. J Physiol. 2013;591:2319–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Phillips SM, van Loon LJC. Dietary protein for athletes: From requirements to optimum adaptation. J Sports Sci. 2011;29:S29–38.

    Article  PubMed  Google Scholar 

  78. Phillips SM. The impact of protein quality on the promotion of resistance exercise-induced changes in muscle mass. Nutr Metab. 2016;13:64.

    Article  CAS  Google Scholar 

  79. Moore DR, Camera DM, Areta JL, Hawley JA. Beyond muscle hypertrophy: why dietary protein is important for endurance athletes 1. Appl Physiol Nutr Metab. 2014;39:987–97.

    Article  CAS  PubMed  Google Scholar 

  80. Rogulska A, Kurasz S. Regeneration of crushed skeletal muscles in experimental animals and the effect of leucine on the course of this process in white rat. Pol Med Sci Hist Bull. 1975;15:245–8.

    CAS  PubMed  Google Scholar 

  81. Kornasio R, Riederer I, Butler-Browne G, Mouly V, Uni Z, Halevy O. β-hydroxy-β-methylbutyrate (HMB) stimulates myogenic cell proliferation, differentiation and survival via the MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta BBA Mol Cell Res. 2009;1793:755–63.

    Article  CAS  Google Scholar 

  82. Kao M, Columbus DA, Suryawan A, Steinhoff-Wagner J, Hernandez-Garcia A, Nguyen HV, et al. Enteral β-hydroxy-β-methylbutyrate supplementation increases protein synthesis in skeletal muscle of neonatal pigs. Am J Physiol Endocrinol Metab. 2016;310:E1072–84.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Davis TA, Fiorotto ML. Regulation of muscle growth in neonates. Curr Opin Clin Nutr Metab Care. 2009;12:78–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Martin NRW, Turner MC, Farrington R, Player DJ, Lewis MP. Leucine elicits myotube hypertrophy and enhances maximal contractile force in tissue engineered skeletal muscle in vitro. J Cell Physiol. 2017;232:2788–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Alway SE, Pereira SL, Edens NK, Hao Y, Bennett BT. β-Hydroxy-β-methylbutyrate (HMB) enhances the proliferation of satellite cells in fast muscles of aged rats during recovery from disuse atrophy. Exp Gerontol. 2013;48:973–84.

    Article  CAS  PubMed  Google Scholar 

  86. Pereira MG, Silva MT, da Cunha FM, Moriscot AS, Aoki MS, Miyabara EH. Leucine supplementation improves regeneration of skeletal muscles from old rats. Exp Gerontol. 2015;72:269–77.

    Article  CAS  PubMed  Google Scholar 

  87. Jash S, Dhar G, Ghosh U, Adhya S. Role of the mTORC1 complex in satellite cell activation by RNA-induced mitochondrial restoration: dual control of cyclin D1 through MicroRNAs. Mol Cell Biol. 2014;34:3594–606.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Zhang P, Liang X, Shan T, Jiang Q, Deng C, Zheng R, et al. mTOR is necessary for proper satellite cell activity and skeletal muscle regeneration. Biochem Biophys Res Commun. 2015;463:102–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Han B, Tong J, Zhu MJ, Ma C, Du M. Insulin-like growth factor-1 (IGF-1) and leucine activate pig myogenic satellite cells through mammalian target of rapamycin (mTOR) pathway. Mol Reprod Dev. 2008;75:810–7.

    Article  CAS  PubMed  Google Scholar 

  90. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, et al. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science. 2008;320:1496–501.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Hulmi JJ, Kovanen V, Lisko I, Selänne H, Mero AA. The effects of whey protein on myostatin and cell cycle-related gene expression responses to a single heavy resistance exercise bout in trained older men. Eur J Appl Physiol. 2008;102:205–13.

    Article  CAS  PubMed  Google Scholar 

  92. Reidy PT, Fry CS, Dickinson JM, Drummond MJ, Rasmussen BB. Postexercise essential amino acid supplementation amplifies skeletal muscle satellite cell proliferation in older men 24 hours postexercise. Physiol Rep. 2017;5:e13269.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. McKay BR, Toth KG, Tarnopolsky MA, Parise G. Satellite cell number and cell cycle kinetics in response to acute myotrauma in humans: immunohistochemistry versus flow cytometry. J Physiol. 2010;588:3307–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Crameri RM, Aagaard P, Qvortrup K, Langberg H, Olesen J, Kjær M. Myofibre damage in human skeletal muscle: effects of electrical stimulation versus voluntary contraction. J Physiol. 2007;583:365–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Rowlands DS, Nelson AR, Raymond F, Metairon S, Mansourian R, Clarke J, et al. Protein-leucine ingestion activates a regenerative inflammo-myogenic transcriptome in skeletal muscle following intense endurance exercise. Physiol Genom. 2016;48:21–32.

    Article  CAS  Google Scholar 

  96. Roberts MD, Dalbo VJ, Hassell SE, Brown R, Kerksick CM. Effects of preexercise feeding on markers of satellite cell activation. Med Sci Sports Exerc. 2010;42:1861–9.

    Article  CAS  PubMed  Google Scholar 

  97. D’Lugos AC, Luden ND, Faller JM, Akers JD, McKenzie AI, Saunders MJ. Supplemental protein during heavy cycling training and recovery impacts skeletal muscle and heart rate responses but not performance. Nutrients [Internet]. 2016;8. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5037535/.

  98. Lindström M, Thornell L-E. New multiple labelling method for improved satellite cell identification in human muscle: application to a cohort of power-lifters and sedentary men. Histochem Cell Biol. 2009;132:141–57.

    Article  PubMed  CAS  Google Scholar 

  99. Lindström M, Pedrosa-Domellöf F, Thornell L-E. Satellite cell heterogeneity with respect to expression of MyoD, myogenin, Dlk1 and c-Met in human skeletal muscle: application to a cohort of power lifters and sedentary men. Histochem Cell Biol. 2010;134:371–85.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Farup J, Rahbek SK, Riis S, Vendelbo MH, de Paoli F, Vissing K. Influence of exercise contraction mode and protein supplementation on human skeletal muscle satellite cell content and muscle fiber growth. J Appl Physiol. 2014;117:898–909.

  101. Mobley CB, Haun CT, Roberson PA, Mumford PW, Romero MA, Kephart WC, et al. Effects of whey, soy or leucine supplementation with 12 weeks of resistance training on strength, body composition, and skeletal muscle and adipose tissue histological attributes in college-aged males. Nutrients. 2017;9:972.

    Article  PubMed Central  Google Scholar 

  102. Spillane M, Willoughby DS. Daily overfeeding from protein and/or carbohydrate supplementation for eight weeks in conjunction with resistance training does not improve body composition and muscle strength or increase markers indicative of muscle protein synthesis and myogenesis in resistance-trained males. J Sports Sci Med. 2016;15:17.

    PubMed  PubMed Central  Google Scholar 

  103. Reidy PT, Lindsay CC, McKenzie AI, Fry CS, Supiano MA, Marcus RL, et al. Aging-related effects of bed rest followed by eccentric exercise rehabilitation on skeletal muscle macrophages and insulin sensitivity. Exp Gerontol. [Internet]. 2017; Available from: http://www.sciencedirect.com/science/article/pii/S0531556517302632.

  104. Reidy PT, Rasmussen BB. Role of ingested amino acids and protein in the promotion of resistance exercise-induced muscle protein anabolism. J Nutr. 2016;146:155–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Molsted S, Andersen JL, Harrison AP, Eidemak I, Mackey AL. Fiber type-specific response of skeletal muscle satellite cells to high-intensity resistance training in dialysis patients. Muscle Nerve. 2015;52:736–45.

    Article  CAS  PubMed  Google Scholar 

  106. Mackey AL, Karlsen A, Couppé C, Mikkelsen UR, Nielsen RH, Magnusson SP, et al. Differential satellite cell density of type I and II fibres with lifelong endurance running in old men. Acta Physiol. 2014;210:612–27.

    Article  CAS  Google Scholar 

  107. McKay BR, Ogborn DI, Bellamy LM, Tarnopolsky MA, Parise G. Myostatin is associated with age-related human muscle stem cell dysfunction. FASEB J Off Publ Fed Am Soc Exp Biol. 2012;26:2509–21.

    CAS  Google Scholar 

  108. Taylor WE, Bhasin S, Artaza J, Byhower F, Azam M, Willard DH, et al. Myostatin inhibits cell proliferation and protein synthesis in C2C12 muscle cells. Am J Physiol Endocrinol Metab. 2001;280:E221–8.

    Article  CAS  PubMed  Google Scholar 

  109. Welle S, Bhatt K, Pinkert CA. Myofibrillar protein synthesis in myostatin-deficient mice. Am J Physiol Endocrinol Metab. 2006;290:E409–15.

    Article  CAS  PubMed  Google Scholar 

  110. Thalacker-Mercer AE, Fleet JC, Craig BA, Carnell NS, Campbell WW. Inadequate protein intake affects skeletal muscle transcript profiles in older humans. Am J Clin Nutr. 2007;85:1344–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Thalacker-Mercer AE, Fleet JC, Craig BA, Campbell WW. The skeletal muscle transcript profile reflects accommodative responses to inadequate protein intake in younger and older males. J Nutr Biochem. 2010;21:1076–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Damas F, Phillips SM, Libardi CA, Vechin FC, Lixandrão ME, Jannig PR, et al. Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J Physiol. 2016;594:5209–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Pasiakos SM, Lieberman HR, McLellan TM. Effects of protein supplements on muscle damage, soreness and recovery of muscle function and physical performance: a systematic review. Sports Med. 2014;44:655–70.

    Article  PubMed  Google Scholar 

  114. Drummond MJ, Reidy PT, Baird LM, Dalley BK, Howard MT. Leucine differentially regulates gene-specific translation in mouse skeletal muscle. J Nutr. 2017;147:1616–23.

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

D.M.C is supported by an Australian Catholic University Research Funding Grant (#36331).

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Correspondence to Donny M. Camera.

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Baubak Shamim, John A. Hawley and Donny M. Camera declare that they have no conflicts of interest.

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Shamim, B., Hawley, J.A. & Camera, D.M. Protein Availability and Satellite Cell Dynamics in Skeletal Muscle. Sports Med 48, 1329–1343 (2018). https://doi.org/10.1007/s40279-018-0883-7

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  • DOI: https://doi.org/10.1007/s40279-018-0883-7

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