Advertisement

Exercise and the control of muscle mass in human

  • Marc Francaux
  • Louise Deldicque
Invited Review

Abstract

During the course of life, muscle mass undergoes many changes in terms of quantity and quality. Skeletal muscle is a dynamic tissue able to hypertrophy or atrophy according to growth, ageing, physical activity, nutrition and health state. The purpose of the present review is to present the mechanisms by which exercise can induce changes in human skeletal muscle mass by modulating protein balance and regulating the fate of satellite cells. Exercise is known to exert transcriptional, translational and post-translational regulations as well as to induce epigenetic modifications and to control messenger RNA stability, which all contribute to the regulation of protein synthesis. Exercise also regulates the autophagy–lysosomal and the ubiquitin–proteasome pathways, the two main proteolytic systems in skeletal muscle, indicating that exercise participates to the regulation of the quality control mechanisms of cellular components and, therefore, to muscle health. Finally, activation, proliferation and differentiation of satellite cells can be enhanced by exercise to induce muscle remodelling and hypertrophy. Each of these mechanisms can potentially impact skeletal muscle mass, depending on the intensity, duration and frequency with which the signal appears.

Keywords

Protein synthesis Protein degradation Satellite cells miRNA Hypertrophy Resistance exercise 

Notes

Funding information

M.F. was supported by the Sports Ministry of the Brussels-Wallonia Federation. This work was supported by the Fonds Scientifique de la Recherche (FSR) from the Université catholique de Louvain and by the Fonds National de la Recherche Scientifique (FNRS, F.4504.17).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Abreu P, Mendes SV, Ceccatto VM, Hirabara SM (2017) Satellite cell activation induced by aerobic muscle adaptation in response to endurance exercise in humans and rodents. Life Sci 170:33–40.  https://doi.org/10.1016/j.lfs.2016.11.016 CrossRefPubMedGoogle Scholar
  2. 2.
    Adams GR, Bamman MM (2012) Characterization and regulation of mechanical loading-induced compensatory muscle hypertrophy. Compr Physiol 2:2829–2870.  https://doi.org/10.1002/cphy.c110066 CrossRefPubMedGoogle Scholar
  3. 3.
    Ahtiainen JP, Hulmi JJ, Lehti M, Kraemer WJ, Nyman K, Selanne H, Alen M, Komulainen J, Kovanen V, Mero AA, Philippou A, Laakkonen EK, Hakkinen K (2016) Effects of resistance training on expression of IGF-I splice variants in younger and older men. Eur J Sport Sci 16:1055–1063.  https://doi.org/10.1080/17461391.2016.1185164 CrossRefPubMedGoogle Scholar
  4. 4.
    Andersen G, Orngreen MC, Preisler N, Jeppesen TD, Krag TO, Hauerslev S, van Hall G, Vissing J (2015) Protein-carbohydrate supplements improve muscle protein balance in muscular dystrophy patients after endurance exercise: a placebo-controlled crossover study. Am J Physiol Regul Integr Comp Physiol 308:R123–R130.  https://doi.org/10.1152/ajpregu.00321.2014 CrossRefPubMedGoogle Scholar
  5. 5.
    Anderson J, Pilipowicz O (2002) Activation of muscle satellite cells in single-fiber cultures. Nitric Oxide 7:36–41CrossRefGoogle Scholar
  6. 6.
    Aoi W, Naito Y, Mizushima K, Takanami Y, Kawai Y, Ichikawa H, Yoshikawa T (2010) The microRNA miR-696 regulates PGC-1{alpha} in mouse skeletal muscle in response to physical activity. Am J Physiol Endocrinol Metab 298:E799–E806.  https://doi.org/10.1152/ajpendo.00448.2009 CrossRefPubMedGoogle Scholar
  7. 7.
    Aronson D, Boppart MD, Dufresne SD, Fielding RA, Goodyear LJ (1998) Exercise stimulates c-Jun NH2 kinase activity and c-Jun transcriptional activity in human skeletal muscle. Biochem Biophys Res Commun 251:106–110.  https://doi.org/10.1006/bbrc.1998.9435 CrossRefPubMedGoogle Scholar
  8. 8.
    Atherton PJ, Phillips BE, Wilkinson DJ (2015) Exercise and regulation of protein metabolism. Prog Mol Biol Transl Sci 135:75–98.  https://doi.org/10.1016/bs.pmbts.2015.06.015 CrossRefPubMedGoogle Scholar
  9. 9.
    Baar K, Blough E, Dineen B, Esser K (1999) Transcriptional regulation in response to exercise. Exerc Sport Sci Rev 27:333–379CrossRefGoogle Scholar
  10. 10.
    Bamman MM, Roberts BM, Adams GR (2018) Molecular regulation of exercise-induced muscle fiber hypertrophy. Cold Spring Harb Perspect Med 8.  https://doi.org/10.1101/cshperspect.a029751 CrossRefGoogle Scholar
  11. 11.
    Barres R, Yan J, Egan B, Treebak JT, Rasmussen M, Fritz T, Caidahl K, Krook A, O’Gorman DJ, Zierath JR (2012) Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab 15:405–411.  https://doi.org/10.1016/j.cmet.2012.01.001 CrossRefPubMedGoogle Scholar
  12. 12.
    Barth S, Glick D, Macleod KF (2010) Autophagy: assays and artifacts. J Pathol 221:117–124.  https://doi.org/10.1002/path.2694 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Barton ER (2006) Viral expression of insulin-like growth factor-I isoforms promotes different responses in skeletal muscle. J Appl Physiol (1985) 100:1778–1784.  https://doi.org/10.1152/japplphysiol.01405.2005 CrossRefGoogle Scholar
  14. 14.
    Bazgir B, Fathi R, Rezazadeh Valojerdi M, Mozdziak P, Asgari A (2017) Satellite cells contribution to exercise mediated muscle hypertrophy and repair. Cell J 18:473–484PubMedGoogle Scholar
  15. 15.
    Bechet D, Tassa A, Taillandier D, Combaret L, Attaix D (2005) Lysosomal proteolysis in skeletal muscle. Int J Biochem Cell Biol 37:2098–2114.  https://doi.org/10.1016/j.biocel.2005.02.029 CrossRefPubMedGoogle Scholar
  16. 16.
    Berryman N, Mujika I, Bosquet L (2018) Concurrent training for sports performance: the two sides of the medal. Int J Sports Physiol Perform:1–22.  https://doi.org/10.1123/ijspp.2018-0103
  17. 17.
    Beyersmann D (2000) Regulation of mammalian gene expression. EXS 89:11–28PubMedGoogle Scholar
  18. 18.
    Bird JW, Carter JH, Triemer RE, Brooks RM, Spanier AM (1980) Proteinases in cardiac and skeletal muscle. Fed Proc 39:20–25PubMedGoogle Scholar
  19. 19.
    Bird SP, Tarpenning KM (2004) Influence of circadian time structure on acute hormonal responses to a single bout of heavy-resistance exercise in weight-trained men. Chronobiol Int 21:131–146CrossRefGoogle Scholar
  20. 20.
    Burd NA, West DW, Staples AW, Atherton PJ, Baker JM, Moore DR, Holwerda AM, Parise G, Rennie MJ, Baker SK, Phillips SM (2010) Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS One 5:e12033.  https://doi.org/10.1371/journal.pone.0012033 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Burley SD, Whittingham-Dowd J, Allen J, Grosset JF, Onambele-Pearson GL (2016) The differential hormonal milieu of morning versus evening may have an impact on muscle hypertrophic potential. PLoS One 11:e0161500.  https://doi.org/10.1371/journal.pone.0161500 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Calalb MB, Polte TR, Hanks SK (1995) Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol 15:954–963CrossRefGoogle Scholar
  23. 23.
    Camera DM (2018) Anabolic heterogeneity following resistance training: a role for circadian rhythm? Front Physiol 9:569.  https://doi.org/10.3389/fphys.2018.00569 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Camera DM, Smiles WJ, Hawley JA (2016) Exercise-induced skeletal muscle signaling pathways and human athletic performance. Free Radic Biol Med 98:131–143.  https://doi.org/10.1016/j.freeradbiomed.2016.02.007 CrossRefPubMedGoogle Scholar
  25. 25.
    Campion DR (1984) The muscle satellite cell: a review. Int Rev Cytol 87:225–251CrossRefGoogle Scholar
  26. 26.
    Carraro F, Stuart CA, Hartl WH, Rosenblatt J, Wolfe RR (1990) Effect of exercise and recovery on muscle protein synthesis in human subjects. Am J Phys 259:E470–E476.  https://doi.org/10.1152/ajpendo.1990.259.4.E470 CrossRefGoogle Scholar
  27. 27.
    Carson JA, Wei L (2000) Integrin signaling’s potential for mediating gene expression in hypertrophying skeletal muscle. J Appl Physiol (1985) 88:337–343.  https://doi.org/10.1152/jappl.2000.88.1.337 CrossRefGoogle Scholar
  28. 28.
    Cary LA, Guan JL (1999) Focal adhesion kinase in integrin-mediated signaling. Front Biosci 4:D102–D113CrossRefGoogle Scholar
  29. 29.
    Cheng Z, Zheng L, Almeida FA (2018) Epigenetic reprogramming in metabolic disorders: nutritional factors and beyond. J Nutr Biochem 54:1–10.  https://doi.org/10.1016/j.jnutbio.2017.10.004 CrossRefPubMedGoogle Scholar
  30. 30.
    Coffey VG, Hawley JA (2007) The molecular bases of training adaptation. Sports Med 37:737–763CrossRefGoogle Scholar
  31. 31.
    Coffey VG, Hawley JA (2017) Concurrent exercise training: do opposites distract? J Physiol 595:2883–2896.  https://doi.org/10.1113/JP272270 CrossRefPubMedGoogle Scholar
  32. 32.
    Crameri RM, Langberg H, Magnusson P, Jensen CH, Schroder HD, Olesen JL, Suetta C, Teisner B, Kjaer M (2004) Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol 558:333–340.  https://doi.org/10.1113/jphysiol.2004.061846 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Davidsen PK, Gallagher IJ, Hartman JW, Tarnopolsky MA, Dela F, Helge JW, Timmons JA, Phillips SM (2011) High responders to resistance exercise training demonstrate differential regulation of skeletal muscle microRNA expression. J Appl Physiol (1985) 110:309–317.  https://doi.org/10.1152/japplphysiol.00901.2010 CrossRefGoogle Scholar
  34. 34.
    Deane CS, Wilkinson DJ, Phillips BE, Smith K, Etheridge T, Atherton PJ (2017) “Nutraceuticals” in relation to human skeletal muscle and exercise. Am J Physiol Endocrinol Metab 312:E282–E299.  https://doi.org/10.1152/ajpendo.00230.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Deaton AM, Bird A (2011) CpG islands and the regulation of transcription. Genes Dev 25:1010–1022.  https://doi.org/10.1101/gad.2037511 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Deldicque L, Atherton P, Patel R, Theisen D, Nielens H, Rennie MJ, Francaux M (2008) Effects of resistance exercise with and without creatine supplementation on gene expression and cell signaling in human skeletal muscle. J Appl Physiol (1985) 104:371–378.  https://doi.org/10.1152/japplphysiol.00873.2007 CrossRefGoogle Scholar
  37. 37.
    Di Donato DM, West DW, Churchward-Venne TA, Breen L, Baker SK, Phillips SM (2014) Influence of aerobic exercise intensity on myofibrillar and mitochondrial protein synthesis in young men during early and late postexercise recovery. Am J Physiol Endocrinol Metab 306:E1025–E1032.  https://doi.org/10.1152/ajpendo.00487.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Donges CE, Burd NA, Duffield R, Smith GC, West DW, Short MJ, Mackenzie R, Plank LD, Shepherd PR, Phillips SM, Edge JA (2012) Concurrent resistance and aerobic exercise stimulates both myofibrillar and mitochondrial protein synthesis in sedentary middle-aged men. J Appl Physiol (1985) 112:1992–2001.  https://doi.org/10.1152/japplphysiol.00166.2012 CrossRefGoogle Scholar
  39. 39.
    Drummond MJ, McCarthy JJ, Fry CS, Esser KA, Rasmussen BB (2008) Aging differentially affects human skeletal muscle microRNA expression at rest and after an anabolic stimulus of resistance exercise and essential amino acids. Am J Physiol Endocrinol Metab 295:E1333–E1340.  https://doi.org/10.1152/ajpendo.90562.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE (2004) Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113:115–123.  https://doi.org/10.1172/JCI18330 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Durieux AC, Desplanches D, Freyssenet D, Fluck M (2007) Mechanotransduction in striated muscle via focal adhesion kinase. Biochem Soc Trans 35:1312–1313.  https://doi.org/10.1042/BST0351312 CrossRefPubMedGoogle Scholar
  42. 42.
    Elia L, Contu R, Quintavalle M, Varrone F, Chimenti C, Russo MA, Cimino V, De Marinis L, Frustaci A, Catalucci D, Condorelli G (2009) Reciprocal regulation of microRNA-1 and insulin-like growth factor-1 signal transduction cascade in cardiac and skeletal muscle in physiological and pathological conditions. Circulation 120:2377–2385.  https://doi.org/10.1161/CIRCULATIONAHA.109.879429 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Fagan JM, Waxman L, Goldberg AL (1987) Skeletal muscle and liver contain a soluble ATP + ubiquitin-dependent proteolytic system. Biochem J 243:335–343CrossRefGoogle Scholar
  44. 44.
    Fernandes T, Magalhaes FC, Roque FR, Phillips MI, Oliveira EM (2012) Exercise training prevents the microvascular rarefaction in hypertension balancing angiogenic and apoptotic factors: role of microRNAs-16, -21, and -126. Hypertension 59:513–520.  https://doi.org/10.1161/HYPERTENSIONAHA.111.185801 CrossRefPubMedGoogle Scholar
  45. 45.
    Figueiredo VC, Markworth JF (2015) Mechanisms of protein synthesis activation following exercise: new pieces to the increasingly complex puzzle. J Physiol 593:4693–4695.  https://doi.org/10.1113/JP271431 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Fluck M, Carson JA, Gordon SE, Ziemiecki A, Booth FW (1999) Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am J Phys 277:C152–C162CrossRefGoogle Scholar
  47. 47.
    Fritzen AM, Madsen AB, Kleinert M, Treebak JT, Lundsgaard AM, Jensen TE, Richter EA, Wojtaszewski J, Kiens B, Frosig C (2016) Regulation of autophagy in human skeletal muscle: effects of exercise, exercise training and insulin stimulation. J Physiol 594:745–761.  https://doi.org/10.1113/JP271405 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Fry CS, Drummond MJ, Glynn EL, Dickinson JM, Gundermann DM, Timmerman KL, Walker DK, Volpi E, Rasmussen BB (2013) Skeletal muscle autophagy and protein breakdown following resistance exercise are similar in younger and older adults. J Gerontol A Biol Sci Med Sci 68:599–607.  https://doi.org/10.1093/gerona/gls209 CrossRefPubMedGoogle Scholar
  49. 49.
    Fyfe JJ, Bishop DJ, Stepto NK (2014) Interference between concurrent resistance and endurance exercise: molecular bases and the role of individual training variables. Sports Med 44:743–762.  https://doi.org/10.1007/s40279-014-0162-1 CrossRefPubMedGoogle Scholar
  50. 50.
    Gissel H (2005) The role of Ca2+ in muscle cell damage. Ann N Y Acad Sci 1066:166–180.  https://doi.org/10.1196/annals.1363.013 CrossRefPubMedGoogle Scholar
  51. 51.
    Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428.  https://doi.org/10.1152/physrev.00027.2001 CrossRefPubMedGoogle Scholar
  52. 52.
    Glynn EL, Fry CS, Drummond MJ, Dreyer HC, Dhanani S, Volpi E, Rasmussen BB (2010) Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. Am J Physiol Regul Integr Comp Physiol 299:R533–R540.  https://doi.org/10.1152/ajpregu.00077.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Goldspink G (2005) Mechanical signals, IGF-I gene splicing, and muscle adaptation. Physiology (Bethesda) 20:232–238.  https://doi.org/10.1152/physiol.00004.2005 CrossRefGoogle Scholar
  54. 54.
    Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83:731–801.  https://doi.org/10.1152/physrev.00029.2002 CrossRefGoogle Scholar
  55. 55.
    Goodman CA (2014) The role of mTORC1 in regulating protein synthesis and skeletal muscle mass in response to various mechanical stimuli. Rev Physiol Biochem Pharmacol 166:43–95.  https://doi.org/10.1007/112_2013_17 CrossRefPubMedGoogle Scholar
  56. 56.
    Gordon BS, Liu C, Steiner JL, Nader GA, Jefferson LS, Kimball SR (2016) Loss of REDD1 augments the rate of the overload-induced increase in muscle mass. Am J Physiol Regul Integr Comp Physiol 311:R545–R557.  https://doi.org/10.1152/ajpregu.00159.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Gordon SE, Fluck M, Booth FW (2001) Selected contribution: skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent. J Appl Physiol (1985) 90:1174–1183; discussion 1165.  https://doi.org/10.1152/jappl.2001.90.3.1174 CrossRefGoogle Scholar
  58. 58.
    Hameed M, Orrell RW, Cobbold M, Goldspink G, Harridge SD (2003) Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J Physiol 547:247–254.  https://doi.org/10.1113/jphysiol.2002.032136 CrossRefPubMedGoogle Scholar
  59. 59.
    Harber MP, Crane JD, Dickinson JM, Jemiolo B, Raue U, Trappe TA, Trappe SW (2009) Protein synthesis and the expression of growth-related genes are altered by running in human vastus lateralis and soleus muscles. Am J Physiol Regul Integr Comp Physiol 296:R708–R714.  https://doi.org/10.1152/ajpregu.90906.2008 CrossRefPubMedGoogle Scholar
  60. 60.
    Harber MP, Konopka AR, Jemiolo B, Trappe SW, Trappe TA, Reidy PT (2010) Muscle protein synthesis and gene expression during recovery from aerobic exercise in the fasted and fed states. Am J Physiol Regul Integr Comp Physiol 299:R1254–R1262.  https://doi.org/10.1152/ajpregu.00348.2010 CrossRefPubMedGoogle Scholar
  61. 61.
    He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531.  https://doi.org/10.1038/nrg1379 CrossRefGoogle Scholar
  62. 62.
    Heinemeier KM, Schjerling P, Heinemeier J, Magnusson SP, Kjaer M (2013) Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb (14)C. FASEB J 27:2074–2079.  https://doi.org/10.1096/fj.12-225599 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Hickson RC (1980) Interference of strength development by simultaneously training for strength and endurance. Eur J Appl Physiol Occup Physiol 45:255–263CrossRefGoogle Scholar
  64. 64.
    Hill M, Goldspink G (2003) Expression and splicing of the insulin-like growth factor gene in rodent muscle is associated with muscle satellite (stem) cell activation following local tissue damage. J Physiol 549:409–418.  https://doi.org/10.1113/jphysiol.2002.035832 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Hollander J, Fiebig R, Gore M, Ookawara T, Ohno H, Ji LL (2001) Superoxide dismutase gene expression is activated by a single bout of exercise in rat skeletal muscle. Pflugers Arch 442:426–434CrossRefGoogle Scholar
  66. 66.
    Holloszy JO (1967) Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 242:2278–2282PubMedGoogle Scholar
  67. 67.
    Holloszy JO, Coyle EF (1984) Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol Respir Environ Exerc Physiol 56:831–838.  https://doi.org/10.1152/jappl.1984.56.4.831 CrossRefPubMedGoogle Scholar
  68. 68.
    Hubal MJ, Gordish-Dressman H, Thompson PD, Price TB, Hoffman EP, Angelopoulos TJ, Gordon PM, Moyna NM, Pescatello LS, Visich PS, Zoeller RF, Seip RL, Clarkson PM (2005) Variability in muscle size and strength gain after unilateral resistance training. Med Sci Sports Exerc 37:964–972CrossRefGoogle Scholar
  69. 69.
    Hughes DC, Ellefsen S, Baar K (2018) Adaptations to endurance and strength training. Cold Spring Harb Perspect Med 8.  https://doi.org/10.1101/cshperspect.a029769 CrossRefGoogle Scholar
  70. 70.
    Jacobs BL, Goodman CA, Hornberger TA (2014) The mechanical activation of mTOR signaling: an emerging role for late endosome/lysosomal targeting. J Muscle Res Cell Motil 35:11–21.  https://doi.org/10.1007/s10974-013-9367-4 CrossRefPubMedGoogle Scholar
  71. 71.
    Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl):245–254.  https://doi.org/10.1038/ng1089 CrossRefPubMedGoogle Scholar
  72. 72.
    Jamart C, Benoit N, Raymackers JM, Kim HJ, Kim CK, Francaux M (2012) Autophagy-related and autophagy-regulatory genes are induced in human muscle after ultraendurance exercise. Eur J Appl Physiol 112:3173–3177.  https://doi.org/10.1007/s00421-011-2287-3 CrossRefPubMedGoogle Scholar
  73. 73.
    Jamart C, Naslain D, Gilson H, Francaux M (2013) Higher activation of autophagy in skeletal muscle of mice during endurance exercise in the fasted state. Am J Physiol Endocrinol Metab 305:E964–E974.  https://doi.org/10.1152/ajpendo.00270.2013 CrossRefPubMedGoogle Scholar
  74. 74.
    Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080.  https://doi.org/10.1126/science.1063127 CrossRefPubMedGoogle Scholar
  75. 75.
    Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492.  https://doi.org/10.1038/nrg3230 CrossRefPubMedGoogle Scholar
  76. 76.
    Jones PA, Baylin SB (2007) The epigenomics of cancer. Cell 128:683–692.  https://doi.org/10.1016/j.cell.2007.01.029 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Kadi F, Charifi N, Denis C, Lexell J, Andersen JL, Schjerling P, Olsen S, Kjaer M (2005) The behaviour of satellite cells in response to exercise: what have we learned from human studies? Pflugers Arch 451:319–327.  https://doi.org/10.1007/s00424-005-1406-6 CrossRefPubMedGoogle Scholar
  78. 78.
    Kadi F, Schjerling P, Andersen LL, Charifi N, Madsen JL, Christensen LR, Andersen JL (2004) The effects of heavy resistance training and detraining on satellite cells in human skeletal muscles. J Physiol 558:1005–1012.  https://doi.org/10.1113/jphysiol.2004.065904 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Kinbara K, Sorimachi H, Ishiura S, Suzuki K (1997) Muscle-specific calpain, p94, interacts with the extreme C-terminal region of connectin, a unique region flanked by two immunoglobulin C2 motifs. Arch Biochem Biophys 342:99–107.  https://doi.org/10.1006/abbi.1997.0108 CrossRefPubMedGoogle Scholar
  80. 80.
    Kirby TJ, McCarthy JJ, Peterson CA, Fry CS (2016) Synergist ablation as a rodent model to study satellite cell dynamics in adult skeletal muscle. Methods Mol Biol 1460:43–52.  https://doi.org/10.1007/978-1-4939-3810-0_4 CrossRefPubMedGoogle Scholar
  81. 81.
    Klionsky DJ (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8:931–937.  https://doi.org/10.1038/nrm2245 CrossRefPubMedGoogle Scholar
  82. 82.
    Klossner S, Durieux AC, Freyssenet D, Flueck M (2009) Mechano-transduction to muscle protein synthesis is modulated by FAK. Eur J Appl Physiol 106:389–398.  https://doi.org/10.1007/s00421-009-1032-7 CrossRefPubMedGoogle Scholar
  83. 83.
    Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ (2009) Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 587:211–217.  https://doi.org/10.1113/jphysiol.2008.164483 CrossRefPubMedGoogle Scholar
  84. 84.
    Kvorning T, Andersen M, Brixen K, Madsen K (2006) Suppression of endogenous testosterone production attenuates the response to strength training: a randomized, placebo-controlled, and blinded intervention study. Am J Physiol Endocrinol Metab 291:E1325–E1332.  https://doi.org/10.1152/ajpendo.00143.2006 CrossRefPubMedGoogle Scholar
  85. 85.
    Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R (2002) Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277:49831–49840.  https://doi.org/10.1074/jbc.M204291200 CrossRefPubMedGoogle Scholar
  86. 86.
    Louis E, Raue U, Yang Y, Jemiolo B, Trappe S (2007) Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol (1985) 103:1744–1751.  https://doi.org/10.1152/japplphysiol.00679.2007 CrossRefGoogle Scholar
  87. 87.
    Lowe DA, Alway SE (1999) Stretch-induced myogenin, MyoD, and MRF4 expression and acute hypertrophy in quail slow-tonic muscle are not dependent upon satellite cell proliferation. Cell Tissue Res 296:531–539CrossRefGoogle Scholar
  88. 88.
    Lundberg TR, Fernandez-Gonzalo R, Gustafsson T, Tesch PA (2013) Aerobic exercise does not compromise muscle hypertrophy response to short-term resistance training. J Appl Physiol (1985) 114:81–89.  https://doi.org/10.1152/japplphysiol.01013.2012 CrossRefGoogle Scholar
  89. 89.
    Martin-Rincon M, Morales-Alamo D, Calbet JAL (2018) Exercise-mediated modulation of autophagy in skeletal muscle. Scand J Med Sci Sports 28:772–781.  https://doi.org/10.1111/sms.12945 CrossRefPubMedGoogle Scholar
  90. 90.
    Mascher H, Ekblom B, Rooyackers O, Blomstrand E (2011) Enhanced rates of muscle protein synthesis and elevated mTOR signalling following endurance exercise in human subjects. Acta Physiol (Oxf) 202:175–184.  https://doi.org/10.1111/j.1748-1716.2011.02274.x CrossRefGoogle Scholar
  91. 91.
    Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495CrossRefGoogle Scholar
  92. 92.
    Mayer C, Grummt I (2006) Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25:6384–6391.  https://doi.org/10.1038/sj.onc.1209883 CrossRefPubMedGoogle Scholar
  93. 93.
    McCarthy JJ, Esser KA (2007) Counterpoint: satellite cell addition is not obligatory for skeletal muscle hypertrophy. J Appl Physiol (1985) 103:1100–1102; discussion 1102–1103.  https://doi.org/10.1152/japplphysiol.00101.2007a CrossRefGoogle Scholar
  94. 94.
    McCarthy JJ, Esser KA (2007) MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J Appl Physiol (1985) 102:306–313. doi: https://doi.org/10.1152/japplphysiol.00932.2006 CrossRefGoogle Scholar
  95. 95.
    McGee SL, Hargreaves M (2011) Histone modifications and exercise adaptations. J Appl Physiol (1985) 110:258–263.  https://doi.org/10.1152/japplphysiol.00979.2010 CrossRefGoogle Scholar
  96. 96.
    McGee SL, Walder KR (2017) Exercise and the skeletal muscle epigenome. Cold Spring Harb Perspect Med 7.  https://doi.org/10.1101/cshperspect.a029876 CrossRefGoogle Scholar
  97. 97.
    McGlory C, van Vliet S, Stokes T, Mittendorfer B, Phillips SM (2018) The impact of exercise and nutrition in the regulation of skeletal muscle mass. J Physiol.  https://doi.org/10.1113/JP275443
  98. 98.
    Meissner JD, Kubis HP, Scheibe RJ, Gros G (2000) Reversible Ca2+-induced fast-to-slow transition in primary skeletal muscle culture cells at the mRNA level. J Physiol 523(Pt 1):19–28CrossRefGoogle Scholar
  99. 99.
    Miller BF, Hansen M, Olesen JL, Schwarz P, Babraj JA, Smith K, Rennie MJ, Kjaer M (2007) Tendon collagen synthesis at rest and after exercise in women. J Appl Physiol (1985) 102:541–546.  https://doi.org/10.1152/japplphysiol.00797.2006 CrossRefGoogle Scholar
  100. 100.
    Miller BF, Olesen JL, Hansen M, Dossing S, Crameri RM, Welling RJ, Langberg H, Flyvbjerg A, Kjaer M, Babraj JA, Smith K, Rennie MJ (2005) Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J Physiol 567:1021–1033.  https://doi.org/10.1113/jphysiol.2005.093690 CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Moller AB, Vendelbo MH, Christensen B, Clasen BF, Bak AM, Jorgensen JO, Moller N, Jessen N (2015) Physical exercise increases autophagic signaling through ULK1 in human skeletal muscle. J Appl Physiol (1985) 118:971–979.  https://doi.org/10.1152/japplphysiol.01116.2014 CrossRefGoogle Scholar
  102. 102.
    Moore DR, Young M, Phillips SM (2012) Similar increases in muscle size and strength in young men after training with maximal shortening or lengthening contractions when matched for total work. Eur J Appl Physiol 112:1587–1592.  https://doi.org/10.1007/s00421-011-2078-x CrossRefPubMedGoogle Scholar
  103. 103.
    Morton RW, Murphy KT, McKellar SR, Schoenfeld BJ, Henselmans M, Helms E, Aragon AA, Devries MC, Banfield L, Krieger JW, Phillips SM (2018) 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 52:376–384.  https://doi.org/10.1136/bjsports-2017-097608 CrossRefPubMedGoogle Scholar
  104. 104.
    Murach KA, Bagley JR (2016) Skeletal muscle hypertrophy with concurrent exercise training: contrary evidence for an interference effect. Sports Med 46:1029–1039.  https://doi.org/10.1007/s40279-016-0496-y CrossRefPubMedGoogle Scholar
  105. 105.
    Nader GA (2006) Concurrent strength and endurance training: from molecules to man. Med Sci Sports Exerc 38:1965–1970.  https://doi.org/10.1249/01.mss.0000233795.39282.33 CrossRefPubMedGoogle Scholar
  106. 106.
    Nader GA, Esser KA (2001) Intracellular signaling specificity in skeletal muscle in response to different modes of exercise. J Appl Physiol (1985) 90:1936–1942.  https://doi.org/10.1152/jappl.2001.90.5.1936 CrossRefGoogle Scholar
  107. 107.
    Nedergaard A, Vissing K, Overgaard K, Kjaer M, Schjerling P (2007) Expression patterns of atrogenic and ubiquitin proteasome component genes with exercise: effect of different loading patterns and repeated exercise bouts. J Appl Physiol (1985) 103:1513–1522.  https://doi.org/10.1152/japplphysiol.01445.2006 CrossRefGoogle Scholar
  108. 108.
    Nielsen S, Scheele C, Yfanti C, Akerstrom T, Nielsen AR, Pedersen BK, Laye MJ (2010) Muscle specific microRNAs are regulated by endurance exercise in human skeletal muscle. J Physiol 588:4029–4037.  https://doi.org/10.1113/jphysiol.2010.189860 CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    O’Connor RS, Pavlath GK, McCarthy JJ, Esser KA (2007) Last word on point:counterpoint: satellite cell addition is/is not obligatory for skeletal muscle hypertrophy. J Appl Physiol (1985) 103:1107.  https://doi.org/10.1152/japplphysiol.00502.2007 CrossRefGoogle Scholar
  110. 110.
    O’Neil TK, Duffy LR, Frey JW, Hornberger TA (2009) The role of phosphoinositide 3-kinase and phosphatidic acid in the regulation of mammalian target of rapamycin following eccentric contractions. J Physiol 587:3691–3701.  https://doi.org/10.1113/jphysiol.2009.173609 CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Olsen S, Aagaard P, Kadi F, Tufekovic G, Verney J, Olesen JL, Suetta C, Kjaer M (2006) Creatine supplementation augments the increase in satellite cell and myonuclei number in human skeletal muscle induced by strength training. J Physiol 573:525–534.  https://doi.org/10.1113/jphysiol.2006.107359 CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Olson EN, Williams RS (2000) Calcineurin signaling and muscle remodeling. Cell 101:689–692CrossRefGoogle Scholar
  113. 113.
    Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131–24145.  https://doi.org/10.1074/jbc.M702824200 CrossRefPubMedGoogle Scholar
  114. 114.
    Pareja-Galeano H, Sanchis-Gomar F, Garcia-Gimenez JL (2014) Physical exercise and epigenetic modulation: elucidating intricate mechanisms. Sports Med 44:429–436.  https://doi.org/10.1007/s40279-013-0138-6 CrossRefPubMedGoogle Scholar
  115. 115.
    Pasiakos SM, Carbone JW (2014) Assessment of skeletal muscle proteolysis and the regulatory response to nutrition and exercise. IUBMB Life 66:478–484.  https://doi.org/10.1002/iub.1291 CrossRefPubMedGoogle Scholar
  116. 116.
    Pasiakos SM, McClung HL, McClung JP, Urso ML, Pikosky MA, Cloutier GJ, Fielding RA, Young AJ (2010) Molecular responses to moderate endurance exercise in skeletal muscle. Int J Sport Nutr Exerc Metab 20:282–290CrossRefGoogle Scholar
  117. 117.
    Petrella JK, Kim JS, Cross JM, Kosek DJ, Bamman MM (2006) Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women. Am J Physiol Endocrinol Metab 291:E937–E946.  https://doi.org/10.1152/ajpendo.00190.2006 CrossRefPubMedGoogle Scholar
  118. 118.
    Phillips SM, Hartman JW, Wilkinson SB (2005) Dietary protein to support anabolism with resistance exercise in young men. J Am Coll Nutr 24:134S–139SCrossRefGoogle Scholar
  119. 119.
    Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Phys 273:E99–E107.  https://doi.org/10.1152/ajpendo.1997.273.1.E99 CrossRefGoogle Scholar
  120. 120.
    Phillips SM, Tipton KD, Ferrando AA, Wolfe RR (1999) Resistance training reduces the acute exercise-induced increase in muscle protein turnover. Am J Phys 276:E118–E124Google Scholar
  121. 121.
    Proud CG (2007) Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J 403:217–234.  https://doi.org/10.1042/BJ20070024 CrossRefPubMedGoogle Scholar
  122. 122.
    Puri PL, Sartorelli V (2000) Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J Cell Physiol 185:155–173.  https://doi.org/10.1002/1097-4652(200011)185:2<155::AID-JCP1>3.0.CO;2-Z CrossRefPubMedGoogle Scholar
  123. 123.
    Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Moreau K, Narayanan U, Renna M, Siddiqi FH, Underwood BR, Winslow AR, Rubinsztein DC (2010) Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 90:1383–1435.  https://doi.org/10.1152/physrev.00030.2009 CrossRefGoogle Scholar
  124. 124.
    Rennie MJ, Wackerhage H, Spangenburg EE, Booth FW (2004) Control of the size of the human muscle mass. Annu Rev Physiol 66:799–828.  https://doi.org/10.1146/annurev.physiol.66.052102.134444 CrossRefPubMedGoogle Scholar
  125. 125.
    Richter EA, Derave W, Wojtaszewski JF (2001) Glucose, exercise and insulin: emerging concepts. J Physiol 535:313–322CrossRefGoogle Scholar
  126. 126.
    Rios R, Carneiro I, Arce VM, Devesa J (2001) Myostatin regulates cell survival during C2C12 myogenesis. Biochem Biophys Res Commun 280:561–566.  https://doi.org/10.1006/bbrc.2000.4159 CrossRefPubMedGoogle Scholar
  127. 127.
    Roig M, O’Brien K, Kirk G, Murray R, McKinnon P, Shadgan B, Reid WD (2009) The effects of eccentric versus concentric resistance training on muscle strength and mass in healthy adults: a systematic review with meta-analysis. Br J Sports Med 43:556–568.  https://doi.org/10.1136/bjsm.2008.051417 CrossRefPubMedGoogle Scholar
  128. 128.
    Roth SM, Martel GF, Ivey FM, Lemmer JT, Tracy BL, Metter EJ, Hurley BF, Rogers MA (2001) Skeletal muscle satellite cell characteristics in young and older men and women after heavy resistance strength training. J Gerontol A Biol Sci Med Sci 56:B240–B247CrossRefGoogle Scholar
  129. 129.
    Russell AP, Lamon S (2015) Exercise, skeletal muscle and circulating microRNAs. Prog Mol Biol Transl Sci 135:471–496.  https://doi.org/10.1016/bs.pmbts.2015.07.018 CrossRefPubMedGoogle Scholar
  130. 130.
    Russell AP, Lamon S, Boon H, Wada S, Guller I, Brown EL, Chibalin AV, Zierath JR, Snow RJ, Stepto N, Wadley GD, Akimoto T (2013) Regulation of miRNAs in human skeletal muscle following acute endurance exercise and short-term endurance training. J Physiol 591:4637–4653.  https://doi.org/10.1113/jphysiol.2013.255695 CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    Safdar A, Abadi A, Akhtar M, Hettinga BP, Tarnopolsky MA (2009) miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6J male mice. PLoS One 4:e5610.  https://doi.org/10.1371/journal.pone.0005610 CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    Sandri M (2013) Protein breakdown in muscle wasting: role of autophagy-lysosome and ubiquitin-proteasome. Int J Biochem Cell Biol 45:2121–2129.  https://doi.org/10.1016/j.biocel.2013.04.023 CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Schlaepfer DD, Hauck CR, Sieg DJ (1999) Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71:435–478CrossRefGoogle Scholar
  134. 134.
    Schultz E, McCormick KM (1994) Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 123:213–257CrossRefGoogle Scholar
  135. 135.
    Schwalm C, Jamart C, Benoit N, Naslain D, Premont C, Prevet J, Van Thienen R, Deldicque L, Francaux M (2015) Activation of autophagy in human skeletal muscle is dependent on exercise intensity and AMPK activation. FASEB J 29:3515–3526.  https://doi.org/10.1096/fj.14-267187 CrossRefPubMedGoogle Scholar
  136. 136.
    Seaborne RA, Strauss J, Cocks M, Shepherd S, O’Brien TD, van Someren KA, Bell PG, Murgatroyd C, Morton JP, Stewart CE, Sharples AP (2018) Human skeletal muscle possesses an epigenetic memory of hypertrophy. Sci Rep 8:1898.  https://doi.org/10.1038/s41598-018-20287-3 CrossRefPubMedPubMedCentralGoogle Scholar
  137. 137.
    Shamim B, Hawley JA, Camera DM (2018) Protein availability and satellite cell dynamics in skeletal muscle. Sports Med 48:1329–1343.  https://doi.org/10.1007/s40279-018-0883-7 CrossRefPubMedGoogle Scholar
  138. 138.
    Sheffield-Moore M, Yeckel CW, Volpi E, Wolf SE, Morio B, Chinkes DL, Paddon-Jones D, Wolfe RR (2004) Postexercise protein metabolism in older and younger men following moderate-intensity aerobic exercise. Am J Physiol Endocrinol Metab 287:E513–E522.  https://doi.org/10.1152/ajpendo.00334.2003 CrossRefPubMedGoogle Scholar
  139. 139.
    Spangenburg EE, Le Roith D, Ward CW, Bodine SC (2008) A functional insulin-like growth factor receptor is not necessary for load-induced skeletal muscle hypertrophy. J Physiol 586:283–291.  https://doi.org/10.1113/jphysiol.2007.141507 CrossRefPubMedGoogle Scholar
  140. 140.
    Stec MJ, Kelly NA, Many GM, Windham ST, Tuggle SC, Bamman MM (2016) Ribosome biogenesis may augment resistance training-induced myofiber hypertrophy and is required for myotube growth in vitro. Am J Physiol Endocrinol Metab 310:E652–E661.  https://doi.org/10.1152/ajpendo.00486.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  141. 141.
    Stefanetti RJ, Lamon S, Wallace M, Vendelbo MH, Russell AP, Vissing K (2015) Regulation of ubiquitin proteasome pathway molecular markers in response to endurance and resistance exercise and training. Pflugers Arch 467:1523–1537.  https://doi.org/10.1007/s00424-014-1587-y CrossRefPubMedGoogle Scholar
  142. 142.
    Stokes T, Hector AJ, Morton RW, McGlory C, Phillips SM (2018) Recent perspectives regarding the role of dietary protein for the promotion of muscle hypertrophy with resistance exercise training. Nutrients 10.  https://doi.org/10.3390/nu10020180
  143. 143.
    Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45.  https://doi.org/10.1038/47412 CrossRefGoogle Scholar
  144. 144.
    Szewczyk NJ, Jacobson LA (2005) Signal-transduction networks and the regulation of muscle protein degradation. Int J Biochem Cell Biol 37:1997–2011.  https://doi.org/10.1016/j.biocel.2005.02.020 CrossRefPubMedGoogle Scholar
  145. 145.
    Tang G (2005) siRNA and miRNA: an insight into RISCs. Trends Biochem Sci 30:106–114.  https://doi.org/10.1016/j.tibs.2004.12.007 CrossRefPubMedGoogle Scholar
  146. 146.
    Ten Broek RW, Grefte S, Von den Hoff JW (2010) Regulatory factors and cell populations involved in skeletal muscle regeneration. J Cell Physiol 224:7–16. doi: https://doi.org/10.1002/jcp.22127
  147. 147.
    Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275:40235–40243.  https://doi.org/10.1074/jbc.M004356200 CrossRefPubMedGoogle Scholar
  148. 148.
    Timmons JA, Larsson O, Jansson E, Fischer H, Gustafsson T, Greenhaff PL, Ridden J, Rachman J, Peyrard-Janvid M, Wahlestedt C, Sundberg CJ (2005) Human muscle gene expression responses to endurance training provide a novel perspective on Duchenne muscular dystrophy. FASEB J 19:750–760.  https://doi.org/10.1096/fj.04-1980com CrossRefPubMedGoogle Scholar
  149. 149.
    Tipton KD, Ferrando AA, Phillips SM, Doyle D Jr, Wolfe RR (1999) Postexercise net protein synthesis in human muscle from orally administered amino acids. Am J Phys 276:E628–E634CrossRefGoogle Scholar
  150. 150.
    Tipton KD, Ferrando AA, Williams BD, Wolfe RR (1996) Muscle protein metabolism in female swimmers after a combination of resistance and endurance exercise. J Appl Physiol (1985) 81:2034–2038.  https://doi.org/10.1152/jappl.1996.81.5.2034 CrossRefGoogle Scholar
  151. 151.
    Turinsky J, Damrau-Abney A (1999) Akt kinases and 2-deoxyglucose uptake in rat skeletal muscles in vivo: study with insulin and exercise. Am J Phys 276:R277–R282Google Scholar
  152. 152.
    van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, Kelm RJ Jr, Olson EN (2009) A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 17:662–673.  https://doi.org/10.1016/j.devcel.2009.10.013 CrossRefPubMedPubMedCentralGoogle Scholar
  153. 153.
    Walsh FS, Celeste AJ (2005) Myostatin: a modulator of skeletal-muscle stem cells. Biochem Soc Trans 33:1513–1517.  https://doi.org/10.1042/BST20051513 CrossRefPubMedGoogle Scholar
  154. 154.
    Wang XH, Zhang L, Mitch WE, LeDoux JM, Hu J, Du J (2010) Caspase-3 cleaves specific 19 S proteasome subunits in skeletal muscle stimulating proteasome activity. J Biol Chem 285:21249–21257.  https://doi.org/10.1074/jbc.M109.041707 CrossRefPubMedPubMedCentralGoogle Scholar
  155. 155.
    Watson K, Baar K (2014) mTOR and the health benefits of exercise. Semin Cell Dev Biol 36:130–139.  https://doi.org/10.1016/j.semcdb.2014.08.013 CrossRefPubMedGoogle Scholar
  156. 156.
    Wei L, Wang L, Carson JA, Agan JE, Imanaka-Yoshida K, Schwartz RJ (2001) beta1 integrin and organized actin filaments facilitate cardiomyocyte-specific RhoA-dependent activation of the skeletal alpha-actin promoter. FASEB J 15:785–796.  https://doi.org/10.1096/fj.00-026com CrossRefPubMedGoogle Scholar
  157. 157.
    West DW, Burd NA, Tang JE, Moore DR, Staples AW, Holwerda AM, Baker SK, Phillips SM (2010) Elevations in ostensibly anabolic hormones with resistance exercise enhance neither training-induced muscle hypertrophy nor strength of the elbow flexors. J Appl Physiol (1985) 108:60–67.  https://doi.org/10.1152/japplphysiol.01147.2009 CrossRefGoogle Scholar
  158. 158.
    West DW, Kujbida GW, Moore DR, Atherton P, Burd NA, Padzik JP, De Lisio M, Tang JE, Parise G, Rennie MJ, Baker SK, Phillips SM (2009) Resistance exercise-induced increases in putative anabolic hormones do not enhance muscle protein synthesis or intracellular signalling in young men. J Physiol 587:5239–5247.  https://doi.org/10.1113/jphysiol.2009.177220 CrossRefPubMedPubMedCentralGoogle Scholar
  159. 159.
    Widegren U, Wretman C, Lionikas A, Hedin G, Henriksson J (2000) Influence of exercise intensity on ERK/MAP kinase signalling in human skeletal muscle. Pflugers Arch 441:317–322CrossRefGoogle Scholar
  160. 160.
    Wilborn CD, Taylor LW, Greenwood M, Kreider RB, Willoughby DS (2009) Effects of different intensities of resistance exercise on regulators of myogenesis. J Strength Cond Res 23:2179–2187.  https://doi.org/10.1519/JSC.0b013e3181bab493 CrossRefPubMedGoogle Scholar
  161. 161.
    Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE, Tarnopolsky MA, Rennie MJ (2008) Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J Physiol 586:3701–3717.  https://doi.org/10.1113/jphysiol.2008.153916 CrossRefPubMedPubMedCentralGoogle Scholar
  162. 162.
    Winder WW, Hardie DG (1999) AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am J Phys 277:E1–E10Google Scholar
  163. 163.
    Wolfe RR (2000) Protein supplements and exercise. Am J Clin Nutr 72:551S–557S.  https://doi.org/10.1093/ajcn/72.2.551S CrossRefPubMedGoogle Scholar
  164. 164.
    Wong TS, Booth FW (1990) Protein metabolism in rat gastrocnemius muscle after stimulated chronic concentric exercise. J Appl Physiol (1985) 69:1709–1717.  https://doi.org/10.1152/jappl.1990.69.5.1709 CrossRefGoogle Scholar
  165. 165.
    Wong TS, Booth FW (1990) Protein metabolism in rat tibialis anterior muscle after stimulated chronic eccentric exercise. J Appl Physiol (1985) 69:1718–1724.  https://doi.org/10.1152/jappl.1990.69.5.1718 CrossRefGoogle Scholar
  166. 166.
    Woodgett JR (1989) Early gene induction by growth factors. Br Med Bull 45:529–540CrossRefGoogle Scholar
  167. 167.
    Yamamoto H, Morino K, Nishio Y, Ugi S, Yoshizaki T, Kashiwagi A, Maegawa H (2012) MicroRNA-494 regulates mitochondrial biogenesis in skeletal muscle through mitochondrial transcription factor A and Forkhead box j3. Am J Physiol Endocrinol Metab 303:E1419–E1427.  https://doi.org/10.1152/ajpendo.00097.2012 CrossRefPubMedGoogle Scholar
  168. 168.
    Yang SY, Goldspink G (2002) Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett 522:156–160CrossRefGoogle Scholar
  169. 169.
    Zeman RJ, Kameyama T, Matsumoto K, Bernstein P, Etlinger JD (1985) Regulation of protein degradation in muscle by calcium. Evidence for enhanced nonlysosomal proteolysis associated with elevated cytosolic calcium. J Biol Chem 260:13619–13624PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of NeuroscienceUniversité catholique de LouvainLouvain-la-NeuveBelgium

Personalised recommendations