Exercise and the Regulation of Skeletal Muscle Hypertrophy

Progress in Molecular Biology and Translational Science

Volumn 135, Issue , 2015, Pages 153-173

  McGlory, Chris ^a   Phillips, Stuart M ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Hypertrophy; MTORC1; P70S6K1; Resistance exercise; Skeletal muscle

Indexed keywords

HORMONE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; TARGET OF RAPAMYCIN KINASE;

AGING; CONFERENCE PAPER; EXERCISE; HUMAN; MUSCLE HYPERTROPHY; MUSCLE MASS; MUSCLE PROTEIN SYNTHESIS; MUSCLE TRAINING; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESISTANCE TRAINING; ANIMAL; HYPERTROPHY; METABOLISM; PATHOLOGY; PHYSIOLOGY; SKELETAL MUSCLE;

ANIMALS; EXERCISE; HUMANS; HYPERTROPHY; MULTIPROTEIN COMPLEXES; MUSCLE, SKELETAL; PROTEIN BIOSYNTHESIS; RESISTANCE TRAINING; TOR SERINE-THREONINE KINASES;

EID: 84938268631     PISSN: 18771173     EISSN: 18780814     Source Type: Book Series    
DOI: 10.1016/bs.pmbts.2015.06.018     Document Type: Conference Paper

References (100)

1. B. Egan, and J.R. Zierath Exercise metabolism and the molecular regulation of skeletal muscle adaptation Cell Metab 17 2 2013 162 184
2. S.M. Phillips Physiologic and molecular bases of muscle hypertrophy and atrophy: impact of resistance exercise on human skeletal muscle (protein and exercise dose effects) Appl Physiol Nutr Metab 34 3 2009 403 410
3. H. Claassen, C. Gerber, H. Hoppeler, J.M. Luthi, and P. Vock Muscle filament spacing and short-term heavy-resistance exercise in humans J Physiol 409 1989 491 495
4. G. Kelley Mechanical overload and skeletal muscle fiber hyperplasia: a meta-analysis J Appl Physiol (1985) 81 4 1996 1584 1588
5. K.D. Tipton, A.A. Ferrando, S.M. Phillips, D. Doyle Jr., and R.R. Wolfe Postexercise net protein synthesis in human muscle from orally administered amino acids Am J Physiol 276 4 pt 1 1999 E628 E634
6. O.C. Witard, M. Tieland, M. Beelen, K.D. Tipton, L.J. van Loon, and R. Koopman Resistance exercise increases postprandial muscle protein synthesis in humans Med Sci Sports Exerc 41 1 2009 144 154
7. N.A. Burd, D.W. West, D.R. Moore, and et al. Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24 h after resistance exercise in young men J Nutr 141 4 2011 568 573
8. T.L. De Lorme, and A.L. Watkins Technics of progressive resistance exercise Arch Phys Med Rehabil 29 5 1948 263 273
9. N.M. Cermak, P.T. Res, L.C. de Groot, W.H. Saris, and L.J. van Loon Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis Am J Clin Nutr 96 6 2012 1454 1464
10. American College of Sports Medicine American college of sports medicine position stand. Progression models in resistance training for healthy adults Med Sci Sports Exerc 41 3 2009 687 708
11. B.J. Schoenfeld, J.M. Wilson, R.P. Lowery, and J.W. Krieger Muscular adaptations in low- versus high-load resistance training: a meta-analysis Eur J Sport Sci 2014 1 10
12. C.J. Mitchell, T.A. Churchward-Venne, D.W.D. West, and et al. Resistance exercise load does not determine training-mediated hypertrophic gains in young men J Appl Physiol 113 1 2012 71 77
13. N.A. Burd, A.M. Holwerda, K.C. Selby, and et al. Resistance exercise volume affects myofibrillar protein synthesis and anabolic signalling molecule phosphorylation in young men J Physiol 588 pt 16 2010 3119 3130
14. M.J. Hubal, H. Gordish-Dressman, P.D. Thompson, and et al. Variability in muscle size and strength gain after unilateral resistance training Med Sci Sports Exerc 37 6 2005 964 972
15. M.M. Bamman, J.K. Petrella, J.S. Kim, D.L. Mayhew, and J.M. Cross Cluster analysis tests the importance of myogenic gene expression during myofiber hypertrophy in humans J Appl Physiol (1985) 102 6 2007 2232 2239
16. J.W. Hartman, J.E. Tang, S.B. Wilkinson, and et al. Consumption of fat-free fluid milk after resistance exercise promotes greater lean mass accretion than does consumption of soy or carbohydrate in young, novice, male weightlifters Am J Clin Nutr 86 2 2007 373 381
17. N.A. Burd, D.R. Moore, C.J. Mitchell, and S.M. Phillips Big claims for big weights but with little evidence Eur J Appl Physiol 113 1 2013 267 268
18. W.J. Kraemer, and N.A. Ratamess Hormonal responses and adaptations to resistance exercise and training Sports Med 35 4 2005 339 361
19. S. Bhasin, T.W. Storer, N. Berman, and et al. The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men N Engl J Med 335 1 1996 1 7
20. M.J. Rennie Claims for the anabolic effects of growth hormone: a case of the emperor's new clothes? Br J Sports Med 37 2 2003 100 105
21. S. Doessing, K.M. Heinemeier, L. Holm, and et al. Growth hormone stimulates the collagen synthesis in human tendon and skeletal muscle without affecting myofibrillar protein synthesis J Physiol 588 pt 2 2010 341 351
22. D.W. West, G.W. Kujbida, D.R. Moore, and et al. Resistance exercise-induced increases in putative anabolic hormones do not enhance muscle protein synthesis or intracellular signalling in young men J Physiol 587 pt 21 2009 5239 5247
23. M.J. Fedele, C.H. Lang, and P.A. Farrell Immunization against IGF-I prevents increases in protein synthesis in diabetic rats after resistance exercise Am J Physiol Endocrinol Metab 280 6 2001 E877 E885
24. E.E. Spangenburg, D. Le Roith, C.W. Ward, and S.C. Bodine A functional insulin-like growth factor receptor is not necessary for load-induced skeletal muscle hypertrophy J Physiol 586 1 2008 283 291
25. D.L. Hamilton, A. Philp, M.G. MacKenzie, and K. Baar A limited role for PI(3,4,5)P3 regulation in controlling skeletal muscle mass in response to resistance exercise PLoS One 5 7 2010 e11624
26. S.M. Phillips, E.I. Glover, and M.J. Rennie Alterations of protein turnover underlying disuse atrophy in human skeletal muscle J Appl Physiol (1985) 107 3 2009 645 654
27. M.L. Cunningham A mouse is not a rat is not a human: species differences exist Toxicol Sci 70 2 2002 157 158
28. P.L. Greenhaff, L.G. Karagounis, N. Peirce, and et al. Disassociation between the effects of amino acids and insulin on signaling, ubiquitin ligases, and protein turnover in human muscle Am J Physiol Endocrinol Metab 295 3 2008 E595 E604
29. J. Trommelen, B. Groen, H. Hamer, L.C. de Groot, and L.J. van Loon Mechanisms in endocrinology: exogenous insulin does not increase muscle protein synthesis rate when administrated systemically: a systematic review Eur J Endocrinol 173 1 2015 R25 R34
30. T. Kvorning, M. Andersen, K. Brixen, and K. Madsen 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 6 2006 E1325 E1332
31. E.T. Schroeder, M. Villanueva, D.D. West, and S.M. Phillips Are acute post-resistance exercise increases in testosterone, growth hormone, and IGF-1 necessary to stimulate skeletal muscle anabolism and hypertrophy? Med Sci Sports Exerc 45 11 2013 2044 2051
32. D.W.D. West, N.A. Burd, T.A. Churchward-Venne, and et al. Sex-based comparisons of myofibrillar protein synthesis after resistance exercise in the fed state J Appl Physiol 112 11 2012 1805 1813
33. D.W. West, N.A. Burd, J.E. Tang, and et al. 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 1 2010 60 67
34. K.G. Foster, and D.C. Fingar Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony J Biol Chem 285 19 2010 14071 14077
35. M. Laplante, and D.M. Sabatini mTOR signaling in growth control and disease Cell 149 2 2012 274 293
36. K. Inoki, Y. Li, T. Xu, and K.L. Guan Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling Genes Dev 17 15 2003 1829 1834
37. K. Inoki, T. Zhu, and K.L. Guan TSC2 mediates cellular energy response to control cell growth and survival Cell 115 5 2003 577 590
38. D.M. Gwinn, D.B. Shackelford, D.F. Egan, and et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint Mol Cell 30 2 2008 214 226
39. K. Inoki, Y. Li, T. Zhu, J. Wu, and K.L. Guan TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling Nat Cell Biol 4 9 2002 648 657
40. E. Vander Haar, S.I. Lee, S. Bandhakavi, T.J. Griffin, and D.H. Kim Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40 Nat Cell Biol 9 3 2007 316 323
41. J.W. Hershey Translational control in mammalian cells Annu Rev Biochem 60 1991 717 755
42. C.J. Richardson, M. Broenstrup, D.C. Fingar, and et al. SKAR is a specific target of S6 kinase 1 in cell growth control Curr Biol 14 17 2004 1540 1549
43. X. Wang, W. Li, M. Williams, N. Terada, D.R. Alessi, and C.G. Proud Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase EMBO J 20 16 2001 4370 4379
44. A.C. Gingras, S.P. Gygi, B. Raught, and et al. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism Genes Dev 13 11 1999 1422 1437
45. M. Laplante, and D.M. Sabatini Regulation of mTORC1 and its impact on gene expression at a glance J Cell Sci 126 pt 8 2013 1713 1719
46. C. Gkogkas, N. Sonenberg, and M. Costa-Mattioli Translational control mechanisms in long-lasting synaptic plasticity and memory J Biol Chem 285 42 2010 31913 31917
47. R.J. Dowling, I. Topisirovic, B.D. Fonseca, and N. Sonenberg Dissecting the role of mTOR: lessons from mTOR inhibitors Biochim Biophys Acta 1804 3 2010 433 439
48. M. Laplante, and D.M. Sabatini mTOR signaling at a glance J Cell Sci 122 pt 20 2009 3589 3594
49. J.L. Areta, L.M. Burke, M.L. Ross, and et al. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis J Physiol 591 pt 9 2013 2319 2331
50. D.R. Moore, M.J. Robinson, J.L. Fry, and et al. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men Am J Clin Nutr 89 1 2009 161 168
51. T.A. Churchward-Venne, N.A. Burd, C.J. Mitchell, and et al. Supplementation of a suboptimal protein dose with leucine or essential amino acids: effects on myofibrillar protein synthesis at rest and following resistance exercise in men J Physiol 590 pt 11 2012 2751 2765
52. C.J. Mitchell, T.A. Churchward-Venne, D.W. West, and et al. Resistance exercise load does not determine training-mediated hypertrophic gains in young men J Appl Physiol (1985) 113 1 2012 71 77
53. K. Baar, and K. Esser Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise Am J Physiol 276 1 pt 1 1999 C120 C127
54. S.C. Bodine, T.N. Stitt, M. Gonzalez, and et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo Nat Cell Biol 3 11 2001 1014 1019
55. C.A. Goodman, J.W. Frey, D.M. Mabrey, and et al. The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth J Physiol 589 pt 22 2011 5485 5501
56. M.J. Drummond, C.S. Fry, E.L. Glynn, and et al. Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis J Physiol Lond 587 7 2009 1535 1546
57. D.M. Gundermann, D.K. Walker, P.T. Reidy, and et al. Activation of mTORC1 signaling and protein synthesis in human muscle following blood flow restriction exercise is inhibited by rapamycin Am J Physiol Endocrinol Metab 306 10 2014 E1198 E1204
58. A.Y. Choo, S.O. Yoon, S.G. Kim, P.P. Roux, and J. Blenis Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation Proc Natl Acad Sci USA 105 45 2008 17414 17419
59. E.I. Glover, S.M. Phillips, B.R. Oates, and et al. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion J Physiol 586 pt 24 2008 6049 6061
60. P.J. Atherton, N.J. Szewczyk, A. Selby, and et al. Cyclic stretch reduces myofibrillar protein synthesis despite increases in FAK and anabolic signalling in L6 cells J Physiol 587 pt 14 2009 3719 3727
61. S.E. Gordon, M. Fluck, and F.W. Booth Selected contribution: skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent J Appl Physiol (1985) 90 3 2001 1174 1183 discussion 1165
62. M. Fluck, J.A. Carson, S.E. Gordon, A. Ziemiecki, and F.W. Booth Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle Am J Physiol 277 1 pt 1 1999 C152 C162
63. M.D. de Boer, A. Selby, P. Atherton, and et al. The temporal responses of protein synthesis, gene expression and cell signalling in human quadriceps muscle and patellar tendon to disuse J Physiol 585 pt 1 2007 241 251
64. H. Crossland, A.A. Kazi, C.H. Lang, and et al. Focal adhesion kinase is required for IGF-I-mediated growth of skeletal muscle cells via a TSC2/mTOR/S6K1-associated pathway Am J Physiol Endocrinol Metab 305 2 2013 E183 E193
65. T.A. Hornberger, W.K. Chu, Y.W. Mak, J.W. Hsiung, S.A. Huang, and S. Chien The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle Proc Natl Acad Sci USA 103 12 2006 4741 4746
66. J.S. You, H.C. Lincoln, C.R. Kim, and et al. The role of diacylglycerol kinase zeta and phosphatidic acid in the mechanical activation of mammalian target of rapamycin (mTOR) signaling and skeletal muscle hypertrophy J Biol Chem 289 3 2014 1551 1563
67. C. McGlory, A. White, C. Treins, and et al. Application of the [gamma-32P] ATP kinase assay to study anabolic signaling in human skeletal muscle J Appl Physiol 116 5 2014 504 513
68. B.L. Jacobs, C.A. Goodman, and T.A. Hornberger The mechanical activation of mTOR signaling: an emerging role for late endosome/lysosomal targeting J Muscle Res Cell Motil 35 1 2014 11 21
69. B.L. Jacobs, C.A. Goodman, and T.A. Hornberger The mechanical activation of mTOR signaling: an emerging role for late endosome/lysosomal targeting J Muscle Res Cell Motil 35 1 2013 11 21
70. S.L. Wolin, and P. Walter Ribosome pausing and stacking during translation of a eukaryotic mRNA EMBO J 7 11 1988 3559 3569
71. T. Chaillou, T.J. Kirby, and J.J. McCarthy Ribosome biogenesis: emerging evidence for a central role in the regulation of skeletal muscle mass J Cell Physiol 229 11 2014 1584 1594
72. S.J. Mahoney, J.M. Dempsey, and J. Blenis Cell signaling in protein synthesis ribosome biogenesis and translation initiation and elongation Prog Mol Biol Transl Sci 90 2009 53 107
73. W.C. Merrick Eukaryotic protein synthesis: still a mystery J Biol Chem 285 28 2010 21197 21201
74. M.J. Drummond, C.S. Fry, E.L. Glynn, and et al. Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis J Physiol 587 pt 7 2009 1535 1546
75. T. Moss, F. Langlois, T. Gagnon-Kugler, and V. Stefanovsky A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis Cell Mol Life Sci 64 1 2007 29 49
76. M. Miyazaki, J.J. McCarthy, M.J. Fedele, and K.A. Esser Early activation of mTORC1 signalling in response to mechanical overload is independent of phosphoinositide 3-kinase/Akt signalling J Physiol 589 pt 7 2011 1831 1846
77. C.J. Mitchell, T.A. Churchward-Venne, G. Parise, and et al. Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men PLoS One 9 2 2014 e89431
78. B.E. Phillips, J.P. Williams, T. Gustafsson, and et al. Molecular networks of human muscle adaptation to exercise and age PLoS Genet 9 3 2013 e1003389
79. C.J. Mitchell, T.A. Churchward-Venne, L. Bellamy, G. Parise, S.K. Baker, and S.M. Phillips Muscular and systemic correlates of resistance training-induced muscle hypertrophy PLoS One 8 10 2013 e78636
80. I. Janssen Evolution of sarcopenia research Appl Physiol Nutr Metab 35 5 2010 707 712
81. I. Janssen The epidemiology of sarcopenia Clin Geriatr Med 27 3 2011 355 363
82. D.R. Moore, T.A. Churchward-Venne, O. Witard, and et al. Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men J Gerontol A Biol Sci Med Sci 70 1 2014 57 62
83. V. Kumar, A. Selby, D. Rankin, and et al. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men J Physiol 587 pt 1 2009 211 217
84. M.J. Drummond, R.L. Marcus, and P.C. Lastayo Targeting anabolic impairment in response to resistance exercise in older adults with mobility impairments: potential mechanisms and rehabilitation approaches J Aging Res 2012 2012 486930
85. C.S. Fry, M.J. Drummond, E.L. Glynn, and et al. Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis Skelet Muscle 1 1 2011 11
86. L. Breen, K.A. Stokes, T.A. Churchward-Venne, and et al. Two weeks of reduced activity decreases leg lean mass and induces "anabolic resistance" of myofibrillar protein synthesis in healthy elderly J Clin Endocrinol Metab 98 6 2013 2604 2612
87. B.T. Wall, M.L. Dirks, and L.J. van Loon Skeletal muscle atrophy during short-term disuse: implications for age-related sarcopenia Ageing Res Rev 12 4 2013 898 906
88. C. Suetta, L.G. Hvid, L. Justesen, and et al. Effects of aging on human skeletal muscle after immobilization and retraining J Appl Physiol (1985) 107 4 2009 1172 1180
89. M.L. Dirks, B.T. Wall, R. Nilwik, D.H. Weerts, L.B. Verdijk, and L.J. van Loon Skeletal muscle disuse atrophy is not attenuated by dietary protein supplementation in healthy older men J Nutr 144 8 2014 1196 1203
90. B.T. Wall, T. Snijders, J.M. Senden, and et al. Disuse impairs the muscle protein synthetic response to protein ingestion in healthy men J Clin Endocrinol Metab 98 12 2013 4872 4881
91. M.B. Reid, A.R. Judge, and S.C. Bodine CrossTalk opposing view: the dominant mechanism causing disuse muscle atrophy is proteolysis J Physiol 592 pt 24 2014 5345 5347
92. S.M. Phillips, and C. McGlory Rebuttal from Stuart M. Phillips and Chris McGlory J Physiol 592 pt 24 2014 5349
93. S.M. Phillips, and C. McGlory CrossTalk proposal: the dominant mechanism causing disuse muscle atrophy is decreased protein synthesis J Physiol 592 pt 24 2014 5341 5343
94. M. Bartoli, and I. Richard Calpains in muscle wasting Int J Biochem Cell Biol 37 10 2005 2115 2133
95. M. Salem, J. Nath, C.E. Rexroad, J. Killefer, and J. Yao Identification and molecular characterization of the rainbow trout calpains (Capn1 and Capn2): their expression in muscle wasting during starvation Comp Biochem Physiol B Biochem Mol Biol 140 1 2005 63 71
96. S.C. Bodine, and L.M. Baehr Skeletal muscle atrophy and the E3 ubiquitin ligases MuRF1 and MAFbx/atrogin-1 Am J Physiol Endocrinol Metab 307 6 2014 E469 E484
97. A.J. Murton, D. Constantin, and P.L. Greenhaff The involvement of the ubiquitin proteasome system in human skeletal muscle remodelling and atrophy Biochim Biophys Acta 1782 12 2008 730 743
98. E. Pasini, R. Aquilani, F.S. Dioguardi, G. D'Antona, M. Gheorghiade, and H. Taegtmeyer Hypercatabolic syndrome: molecular basis and effects of nutritional supplements with amino acids Am J Cardiol 101 11A 2008 11E 15E
99. A. Csibi, M.P. Leibovitch, K. Cornille, L.A. Tintignac, and S.A. Leibovitch MAFbx/atrogin-1 controls the activity of the initiation factor eIF3-f in skeletal muscle atrophy by targeting multiple C-terminal lysines J Biol Chem 284 7 2009 4413 4421
100. Csibi A., Cornille K., Leibovitch M.P. et al., The translation regulatory subunit eIF3f controls the kinase-dependent mTOR signaling required for muscle differentiation and hypertrophy in mouse. PLoS One, 2010, 5(2) e8994.