Introduction
Les facteurs physiologiques affectant la réactivité des traits à l’entrainement physique (comme le changement des capacités aérobie, la force ou la croissance musculaire) ont gagné récemment l’intérêt des chercheurs. D’un point de vue historique, cet intérêt a largement été inspiré par la célèbre étude HERITAGE, où les changements de la V02max auraient varié de pratiquement aucun gain à une augmentation de 100%, après un entrainement en endurance de 20 semaines, chez des sujets sédentaires.
Aussi, Van Etten et al (1994), examine la réponse musculaire hypertrophique chez des individus classés comme « svelte » (slender : bas répondeur) ou « robuste » (solid : haut répondeur), après un entrainement physique en résistance de 12 semaines. Les sujets ont été classés selon leur indice de masse sans gras (FFMI), déterminé par mesure des plis de peau, pour lequel les sujets sveltes ont eu des valeurs inférieures comparés aux sujets robustes. Les auteurs rapportent que les sujets robustes présentaient une augmentation significative de la masse sans gras après un entrainement physique, alors que les sujets sveltes n’expérimentaient en pratique aucun gain.
Plus d’une décennie après, Bamman et al. (2007) rapportent qu’il existe différents biomarqueurs dans les muscles squelettiques entre les groupes de réponse hypertrophique du muscle squelettique. Les « répondeurs extrêmes » (ici, haut répondeur), présentent une importante augmentation de la section transversale de leur fibre musculaire, comparé au « non répondeur » (ici, bas répondeur), après un entrainement physique. Les hauts répondeurs (HR) ont également exprimé des taux plus élevés de variantes d'ARNm du facteur de croissance 1 ressemblant à l’insuline (IGF-1) du muscle squelettique, ainsi qu'un ARNm indicatif de la différenciation des cellules satellites par rapport aux sujets bas répondeurs (BR) après l’entrainement en résistance.
Le but de cette revue est de résumer les résultats de ces recherches. Etant donné que seules quelques études ont examiné les biomarqueurs musculaires exprimés différentiellement entre les patients ayant une réponse faible et élevée, nous proposons également des facteurs moins examinés qui pourraient contribuer aux réactions hypertrophiques différentielles qui se produisent pendant l'entraînement en résistance et qui devraient être mieux étudiés à l’avenir.
Un bref rappel général des mécanismes facilitant l’hypertrophie
L’hypertrophie musculaire en réponse à des exercices en résistance est influencé par l’interaction de nombreux facteurs extrinsèques et intrinsèques. Parmi les facteurs intrinsèques, nous retiendrons ici 3 facteurs majeurs :
Le tableau 1 regroupe différentes études cherchant à définir les caractéristiques physiologiques de BR et des HR.
Les facteurs physiologiques affectant la réactivité des traits à l’entrainement physique (comme le changement des capacités aérobie, la force ou la croissance musculaire) ont gagné récemment l’intérêt des chercheurs. D’un point de vue historique, cet intérêt a largement été inspiré par la célèbre étude HERITAGE, où les changements de la V02max auraient varié de pratiquement aucun gain à une augmentation de 100%, après un entrainement en endurance de 20 semaines, chez des sujets sédentaires.
Aussi, Van Etten et al (1994), examine la réponse musculaire hypertrophique chez des individus classés comme « svelte » (slender : bas répondeur) ou « robuste » (solid : haut répondeur), après un entrainement physique en résistance de 12 semaines. Les sujets ont été classés selon leur indice de masse sans gras (FFMI), déterminé par mesure des plis de peau, pour lequel les sujets sveltes ont eu des valeurs inférieures comparés aux sujets robustes. Les auteurs rapportent que les sujets robustes présentaient une augmentation significative de la masse sans gras après un entrainement physique, alors que les sujets sveltes n’expérimentaient en pratique aucun gain.
Plus d’une décennie après, Bamman et al. (2007) rapportent qu’il existe différents biomarqueurs dans les muscles squelettiques entre les groupes de réponse hypertrophique du muscle squelettique. Les « répondeurs extrêmes » (ici, haut répondeur), présentent une importante augmentation de la section transversale de leur fibre musculaire, comparé au « non répondeur » (ici, bas répondeur), après un entrainement physique. Les hauts répondeurs (HR) ont également exprimé des taux plus élevés de variantes d'ARNm du facteur de croissance 1 ressemblant à l’insuline (IGF-1) du muscle squelettique, ainsi qu'un ARNm indicatif de la différenciation des cellules satellites par rapport aux sujets bas répondeurs (BR) après l’entrainement en résistance.
Le but de cette revue est de résumer les résultats de ces recherches. Etant donné que seules quelques études ont examiné les biomarqueurs musculaires exprimés différentiellement entre les patients ayant une réponse faible et élevée, nous proposons également des facteurs moins examinés qui pourraient contribuer aux réactions hypertrophiques différentielles qui se produisent pendant l'entraînement en résistance et qui devraient être mieux étudiés à l’avenir.
Un bref rappel général des mécanismes facilitant l’hypertrophie
L’hypertrophie musculaire en réponse à des exercices en résistance est influencé par l’interaction de nombreux facteurs extrinsèques et intrinsèques. Parmi les facteurs intrinsèques, nous retiendrons ici 3 facteurs majeurs :
- La régulation à la hausse de la synthèse protéique myofibrillaire et globale des protéines musculaires (MyoPS et MPS) durant la période post exercice. Celle-ci est largement modulée via la signalisation de mTORC1 (mammalian target of rapamycin complex 1).
- La réduction de la protéolyse dans la période post exercice
- Une augmentation de l’addition myonucléaire par médiation des cellules satellites.
Le tableau 1 regroupe différentes études cherchant à définir les caractéristiques physiologiques de BR et des HR.
Il est cependant nécessaire que les études utilisent des mesures différentes, avec des modalités d’entrainement différentes, sur des populations différentes. Néanmoins, les résultats suivants permettent d’identifier les BR et les HR :
Différences physiologiques entre bas et hauts répondeurs hypertrophiques
Étant donné que les ribosomes catalysent la MyoPS et la MPS, et que les augmentations répétées de ces taux de synthèse après l'exercice facilitent vraisemblablement la croissance musculaire, une augmentation du contenu en ribosomes des fibres musculaires pendant les périodes d'entraînement en résistance est apparemment avantageuse pour l'hypertrophie des muscles squelettiques. Bamman’s (2016) décrit que le contenu en ribosome augmentait d’environ 30% chez des sujets mâles plus âgés, qui était haut répondeur (+83% type II fCSA) alors que qu’aucun changement du contenu en ribosome n’a été observé chez les sujets bas répondeurs.
Les futures directions de recherche examinant quels facteurs pourraient contribuer à des réponses différentielles à l’hypertrophie
De nombreux facteurs physiologiques rentrent donc en compte dans la différenciation entre bas et haut répondeur hypertrophique, pouvant prédisposer tel ou tel individu à gagner en volume ou en force musculaire, et donc à performer. Les auteurs suggèrent une liste non exhaustive des différentes orientations intéressantes pour de futures recherches sur le sujet, parmi lesquelles :
Mots clé : hypertrophie, biogénèse des ribosomes, cellules satellites, microARN, IGF-1, récepteur androgène.
Article original : Michael D. Roberts, Cody T. Haun, Christopher B. Mobley, Petey W. Mumford, Matthew A. Romero, Paul A. Roberson, Christopher G. Vann and John J. McCarthy. Physiological Differences Between Low Versus High Skeletal Muscle Hypertrophic Responders to Resistance Exercise Training: Current Perspectives and Future Research Directions. Front. Physiol. 9:834. doi: 10.3389/fphys.2018.00834
Référence :
Armstrong, D. D., and Esser, K. A. (2005). Wnt/beta-catenin signaling activates growth-control genes during overload-induced skeletal muscle hypertrophy. Am. J. Physiol. Cell Physiol. 289, C853–C859. doi: 10.1152/ajpcell.00093.2005
Atkinson, G., and Batterham, A. M. (2015). True and false interindividual di erences in the physiological response to an intervention. Exp. Physiol. 100, 577–588. doi: 10.1113/EP085070
Baar, K., and Esser, K. (1999). Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am. J. Physiol. 276, C120–C127.
Bamman, M. M., Petrella, J. K., Kim, J. S., Mayhew, D. L., and Cross, J. M. (2007). Cluster analysis tests the importance of myogenic gene expression during myofiber hypertrophy in humans. J. Appl. Physiol. 102, 2232–2239. doi: 10.1152/japplphysiol.00024.2007
Bellamy, L. M., Joanisse, S., Grubb, A., Mitchell, C. J., Mckay, B. R., Phillips, S. M., et al. (2014). The acute satellite cell response and skeletal muscle hypertrophy following resistance training. PLoS One 9:e109739. doi: 10.1371/journal.pone. 0109739
Betz, C., and Hall, M. N. (2013). Where is mTOR and what is it doing there? J. Cell Biol. 203, 563–574. doi: 10.1083/jcb.201306041
Bistrian, B. R., Schwartz, J., and Istfan, N. W. (1992). Cytokines, muscle proteolysis, and the catabolic response to infection and inflammation. Proc. Soc. Exp. Biol. Med. 200, 220–223. doi: 10.3181/00379727-200-43423
Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., et al. (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3, 1014– 1019. doi: 10.1038/ncb1101-1014
Bond, P. (2016). Regulation of mTORC1 by growth factors, energy status, amino acids and mechanical stimuli at a glance. J. Int. Soc. Sports Nutr. 13:8. doi: 10.1186/s12970-016-0118-y
Bouchard, C., and Rankinen, T. (2001). Individual di erences in response to regular physical activity. Med. Sci. Sports Exerc. 33, S446–S451. doi: 10.1097/ 00005768- 200106001- 00013
Bouchard, C., Sarzynski, M. A., Rice, T. K., Kraus, W. E., Church, T. S., Sung, Y. J., et al. (2011). Genomic predictors of the maximal O2 uptake response to standardized exercise training programs. J. Appl. Physiol. 110, 1160–1170. doi: 10.1152/japplphysiol.00973.2010
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. L., Phillips, B. E., Szewczyk, N. J., et al. (2017). A novel D2O tracer method to quantify RNA turnover as a biomarker of de novo ribosomal biogenesis, in vitro, in animal models, and in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 313, E681–E689. doi: 10.1152/ajpendo.00157.2017
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. N., Szewczyk, N. J., Greenha , P. L., et al. (2015). Skeletal muscle hypertrophy adaptations predominate in the early stages of resistance exercise training, matching deuterium oxide-derived measures of muscle protein synthesis and mechanistic target of rapamycin complex 1 signaling. FASEB J. 29, 4485–4496. doi: 10.1096/ fj.15- 273755
Campbell, B., Kreider, R. B., Ziegenfuss, T., La Bounty, P., Roberts, M., Burke, D., et al. (2007). International society of sports nutrition position stand: protein and exercise. J. Int. Soc. Sports Nutr. 4:8. doi: 10.1186/1550-2783-4-8
Chaillou, T., Kirby, T. J., and Mccarthy, J. J. (2014). Ribosome biogenesis: emerging evidence for a central role in the regulation of skeletal muscle mass. J. Cell. Physiol. 229, 1584–1594. doi: 10.1002/jcp.24604
Chandler, P. N., Liu, C., Von Walden, F., and Nader, G. A. (2017). Proteasome activity is required for ribosomal DNA transcription and muscle hypertrophy. FASEB J. 31:lb782–lb782.
Charbonneau, D. E., Hanson, E. D., Ludlow, A. T., Delmonico, M. J., Hurley, B. F., and Roth, S. M. (2008). ACE genotype and the muscle hypertrophic and strength responses to strength training. Med. Sci. Sports Exerc. 40, 677–683. doi: 10.1249/MSS.0b013e318161eab9
Cheek, D. B., Holt, A. B., Hill, D. E., and Talbert, J. L. (1971). Skeletal muscle cell mass and growth: the concept of the deoxyribonucleic acid unit. Pediatr. Res. 5, 329–334. doi: 10.1203/00006450-197107000-00004
Clarkson, P. M., Devaney, J. M., Gordish-Dressman, H., Thompson, P. D., Hubal, M. J., Urso, M., et al. (2005). ACTN3 genotype is associated with increases in muscle strength in response to resistance training in women. J. Appl. Physiol. 99, 154–163. doi: 10.1152/japplphysiol.01139.2004
Clemente, C. F., Xavier-Neto, J., Dalla Costa, A. P., Consonni, S. R., Antunes, J. E., Rocco, S. A., et al. (2012). Focal adhesion kinase governs cardiac concentric hypertrophic growth by activating the AKT and mTOR pathways. J. Mol. Cell. Cardiol 52, 493–501. doi: 10.1016/j.yjmcc.2011.10.015
Crameri, R. M., Langberg, H., Magnusson, P., Jensen, C. H., Schroder, H. D., Olesen, J. L., et al. (2004). Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J. Physiol. 558, 333–340. doi: 10.1113/jphysiol.2004.061846
Dalbo, V. J., Roberts, M. D., Hassell, S., and Kerksick, C. M. (2013). E ects of pre-exercise feeding on serum hormone concentrations and biomarkers of
myostatin and ubiquitin proteasome pathway activity. Eur. J. Nutr. 52, 477–487.
doi: 10.1007/s00394-012-0349-x
Dalbo, V. J., Roberts, M. D., Sunderland, K. L., Poole, C. N., Stout, J. R., Beck, T. W.,
et al. (2011). Acute loading and aging e ects on myostatin pathway biomarkers in human skeletal muscle after three sequential bouts of resistance exercise. J. Gerontol. A Biol. Sci. Med. Sci. 66, 855–865. doi: 10.1093/gerona/glr091
Damas, F., Libardi, C. A., Ugrinowitsch, C., Vechin, F. C., Lixandrao, M. E., Snijders, T., et al. (2018). Early- and later-phases satellite cell responses and myonuclear content with resistance training in young men. PLoS One 13:e0191039. doi: 10.1371/journal.pone.0191039
Damas, F., Phillips, S. M., Libardi, C. A., Vechin, F. C., Lixandrao, M. E., Jannig, P. R., et al. (2016). Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J. Physiol. 594, 5209–5222. doi: 10.1113/JP272472
Davidsen, P. K., Gallagher, I. J., Hartman, J. W., Tarnopolsky, M. A., Dela, F., Helge, J. W., et al. (2011). High responders to resistance exercise training demonstrate di erential regulation of skeletal muscle microRNA expression. J. Appl. Physiol. 110, 309–317. doi: 10.1152/japplphysiol.00901.2010
De Larichaudy, J., Zu erli, A., Serra, F., Isidori, A. M., Naro, F., Dessalle, K., et al. (2012). TNF-alpha- and tumor-induced skeletal muscle atrophy involves sphingolipid metabolism. Skelet. Muscle 2:2. doi: 10.1186/2044-5040-2-2
Dennis, R. A., Zhu, H., Kortebein, P. M., Bush, H. M., Harvey, J. F., Sullivan, D. H., et al. (2009). Muscle expression of genes associated with inflammation, growth, and remodeling is strongly correlated in older adults with resistance training outcomes. Physiol. Genomics 38, 169–175. doi: 10.1152/physiolgenomics.00056. 2009
Drummond, M. J., Fry, C. S., Glynn, E. L., Dreyer, H. C., Dhanani, S., Timmerman, K. L., et al. (2009). Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis. J. Physiol. 587, 1535–1546. doi: 10.1113/jphysiol.2008.163816
Egner, I. M., Bruusgaard, J. C., and Gundersen, K. (2016). Satellite cell depletion prevents fiber hypertrophy in skeletal muscle. Development 143, 2898–2906. doi: 10.1242/dev.134411
Ferrando, A. A., Tipton, K. D., Doyle, D., Phillips, S. M., Cortiella, J., and Wolfe, R. R. (1998). Testosterone injection stimulates net protein synthesis but not tissue amino acid transport. Am. J. Physiol. 275, E864–E871. doi: 10.1152/ ajpendo.1998.275.5.E864
Figueiredo, V. C., Caldow, M. K., Massie, V., Markworth, J. F., Cameron- Smith, D., and Blazevich, A. J. (2015). Ribosome biogenesis adaptation in resistance training-induced human skeletal muscle hypertrophy. Am. J. Physiol. Endocrinol. Metab. 309, E72–E83. doi: 10.1152/ajpendo.00050.2015
Fluck, M., Carson, J. A., Gordon, S. E., Ziemiecki, A., and Booth, F. W. (1999). Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am. J. Physiol. 277, C152–C162. doi: 10.1152/ajpcell.1999.277.1.C152
Franchi, M. V., Longo, S., Mallinson, J., Quinlan, J. I., Taylor, T., Greenha , P. L., et al. (2018a). Muscle thickness correlates to muscle cross-sectional area in the assessment of strength training-induced hypertrophy. Scand. J. Med. Sci. Sports 28, 846–853. doi: 10.1111/sms.12961
Franchi, M. V., Ruoss, S., Valdivieso, P., Mitchell, K. W., Smith, K., Atherton, P. J., et al. (2018b). Regional regulation of focal adhesion kinase after concentric and eccentric loading is related to remodelling of human skeletal muscle. Acta Physiol. 223:e13056. doi: 10.1111/apha.13056
Fry, C. S., Kirby, T. J., Kosmac, K., Mccarthy, J. J., and Peterson, C. A. (2017). Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy. Cell Stem Cell 20, 56–69. doi: 10.1016/j. stem.2016.09.010
Fry, C. S., Lee, J. D., Jackson, J. R., Kirby, T. J., Stasko, S. A., Liu, H., et al. (2014). Regulation of the muscle fiber microenvironment by activated satellite cells during hypertrophy. FASEB J. 28, 1654–1665. doi: 10.1096/fj.13-239426
Gao, S., Durstine, J. L., Koh, H. J., Carver, W. E., Frizzell, N., and Carson, J. A. (2017). Acute myotube protein synthesis regulation by IL-6-related cytokines. Am. J. Physiol. Cell Physiol. 313, C487–C500. doi: 10.1152/ajpcell.00112.2017
Gauthier, G. F., and Mason-Savas, A. (1993). Ribosomes in the skeletal muscle filament lattice. Anat. Rec. 237, 149–156. doi: 10.1002/ar.1092370202
Gavin, T. P., Drew, J. L., Kubik, C. J., Pofahl, W. E., and Hickner, R. C. (2007). Acute resistance exercise increases skeletal muscle angiogenic growth factor expression. Acta Physiol. 191, 139–146. doi: 10.1111/j.1748-1716.2007. 01723.x
Gibbons, J. G., Branco, A. T., Yu, S., and Lemos, B. (2014). Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans. Nat. Commun. 5:4850. doi: 10.1038/ncomms 5850
Goodman, C. A., Dietz, J. M., Jacobs, B. L., Mcnally, R. M., You, J. S., and Hornberger, T. A. (2015). Yes-associated protein is up-regulated by mechanical overload and is su cient to induce skeletal muscle hypertrophy. FEBS Lett. 589, 1491–1497. doi: 10.1016/j.febslet.2015.04.047
Griggs, R. C., Kingston, W., Jozefowicz, R. F., Herr, B. E., Forbes, G., and Halliday, D. (1989). E ect of testosterone on muscle mass and muscle protein synthesis. J. Appl. Physiol. 66, 498–503. doi: 10.1152/jappl.1989.66.1.498
Groennebaek, T., and Vissing, K. (2017). Impact of resistance training on skeletal muscle mitochondrial biogenesis, content, and function. Front. Physiol. 8:713. doi: 10.3389/fphys.2017.00713
Guth, L. M., and Roth, S. M. (2013). Genetic influence on athletic performance. Curr. Opin. Pediatr. 25, 653–658. doi: 10.1097/MOP.0b013e3283659087
Habets, P. E., Franco, D., Ruijter, J. M., Sargeant, A. J., Pereira, J. A., and Moorman, A. F. (1999). RNA content di ers in slow and fast muscle fibers: implications for interpretation of changes in muscle gene expression. J. Histochem. Cytochem. 47, 995–1004. doi: 10.1177/002215549904700803
Haddad, F., Zaldivar, F., Cooper, D. M., and Adams, G. R. (2005). IL-6-induced skeletal muscle atrophy. J. Appl. Physiol. 98, 911–917. doi: 10.1152/japplphysiol. 01026.2004
Hall, Z. W., and Ralston, E. (1989). Nuclear domains in muscle cells. Cell 59, 771–772. doi: 10.1016/0092-8674(89)90597-7
Hameed, M., Orrell, R. W., Cobbold, M., Goldspink, G., and Harridge, S. D. (2003). Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J. Physiol. 547, 247–254. doi: 10.1113/jphysiol. 2002.032136
Hammond, H. K., White, F. C., Bhargava, V., and Shabetai, R. (1992). Heart size and maximal cardiac output are limited by the pericardium. Am. J. Physiol. 263, H1675–H1681. doi: 10.1152/ajpheart.1992.263.6.H1675
Hikida, R. S., Staron, R. S., Hagerman, F. C., Walsh, S., Kaiser, E., Shell, S., et al. (2000). E ects of high-intensity resistance training on untrained older men. II. Muscle fiber characteristics and nucleo-cytoplasmic relationships. J. Gerontol. A Biol. Sci. Med. Sci. 55, B347–B354.
Hjorth, M., Norheim, F., Meen, A. J., Pourteymour, S., Lee, S., Holen, T., et al. (2015). The e ect of acute and long-term physical activity on extracellular matrix and serglycin in human skeletal muscle. Physiol. Rep. 3:e12473. doi: 10.14814/phy2.12473
Hornberger, T. A. (2011). Mechanotransduction and the regulation of mTORC1 signaling in skeletal muscle. Int. J. Biochem. Cell Biol. 43, 1267–1276. doi: 10.1016/j.biocel.2011.05.007
Hornberger, T. A., Chu, W. K., Mak, Y. W., Hsiung, J. W., Huang, S. A., and Chien, S. (2006). The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 103, 4741–4746. doi: 10.1073/pnas.0600678103
Hulmi, J. J., Tannerstedt, J., Selanne, H., Kainulainen, H., Kovanen, V., and Mero, A. A. (2009). Resistance exercise with whey protein ingestion a ects mTOR signaling pathway and myostatin in men. J. Appl. Physiol. 106, 1720–1729. doi: 10.1152/japplphysiol.00087.2009
Ingjer, F. (1979). Capillary supply and mitochondrial content of di erent skeletal muscle fiber types in untrained and endurance-trained men. A histochemical and ultrastructural study. Eur. J. Appl. Physiol. Occup. Physiol. 40, 197–209. doi: 10.1007/BF00426942
Jiang, M., Ma, Y., Chen, C., Fu, X., Yang, S., Li, X., et al. (2009). Androgen- responsive gene database: integrated knowledge on androgen-responsive genes. Mol. Endocrinol. 23, 1927–1933. doi: 10.1210/me.2009-0103
Kadi, F., Eriksson, A., Holmner, S., and Thornell, L. E. (1999). E ects of anabolic steroids on the muscle cells of strength-trained athletes. Med. Sci. Sports Exerc. 31, 1528–1534. doi: 10.1097/00005768-199911000-00006
Kadi, F., Schjerling, P., Andersen, L. L., Charifi, N., Madsen, J. L., Christensen, L. R., et al. (2004). The e ects of heavy resistance training and detraining on satellite cells in human skeletal muscles. J. Physiol. 558, 1005–1012. doi: 10.1113/jphysiol.2004.065904
Kerksick, C. M., Kreider, R. B., and Willoughby, D. S. (2010). Intramuscular adaptations to eccentric exercise and antioxidant supplementation. Amino Acids 39, 219–232. doi: 10.1007/s00726-009-0432-7
Kerksick, C. M., Roberts, M. D., Dalbo, V. J., Kreider, R. B., and Willoughby, D. S. (2013). Changes in skeletal muscle proteolytic gene expression after prophylactic supplementation of EGCG and NAC and eccentric damage. Food Chem. Toxicol. 61, 47–52. doi: 10.1016/j.fct.2013.01.026
Kim, J. S., Petrella, J. K., Cross, J. M., and Bamman, M. M. (2007). Load-mediated downregulation of myostatin mRNA is not su cient to promote myofiber hypertrophy in humans: a cluster analysis. J. Appl. Physiol. 103, 1488–1495. doi: 10.1152/japplphysiol.01194.2006
Knowles, O. E., Drinkwater, E. J., Urwin, C. S., Lamon, S., and Aisbett, B. (2018). Inadequate sleep and muscle strength: Implications for resistance training. J. Sci. Med. Sport. doi: 10.1016/j.jsams.2018.01.012 [Epub ahead of print].
Kostek, M. C., Delmonico, M. J., Reichel, J. B., Roth, S. M., Douglass, L., Ferrell, R. E., et al. (2005). Muscle strength response to strength training is influenced by insulin-like growth factor 1 genotype in older adults. J. Appl. Physiol. 98, 2147–2154. doi: 10.1152/japplphysiol.00817.2004
Krentz, J. R., Quest, B., Farthing, J. P., Quest, D. W., and Chilibeck, P. D. (2008). The e ects of ibuprofen on muscle hypertrophy, strength, and soreness during resistance training. Appl. Physiol. Nutr. Metab. 33, 470–475. doi: 10.1139/H08- 019
Kwon, I., Lee, Y., Cosio-Lima, L. M., Cho, J. Y., and Yeom, D. C. (2015). E ects of long-term resistance exercise training on autophagy in rat skeletal muscle of chloroquine-induced sporadic inclusion body myositis. J. Exerc. Nutr. Biochem. 19, 225–234. doi: 10.5717/jenb.2015.15090710
Li, X., Wang, S. J., Tan, S. C., Chew, P. L., Liu, L., Wang, L., et al. (2014). The A55T and K153R polymorphisms of MSTN gene are associated with the strength training-induced muscle hypertrophy among Han Chinese men. J. Sports Sci. 32, 883–891. doi: 10.1080/02640414.2013.865252
Lindstrom, M., and Thornell, L. E. (2009). 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. 132, 141–157. doi: 10.1007/s00418-009-0606-0
Louis, E., Raue, U., Yang, Y., Jemiolo, B., and Trappe, S. (2007). Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J. Appl. Physiol. 103, 1744–1751. doi: 10.1152/ japplphysiol.00679.2007
Lueders, T. N., Zou, K., Huntsman, H. D., Meador, B., Mahmassani, Z., Abel, M., et al. (2011). The alpha7beta1-integrin accelerates fiber hypertrophy and myogenesis following a single bout of eccentric exercise. Am. J. Physiol. Cell Physiol. 301, C938–C946. doi: 10.1152/ajpcell.00515.2010
Mackey, A. L., Esmarck, B., Kadi, F., Koskinen, S. O., Kongsgaard, M., Sylvestersen, A., et al. (2007). Enhanced satellite cell proliferation with resistance training in elderly men and women. Scand. J. Med. Sci. Sports 17, 34–42.
Mann, T. N., Lamberts, R. P., and Lambert, M. I. (2014). High responders and low responders: factors associated with individual variation in response to standardized training. Sports Med. 44, 1113–1124. doi: 10.1007/s40279-014- 0197- 3
Markworth, J. F., and Cameron-Smith, D. (2011). Prostaglandin F2&↵ stimulates PI3K/ERK/mTOR signaling and skeletal myotube hypertrophy. Am. J. Physiol. Cell Physiol. 300, C671–C682. doi: 10.1152/ajpcell.00549.2009
Masiero, E., and Sandri, M. (2010). Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles. Autophagy 6, 307–309. doi: 10.4161/auto. 6.2.11137
Mayhew, D. L., Kim, J. S., Cross, J. M., Ferrando, A. A., and Bamman, M. M. (2009). Translational signaling responses preceding resistance training- mediated myofiber hypertrophy in young and old humans. J. Appl. Physiol. 107, 1655–1662. doi: 10.1152/japplphysiol.91234.2008
McCall, G. E., Byrnes, W. C., Dickinson, A., Pattany, P. M., and Fleck, S. J. (1996). Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training. J. Appl. Physiol. 81, 2004–2012. doi: 10.1152/jappl.1996.81. 5.2004
McCarthy, J. J., and Esser, K. A. (2007). MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J. Appl. Physiol. 102, 306–313. doi: 10.1152/japplphysiol.00932.2006
McCarthy, J. J., Mula, J., Miyazaki, M., Erfani, R., Garrison, K., Farooqui, A. B., et al. (2011). E ective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138, 3657–3666. doi: 10.1242/dev.068858
Mitchell, C. J., Churchward-Venne, T. A., Bellamy, L., Parise, G., Baker, S. K., and Phillips, S. M. (2013). Muscular and systemic correlates of resistance training- induced muscle hypertrophy. PLoS One 8:e78636. doi: 10.1371/journal.pone. 0078636
Mitchell, C. J., Churchward-Venne, T. A., Parise, G., Bellamy, L., Baker, S. K., Smith, K., et al. (2014). Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PLoS One 9:e89431. doi: 10.1371/journal.pone.0089431
Mitchell, C. J., Churchward-Venne, T. A., West, D. W., Burd, N. A., Breen, L., Baker, S. K., et al. (2012). Resistance exercise load does not determine training- mediated hypertrophic gains in young men. J. Appl. Physiol. 113, 71–77. doi: 10.1152/japplphysiol.00307.2012
Mobley, C. B., Fox, C. D., Thompson, R. M., Healy, J. C., Santucci, V., Kephart, W. C., et al. (2016). Comparative e ects of whey protein versus L-leucine on skeletal muscle protein synthesis and markers of ribosome biogenesis following resistance exercise. Amino Acids 48, 733–750. doi: 10.1007/s00726-015- 2121-z
Mobley, C. B., Haun, C. T., Roberson, P. A., Mumford, P. W., Kephart, W. C., Romero, M. A., et al. (2018a). Biomarkers associated with low, moderate, and high vastus lateralis muscle hypertrophy following 12 weeks of resistance training. PLoS One 13:e0195203. doi: 10.1371/journal.pone.01 95203
Mobley, C. B., Haun, C. T., Roberson, P. A., Mumford, P. W., Romero, M. A., Kephart, W. C., et al. (2017). E ects 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 9:E972. doi: 10.3390/nu9090972
Mobley, C. B., Holland, A. M., Kephart, W. C., Mumford, P. W., Lowery, R. P., Kavazis, A. N., et al. (2018b). Progressive resistance-loaded voluntary wheel running increases hypertrophy and di erentially a ects muscle protein synthesis, ribosome biogenesis, and proteolytic markers in rat muscle. J. Anim. Physiol. Anim. Nutr. 102, 317–329. doi: 10.1111/jpn.12691
Morissette, M. R., Cook, S. A., Buranasombati, C., Rosenberg, M. A., and Rosenzweig, A. (2009). Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt. Am. J. Physiol. Cell Physiol. 297, C1124–C1132. doi: 10.1152/ ajpcell.00043.2009
Munoz-Canoves, P., Scheele, C., Pedersen, B. K., and Serrano, A. L. (2013). Interleukin-6 myokine signaling in skeletal muscle: a double-edged sword? FEBS J. 280, 4131–4148. doi: 10.1111/febs.12338
Murach, K. A., Fry, C. S., Kirby, T. J., Jackson, J. R., Lee, J. D., White, S. H., et al. (2018). Starring or supporting role? Satellite cells and skeletal muscle fiber size regulation. Physiology 33, 26–38. doi: 10.1152/physiol.00019.2017
Nader, G. A., Mcloughlin, T. J., and Esser, K. A. (2005). mTOR function in skeletal muscle hypertrophy: increased ribosomal RNA via cell cycle regulators. Am. J. Physiol. Cell Physiol. 289, C1457–C1465. doi: 10.1152/ajpcell.00165. 2005
Nakada, S., Ogasawara, R., Kawada, S., Maekawa, T., and Ishii, N. (2016). Correlation between ribosome biogenesis and the magnitude of hypertrophy in overloaded skeletal muscle. PLoS One 11:e0147284. doi: 10.1371/journal.pone. 0147284
Nederveen, J. P., Joanisse, S., Seguin, C. M., Bell, K. E., Baker, S. K., Phillips, S. M., et al. (2015). The e ect of exercise mode on the acute response of satellite cells in old men. Acta Physiol. 215, 177–190. doi: 10.1111/apha.12601
Nederveen, J. P., Snijders, T., Joanisse, S., Wavell, C. G., Mitchell, C. J., Johnston, L. M., et al. (2017). Altered muscle satellite cell activation following 16 wk of resistance training in young men. Am. J. Physiol. Regul. Integr. Comp. Physiol. 312, R85–R92. doi: 10.1152/ajpregu.00221.2016
Norrby, M., and Tagerud, S. (2010). Mitogen-activated protein kinase-activated protein kinase 2 (MK2) in skeletal muscle atrophy and hypertrophy. J. Cell. Physiol. 223, 194–201. doi: 10.1002/jcp.22023
Ogasawara, R., Akimoto, T., Umeno, T., Sawada, S., Hamaoka, T., and Fujita, S. (2016). MicroRNA expression profiling in skeletal muscle reveals di erent regulatory patterns in high and low responders to resistance training. Physiol. Genomics 48, 320–324. doi: 10.1152/physiolgenomics.00124. 2015
Ogborn, D., and Schoenfeld, B. J. (2014). The role of fiber types in muscle hypertrophy: implications for loading strategies. Strength Cond. J. 36, 20–25. doi: 10.1519/SSC.0000000000000030
O’Reilly, C., Mckay, B., Phillips, S., Tarnopolsky, M., and Parise, G. (2008). Hepatocyte growth factor (HGF) and the satellite cell response following muscle lengthening contractions in humans. Muscle Nerve 38, 1434–1442. doi: 10.1002/ mus.21146
Pasiakos, S. M., and Carbone, J. W. (2014). Assessment of skeletal muscle proteolysis and the regulatory response to nutrition and exercise. IUBMB Life 66, 478–484. doi: 10.1002/iub.1291
Pesta, D., Hoppel, F., Macek, C., Messner, H., Faulhaber, M., Kobel, C., et al. (2011). Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R1078– R1087. doi: 10.1152/ajpregu.00285.2011
Petrella, J. K., Kim, J. S., Cross, J. M., Kosek, D. J., and Bamman, M. M. (2006). E cacy of myonuclear addition may explain di erential myofiber growth among resistance-trained young and older men and women. Am. J. Physiol. Endocrinol. Metab. 291, E937–E946. doi: 10.1152/ajpendo.00190.2006
Petrella, J. K., Kim, J. S., Mayhew, D. L., Cross, J. M., and Bamman, M. M. (2008). Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J. Appl. Physiol. 104, 1736–1742. doi: 10.1152/japplphysiol.01215.2007
Phillips, B. E., Williams, J. P., Gustafsson, T., Bouchard, C., Rankinen, T., Knudsen, S., et al. (2013). Molecular networks of human muscle adaptation to exercise and age. PLoS Genet. 9:e1003389. doi: 10.1371/journal.pgen.100 3389
Phillips, S. M., Tipton, K. D., Ferrando, A. A., and Wolfe, R. R. (1999). Resistance training reduces the acute exercise-induced increase in muscle protein turnover. Am. J. Physiol. 276, E118–E124. doi: 10.1152/ajpendo.1999.276.1.E118
Popadic Gacesa, J. Z., Momcilovic, M., Veselinovic, I., Brodie, D. A., and Grujic, N. G. (2012). Bradykinin type 2 receptor -9/-9 genotype is associated with triceps brachii muscle hypertrophy following strength training in young healthy men. BMC Musculoskelet. Disord. 13:217. doi: 10.1186/1471-2474- 13-217
Porter, C., Reidy, P. T., Bhattarai, N., Sidossis, L. S., and Rasmussen, B. B. (2015). Resistance exercise training alters mitochondrial function in human skeletal muscle. Med. Sci. Sports Exerc. 47, 1922–1931. doi: 10.1249/MSS. 0000000000000605
Potts, G. K., Mcnally, R. M., Blanco, R., You, J. S., Hebert, A. S., Westphall, M. S., et al. (2017). A map of the phosphoproteomic alterations that occur after a bout of maximal-intensity contractions. J. Physiol. 595, 5209–5226. doi: 10.1113/JP273904
Prior, S. J., Ryan, A. S., Blumenthal, J. B., Watson, J. M., Katzel, L. I., and Goldberg, A. P. (2016). Sarcopenia is associated with lower skeletal muscle capillarization and exercise capacity in older adults. J. Gerontol. A Biol. Sci. Med. Sci. 71, 1096–1101. doi: 10.1093/gerona/glw017
Puthucheary, Z., Skipworth, J. R., Rawal, J., Loosemore, M., Van Someren, K., and Montgomery, H. E. (2011). The ACE gene and human performance: 12 years on. Sports Med. 41, 433–448. doi: 10.2165/11588720-000000000-00000
Raj, D. S., Moseley, P., Dominic, E. A., Onime, A., Tzamaloukas, A. H., Boyd, A., et al. (2008). Interleukin-6 modulates hepatic and muscle protein synthesis during hemodialysis. Kidney Int. 73, 1054–1061. doi: 10.1038/ki.2008.21
Raue, U., Trappe, T. A., Estrem, S. T., Qian, H. R., Helvering, L. M., Smith, R. C., et al. (2012). Transcriptome signature of resistance exercise adaptations: mixed muscle and fiber type specific profiles in young and old adults. J. Appl. Physiol. 112, 1625–1636. doi: 10.1152/japplphysiol.00435.2011
Reidy, P. T., Borack, M. S., Markofski, M. M., Dickinson, J. M., Fry, C. S., Deer, R. R., et al. (2017a). Post-absorptive muscle protein turnover a ects resistance training hypertrophy. Eur. J. Appl. Physiol. 117, 853–866. doi: 10.1007/s00421- 017- 3566- 4
Reidy, P. T., Fry, C. S., Igbinigie, S., Deer, R. R., Jennings, K., Cope, M. B., et al. (2017b). Protein supplementation does not a ect myogenic adaptations to resistance training. Med. Sci. Sports Exerc. 49, 1197–1208. doi: 10.1249/MSS. 0000000000001224
Reidy, P. T., and Rasmussen, B. B. (2016). Role of ingested amino acids and protein in the promotion of resistance exercise-induced muscle protein anabolism. J. Nutr. 146, 155–183. doi: 10.3945/jn.114.203208
Roberts, M. D., Dalbo, V. J., Sunderland, K. L., Poole, C. N., Hassell, S. E., Bemben, D., et al. (2010). IGF-1 splice variant and IGF-1 peptide expression patterns in young and old human skeletal muscle prior to and following sequential exercise bouts. Eur. J. Appl. Physiol. 110, 961–969. doi: 10.1007/
s00421- 010- 1588- 2
Roberts, M. D., Holland, A. M., Kephart, W. C., Mobley, C. B., Mumford, P. W.,
Lowery, R. P., et al. (2016). A putative low-carbohydrate ketogenic diet elicits mild nutritional ketosis but does not impair the acute or chronic hypertrophic responses to resistance exercise in rodents. J. Appl. Physiol. 120, 1173–1185. doi: 10.1152/japplphysiol.00837.2015
Rommel, C., Bodine, S. C., Clarke, B. A., Rossman, R., Nunez, L., Stitt, T. N., et al. (2001). Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3, 1009– 1013. doi: 10.1038/ncb1101-1009
Salvadego, D., Domenis, R., Lazzer, S., Porcelli, S., Rittweger, J., Rizzo, G., et al. (2013). Skeletal muscle oxidative function in vivo and ex vivo in athletes with marked hypertrophy from resistance training. J. Appl. Physiol. 114, 1527–1535. doi: 10.1152/japplphysiol.00883.2012
Schia no, S., and Mammucari, C. (2011). Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet. Muscle 1:4. doi: 10.1186/2044-5040-1-4
Schuelke, M., Wagner, K. R., Stolz, L. E., Hubner, C., Riebel, T., Komen, W., et al. (2004). Myostatin mutation associated with gross muscle hypertrophy in a child. N. Engl. J. Med. 350, 2682–2688. doi: 10.1056/NEJMoa040933
Silva, G. J. J., Bye, A., El Azzouzi, H., and Wislo , U. (2017). MicroRNAs as important regulators of exercise adaptation. Prog. Cardiovasc. Dis. 60, 130–151. doi: 10.1016/j.pcad.2017.06.003
Sinha-Hikim, I., Artaza, J., Woodhouse, L., Gonzalez-Cadavid, N., Singh, A. B., Lee, M. I., et al. (2002). Testosterone-induced increase in muscle size in healthy young men is associated with muscle fiber hypertrophy. Am J. Physiol. Endocrinol. Metab. 283, E154–E164. doi: 10.1152/ajpendo.00502. 2001
Sinha-Hikim, I., Roth, S. M., Lee, M. I., and Bhasin, S. (2003). Testosterone-induced muscle hypertrophy is associated with an increase in satellite cell number in healthy, young men. Am. J. Physiol. Endocrinol. Metab. 285, E197–E205. doi: 10.1152/ajpendo.00370.2002
Snijders, T., Nederveen, J. P., Joanisse, S., Leenders, M., Verdijk, L. B., Van Loon, L. J., et al. (2017). Muscle fibre capillarization is a critical factor in muscle fibre hypertrophy during resistance exercise training in older men. J. Cachexia Sarcopenia Muscle 8, 267–276. doi: 10.1002/jcsm.12137
Snijders, T., Smeets, J. S., Van Kranenburg, J., Kies, A. K., Van Loon, L. J., and Verdijk, L. B. (2016). Changes in myonuclear domain size do not precede muscle hypertrophy during prolonged resistance-type exercise training. Acta Physiol. 216, 231–239. doi: 10.1111/apha.12609
Standley, R. A., Liu, S. Z., Jemiolo, B., Trappe, S. W., and Trappe, T. A. (2013). Prostaglandin E2 induces transcription of skeletal muscle mass regulators interleukin-6 and muscle RING finger-1 in humans. Prostaglandins Leukot. Essent. Fatty Acids 88, 361–364. doi: 10.1016/j.plefa.2013.02.004
Stec, M. J., Kelly, N. A., Many, G. M., Windham, S. T., Tuggle, S. C., and Bamman, M. M. (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. doi: 10.1152/ajpendo.00486. 2015
Stefanetti, R. J., Lamon, S., Wallace, M., Vendelbo, M. H., Russell, A. P., and Vissing, K. (2015). Regulation of ubiquitin proteasome pathway molecular markers in response to endurance and resistance exercise and training. Pflugers Arch. 467, 1523–1537. doi: 10.1007/s00424-014-1587-y
Stouthamer, A. H. (1973). A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie Van Leeuwenhoek 39, 545–565. doi: 10.1007/BF02578899
Terzis, G., Georgiadis, G., Stratakos, G., Vogiatzis, I., Kavouras, S., Manta, P., et al. (2008). Resistance exercise-induced increase in muscle mass correlates with p70S6 kinase phosphorylation in human subjects. Eur. J. Appl. Physiol. 102, 145–152. doi: 10.1007/s00421-007-0564-y
Tesch, P. A., Thorsson, A., and Kaiser, P. (1984). Muscle capillary supply and fiber type characteristics in weight and power lifters. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 56, 35–38.
Thalacker-Mercer, A., Stec, M., Cui, X., Cross, J., Windham, S., and Bamman, M. (2013). Cluster analysis reveals di erential transcript profiles associated with resistance training-induced human skeletal muscle hypertrophy. Physiol. Genomics 45, 499–507. doi: 10.1152/physiolgenomics.00167.2012
Thalacker-Mercer, A. E., Petrella, J. K., and Bamman, M. M. (2009). Does habitual dietary intake influence myofiber hypertrophy in response to resistance training? A cluster analysis. Appl. Physiol. Nutr. Metab. 34, 632–639. doi: 10. 1139/H09- 038
Timmerman, K. L., Dhanani, S., Glynn, E. L., Fry, C. S., Drummond, M. J., Jennings, K., et al. (2012). A moderate acute increase in physical activity enhances nutritive flow and the muscle protein anabolic response to mixed nutrient intake in older adults. Am. J. Clin. Nutr. 95, 1403–1412. doi: 10.3945/ ajcn.111.020800
Tipton, K. D., Hamilton, D. L., and Gallagher, I. J. (2018). Assessing the role of muscle protein breakdown in response to nutrition and exercise in humans. Sports Med. 48, 53–64. doi: 10.1007/s40279-017-0845-5
Trappe, S., Luden, N., Minchev, K., Raue, U., Jemiolo, B., and Trappe, T. A. (2015). Skeletal muscle signature of a champion sprint runner. J. Appl. Physiol. 118, 1460–1466. doi: 10.1152/japplphysiol.00037.2015
Trappe, T. A., Carroll, C. C., Dickinson, J. M., Lemoine, J. K., Haus, J. M., Sullivan, B. E., et al. (2011). Influence of acetaminophen and ibuprofen on skeletal muscle adaptations to resistance exercise in older adults. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R655–R662. doi: 10.1152/ajpregu.00611. 2010
Trappe, T. A., Fluckey, J. D., White, F., Lambert, C. P., and Evans, W. J. (2001). Skeletal muscle PGF(2)(alpha) and PGE(2) in response to eccentric resistance exercise: influence of ibuprofen acetaminophen. J. Clin. Endocrinol. Metab. 86, 5067–5070.
Trappe, T. A., White, F., Lambert, C. P., Cesar, D., Hellerstein, M., and Evans, W. J. (2002). E ect of ibuprofen and acetaminophen on postexercise muscle protein synthesis. Am. J. Physiol. Endocrinol. Metab. 282, E551–E556. doi: 10. 1152/ajpendo.00352.2001
Van Etten, L. M., Verstappen, F. T., and Westerterp, K. R. (1994). E ect of body build on weight-training-induced adaptations in body composition and muscular strength. Med. Sci. Sports Exerc. 26, 515–521. doi: 10.1249/00005768- 199404000- 00018
Verdijk, L. B., Snijders, T., Drost, M., Delhaas, T., Kadi, F., and Van Loon, L. J. (2014). Satellite cells in human skeletal muscle; from birth to old age. Age 36, 545–547. doi: 10.1007/s11357-013-9583-2
Verdijk, L. B., Snijders, T., Holloway, T. M., Van Kranenburg, J., and Van Loon, L. J. (2016). Resistance training increases skeletal muscle capillarization in healthy older men. Med. Sci. Sports Exerc. 48, 2157–2164. doi: 10.1249/MSS. 0000000000001019
Volek, J. S., Forsythe, C. E., and Kraemer, W. J. (2006). Nutritional aspects of women strength athletes. Br. J. Sports Med. 40, 742–748. doi: 10.1136/bjsm. 2004.016709
Walker, D. K., Fry, C. S., Drummond, M. J., Dickinson, J. M., Timmerman, K. L., Gundermann, D. M., et al. (2012). PAX7 + satellite cells in young and older adults following resistance exercise. Muscle Nerve 46, 51–59. doi: 10.1002/mus. 23266
Wang, D. T., Yin, Y., Yang, Y. J., Lv, P. J., Shi, Y., Lu, L., et al. (2014). Resveratrol prevents TNF-alpha-induced muscle atrophy via regulation of Akt/mTOR/FoxO1 signaling in C2C12 myotubes. Int. Immunopharmacol. 19, 206–213. doi: 10.1016/j.intimp.2014.02.002
Wang, M., and Lemos, B. (2017). Ribosomal DNA copy number amplification and loss in human cancers is linked to tumor genetic context, nucleolus activity, and proliferation. PLoS Genet. 13:e1006994. doi: 10.1371/journal.pgen.100 6994
Wang, X., and Proud, C. G. (2006). The mTOR pathway in the control of protein synthesis. Physiology 21, 362–369. doi: 10.1152/physiol.00024.2006
Watt, K. I., Goodman, C. A., Hornberger, T. A., and Gregorevic, P. (2018). The hippo signaling pathway in the regulation of skeletal muscle mass and function. Exerc. Sport Sci. Rev. 46, 92–96. doi: 10.1249/JES.00000000000 00142
West, D. W., Baehr, L. M., Marcotte, G. R., Chason, C. M., Tolento, L., Gomes, A. V., et al. (2016). Acute resistance exercise activates rapamycin-sensitive and -insensitive mechanisms that control translational activity and capacity in skeletal muscle. J. Physiol. 594, 453–468. doi: 10.1113/JP271365
White, J. P., Reecy, J. M., Washington, T. A., Sato, S., Le, M. E., Davis, J. M., et al. (2009). Overload-induced skeletal muscle extracellular matrix remodelling and myofibre growth in mice lacking IL-6. Acta Physiol. 197, 321–332. doi: 10.1111/j.1748-1716.2009.02029.x
Wilkinson, D. J., Franchi, M. V., Brook, M. S., Narici, M. V., Williams, J. P., Mitchell, W. K., et al. (2014). A validation of the application of D(2)O stable isotope tracer techniques for monitoring day-to-day changes in muscle protein subfraction synthesis in humans. Am. J. Physiol. Endocrinol. Metab. 306, E571– E579. doi: 10.1152/ajpendo.00650.2013
Zak, R., Rabinowitz, M., and Platt, C. (1967). Ribonucleic acids associated with myofibrils. Biochemistry 6, 2493–2499. doi: 10.1021/bi00860a028
Zamir, O., Hasselgren, P. O., Higashiguchi, T., Frederick, J. A., and Fischer, J. E. (1992). Tumour necrosis factor (TNF) and interleukin-1 (IL-1) induce muscle proteolysis through di erent mechanisms. Mediators Inflamm. 1, 247–250. doi: 10.1155/S0962935192000371
Bas répondeur | Haut répondeur | |
Aire de section transversale des fibres musculaires (fCSA) du quadriceps | 0% | 20% |
Volume du quadriceps | 0% | 83% |
Épaisseur du vaste latérale | 4% | 30% |
Augmentation de la masse sèche corps entier | 0,5 – 1,2 kg | 2,2 – 4,5 kg |
Différences physiologiques entre bas et hauts répondeurs hypertrophiques
- La biogénèse des ribosomes induite par l’entrainement est plus grande chez les HR par rapport au BR :
Étant donné que les ribosomes catalysent la MyoPS et la MPS, et que les augmentations répétées de ces taux de synthèse après l'exercice facilitent vraisemblablement la croissance musculaire, une augmentation du contenu en ribosomes des fibres musculaires pendant les périodes d'entraînement en résistance est apparemment avantageuse pour l'hypertrophie des muscles squelettiques. Bamman’s (2016) décrit que le contenu en ribosome augmentait d’environ 30% chez des sujets mâles plus âgés, qui était haut répondeur (+83% type II fCSA) alors que qu’aucun changement du contenu en ribosome n’a été observé chez les sujets bas répondeurs.
- L’addition myonucléaire par médiation des cellules satellites pourrait dicter la réponse hypertrophique à l’entrainement en résistance : Petralla et al supportent le paradigme selon lequel la quantité de cellule satellite pré et post entrainement était plus grande chez les sujet HR que les sujets BR, après 16 semaines d’entrainement en résistance.
- Les microARNs (mARN) pourrait influencer la réponse hypertrophique par influence de l’IGF1 : Bamman et al (2007) ainsi que Davidsen et al (2011), rapportent que les niveaux de mARN de l’IGF1 sont significativement plus élevés chez les sujets hauts répondeurs.
- L’induction des récepteurs androgéniques des muscles squelettiques pourrait tracer la réponse hypertrophique. En effet, plusieurs études suggèrent qu’une augmentation de la teneur en protéine des récepteurs à androgènes pourrait promouvoir une augmentation de l’hypertrophie musculaire après un entrainement en résistance. Ahtiainen et al (2011) rapportent une corrélation entre l’augmentation de ce facteur et l’augmentation de la fCSA et de la masse sèche.
- La composition en type de fibre avant entrainement ne définit probablement pas les groupes de réponses à l’entrainement en résistance. En effet, un consensus pourtant bien établit admet que les individus ayant une haute proportion de fibres musculaires de type II sont prédisposés à être des athlètes de force/puissance, alors que les individus ayant une haute proportion de fibres musculaires de type I sont prédisposés à être des athlètes d’endurance. Pourtant, une revue récente cite plusieurs lignes de preuves qui suggèrent que le potentiel de croissance de 2 types de fibres apparait similaire lors d’un entrainement en résistance.
Les futures directions de recherche examinant quels facteurs pourraient contribuer à des réponses différentielles à l’hypertrophie
De nombreux facteurs physiologiques rentrent donc en compte dans la différenciation entre bas et haut répondeur hypertrophique, pouvant prédisposer tel ou tel individu à gagner en volume ou en force musculaire, et donc à performer. Les auteurs suggèrent une liste non exhaustive des différentes orientations intéressantes pour de futures recherches sur le sujet, parmi lesquelles :
- Le tissu conjonctif limite t-il la croissance musculaire en réponse à un entrainement en hypertrophie ?
- La réponse inflammatoire en réponse à un entrainement en résistance limite t’elle la croissance musculaire ?
- Existe-t-il une relation entre les caractéristiques mitochondriales et le type de répondeurs hypertrophiques ?
- Les groupes de réponse hypertrophique possèdent ils des différences de propriétés vasculaires ?
Mots clé : hypertrophie, biogénèse des ribosomes, cellules satellites, microARN, IGF-1, récepteur androgène.
Article original : Michael D. Roberts, Cody T. Haun, Christopher B. Mobley, Petey W. Mumford, Matthew A. Romero, Paul A. Roberson, Christopher G. Vann and John J. McCarthy. Physiological Differences Between Low Versus High Skeletal Muscle Hypertrophic Responders to Resistance Exercise Training: Current Perspectives and Future Research Directions. Front. Physiol. 9:834. doi: 10.3389/fphys.2018.00834
Référence :
Armstrong, D. D., and Esser, K. A. (2005). Wnt/beta-catenin signaling activates growth-control genes during overload-induced skeletal muscle hypertrophy. Am. J. Physiol. Cell Physiol. 289, C853–C859. doi: 10.1152/ajpcell.00093.2005
Atkinson, G., and Batterham, A. M. (2015). True and false interindividual di erences in the physiological response to an intervention. Exp. Physiol. 100, 577–588. doi: 10.1113/EP085070
Baar, K., and Esser, K. (1999). Phosphorylation of p70(S6k) correlates with increased skeletal muscle mass following resistance exercise. Am. J. Physiol. 276, C120–C127.
Bamman, M. M., Petrella, J. K., Kim, J. S., Mayhew, D. L., and Cross, J. M. (2007). Cluster analysis tests the importance of myogenic gene expression during myofiber hypertrophy in humans. J. Appl. Physiol. 102, 2232–2239. doi: 10.1152/japplphysiol.00024.2007
Bellamy, L. M., Joanisse, S., Grubb, A., Mitchell, C. J., Mckay, B. R., Phillips, S. M., et al. (2014). The acute satellite cell response and skeletal muscle hypertrophy following resistance training. PLoS One 9:e109739. doi: 10.1371/journal.pone. 0109739
Betz, C., and Hall, M. N. (2013). Where is mTOR and what is it doing there? J. Cell Biol. 203, 563–574. doi: 10.1083/jcb.201306041
Bistrian, B. R., Schwartz, J., and Istfan, N. W. (1992). Cytokines, muscle proteolysis, and the catabolic response to infection and inflammation. Proc. Soc. Exp. Biol. Med. 200, 220–223. doi: 10.3181/00379727-200-43423
Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., et al. (2001). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3, 1014– 1019. doi: 10.1038/ncb1101-1014
Bond, P. (2016). Regulation of mTORC1 by growth factors, energy status, amino acids and mechanical stimuli at a glance. J. Int. Soc. Sports Nutr. 13:8. doi: 10.1186/s12970-016-0118-y
Bouchard, C., and Rankinen, T. (2001). Individual di erences in response to regular physical activity. Med. Sci. Sports Exerc. 33, S446–S451. doi: 10.1097/ 00005768- 200106001- 00013
Bouchard, C., Sarzynski, M. A., Rice, T. K., Kraus, W. E., Church, T. S., Sung, Y. J., et al. (2011). Genomic predictors of the maximal O2 uptake response to standardized exercise training programs. J. Appl. Physiol. 110, 1160–1170. doi: 10.1152/japplphysiol.00973.2010
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. L., Phillips, B. E., Szewczyk, N. J., et al. (2017). A novel D2O tracer method to quantify RNA turnover as a biomarker of de novo ribosomal biogenesis, in vitro, in animal models, and in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 313, E681–E689. doi: 10.1152/ajpendo.00157.2017
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. N., Szewczyk, N. J., Greenha , P. L., et al. (2015). Skeletal muscle hypertrophy adaptations predominate in the early stages of resistance exercise training, matching deuterium oxide-derived measures of muscle protein synthesis and mechanistic target of rapamycin complex 1 signaling. FASEB J. 29, 4485–4496. doi: 10.1096/ fj.15- 273755
Campbell, B., Kreider, R. B., Ziegenfuss, T., La Bounty, P., Roberts, M., Burke, D., et al. (2007). International society of sports nutrition position stand: protein and exercise. J. Int. Soc. Sports Nutr. 4:8. doi: 10.1186/1550-2783-4-8
Chaillou, T., Kirby, T. J., and Mccarthy, J. J. (2014). Ribosome biogenesis: emerging evidence for a central role in the regulation of skeletal muscle mass. J. Cell. Physiol. 229, 1584–1594. doi: 10.1002/jcp.24604
Chandler, P. N., Liu, C., Von Walden, F., and Nader, G. A. (2017). Proteasome activity is required for ribosomal DNA transcription and muscle hypertrophy. FASEB J. 31:lb782–lb782.
Charbonneau, D. E., Hanson, E. D., Ludlow, A. T., Delmonico, M. J., Hurley, B. F., and Roth, S. M. (2008). ACE genotype and the muscle hypertrophic and strength responses to strength training. Med. Sci. Sports Exerc. 40, 677–683. doi: 10.1249/MSS.0b013e318161eab9
Cheek, D. B., Holt, A. B., Hill, D. E., and Talbert, J. L. (1971). Skeletal muscle cell mass and growth: the concept of the deoxyribonucleic acid unit. Pediatr. Res. 5, 329–334. doi: 10.1203/00006450-197107000-00004
Clarkson, P. M., Devaney, J. M., Gordish-Dressman, H., Thompson, P. D., Hubal, M. J., Urso, M., et al. (2005). ACTN3 genotype is associated with increases in muscle strength in response to resistance training in women. J. Appl. Physiol. 99, 154–163. doi: 10.1152/japplphysiol.01139.2004
Clemente, C. F., Xavier-Neto, J., Dalla Costa, A. P., Consonni, S. R., Antunes, J. E., Rocco, S. A., et al. (2012). Focal adhesion kinase governs cardiac concentric hypertrophic growth by activating the AKT and mTOR pathways. J. Mol. Cell. Cardiol 52, 493–501. doi: 10.1016/j.yjmcc.2011.10.015
Crameri, R. M., Langberg, H., Magnusson, P., Jensen, C. H., Schroder, H. D., Olesen, J. L., et al. (2004). Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J. Physiol. 558, 333–340. doi: 10.1113/jphysiol.2004.061846
Dalbo, V. J., Roberts, M. D., Hassell, S., and Kerksick, C. M. (2013). E ects of pre-exercise feeding on serum hormone concentrations and biomarkers of
myostatin and ubiquitin proteasome pathway activity. Eur. J. Nutr. 52, 477–487.
doi: 10.1007/s00394-012-0349-x
Dalbo, V. J., Roberts, M. D., Sunderland, K. L., Poole, C. N., Stout, J. R., Beck, T. W.,
et al. (2011). Acute loading and aging e ects on myostatin pathway biomarkers in human skeletal muscle after three sequential bouts of resistance exercise. J. Gerontol. A Biol. Sci. Med. Sci. 66, 855–865. doi: 10.1093/gerona/glr091
Damas, F., Libardi, C. A., Ugrinowitsch, C., Vechin, F. C., Lixandrao, M. E., Snijders, T., et al. (2018). Early- and later-phases satellite cell responses and myonuclear content with resistance training in young men. PLoS One 13:e0191039. doi: 10.1371/journal.pone.0191039
Damas, F., Phillips, S. M., Libardi, C. A., Vechin, F. C., Lixandrao, M. E., Jannig, P. R., et al. (2016). Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. J. Physiol. 594, 5209–5222. doi: 10.1113/JP272472
Davidsen, P. K., Gallagher, I. J., Hartman, J. W., Tarnopolsky, M. A., Dela, F., Helge, J. W., et al. (2011). High responders to resistance exercise training demonstrate di erential regulation of skeletal muscle microRNA expression. J. Appl. Physiol. 110, 309–317. doi: 10.1152/japplphysiol.00901.2010
De Larichaudy, J., Zu erli, A., Serra, F., Isidori, A. M., Naro, F., Dessalle, K., et al. (2012). TNF-alpha- and tumor-induced skeletal muscle atrophy involves sphingolipid metabolism. Skelet. Muscle 2:2. doi: 10.1186/2044-5040-2-2
Dennis, R. A., Zhu, H., Kortebein, P. M., Bush, H. M., Harvey, J. F., Sullivan, D. H., et al. (2009). Muscle expression of genes associated with inflammation, growth, and remodeling is strongly correlated in older adults with resistance training outcomes. Physiol. Genomics 38, 169–175. doi: 10.1152/physiolgenomics.00056. 2009
Drummond, M. J., Fry, C. S., Glynn, E. L., Dreyer, H. C., Dhanani, S., Timmerman, K. L., et al. (2009). Rapamycin administration in humans blocks the contraction-induced increase in skeletal muscle protein synthesis. J. Physiol. 587, 1535–1546. doi: 10.1113/jphysiol.2008.163816
Egner, I. M., Bruusgaard, J. C., and Gundersen, K. (2016). Satellite cell depletion prevents fiber hypertrophy in skeletal muscle. Development 143, 2898–2906. doi: 10.1242/dev.134411
Ferrando, A. A., Tipton, K. D., Doyle, D., Phillips, S. M., Cortiella, J., and Wolfe, R. R. (1998). Testosterone injection stimulates net protein synthesis but not tissue amino acid transport. Am. J. Physiol. 275, E864–E871. doi: 10.1152/ ajpendo.1998.275.5.E864
Figueiredo, V. C., Caldow, M. K., Massie, V., Markworth, J. F., Cameron- Smith, D., and Blazevich, A. J. (2015). Ribosome biogenesis adaptation in resistance training-induced human skeletal muscle hypertrophy. Am. J. Physiol. Endocrinol. Metab. 309, E72–E83. doi: 10.1152/ajpendo.00050.2015
Fluck, M., Carson, J. A., Gordon, S. E., Ziemiecki, A., and Booth, F. W. (1999). Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am. J. Physiol. 277, C152–C162. doi: 10.1152/ajpcell.1999.277.1.C152
Franchi, M. V., Longo, S., Mallinson, J., Quinlan, J. I., Taylor, T., Greenha , P. L., et al. (2018a). Muscle thickness correlates to muscle cross-sectional area in the assessment of strength training-induced hypertrophy. Scand. J. Med. Sci. Sports 28, 846–853. doi: 10.1111/sms.12961
Franchi, M. V., Ruoss, S., Valdivieso, P., Mitchell, K. W., Smith, K., Atherton, P. J., et al. (2018b). Regional regulation of focal adhesion kinase after concentric and eccentric loading is related to remodelling of human skeletal muscle. Acta Physiol. 223:e13056. doi: 10.1111/apha.13056
Fry, C. S., Kirby, T. J., Kosmac, K., Mccarthy, J. J., and Peterson, C. A. (2017). Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy. Cell Stem Cell 20, 56–69. doi: 10.1016/j. stem.2016.09.010
Fry, C. S., Lee, J. D., Jackson, J. R., Kirby, T. J., Stasko, S. A., Liu, H., et al. (2014). Regulation of the muscle fiber microenvironment by activated satellite cells during hypertrophy. FASEB J. 28, 1654–1665. doi: 10.1096/fj.13-239426
Gao, S., Durstine, J. L., Koh, H. J., Carver, W. E., Frizzell, N., and Carson, J. A. (2017). Acute myotube protein synthesis regulation by IL-6-related cytokines. Am. J. Physiol. Cell Physiol. 313, C487–C500. doi: 10.1152/ajpcell.00112.2017
Gauthier, G. F., and Mason-Savas, A. (1993). Ribosomes in the skeletal muscle filament lattice. Anat. Rec. 237, 149–156. doi: 10.1002/ar.1092370202
Gavin, T. P., Drew, J. L., Kubik, C. J., Pofahl, W. E., and Hickner, R. C. (2007). Acute resistance exercise increases skeletal muscle angiogenic growth factor expression. Acta Physiol. 191, 139–146. doi: 10.1111/j.1748-1716.2007. 01723.x
Gibbons, J. G., Branco, A. T., Yu, S., and Lemos, B. (2014). Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans. Nat. Commun. 5:4850. doi: 10.1038/ncomms 5850
Goodman, C. A., Dietz, J. M., Jacobs, B. L., Mcnally, R. M., You, J. S., and Hornberger, T. A. (2015). Yes-associated protein is up-regulated by mechanical overload and is su cient to induce skeletal muscle hypertrophy. FEBS Lett. 589, 1491–1497. doi: 10.1016/j.febslet.2015.04.047
Griggs, R. C., Kingston, W., Jozefowicz, R. F., Herr, B. E., Forbes, G., and Halliday, D. (1989). E ect of testosterone on muscle mass and muscle protein synthesis. J. Appl. Physiol. 66, 498–503. doi: 10.1152/jappl.1989.66.1.498
Groennebaek, T., and Vissing, K. (2017). Impact of resistance training on skeletal muscle mitochondrial biogenesis, content, and function. Front. Physiol. 8:713. doi: 10.3389/fphys.2017.00713
Guth, L. M., and Roth, S. M. (2013). Genetic influence on athletic performance. Curr. Opin. Pediatr. 25, 653–658. doi: 10.1097/MOP.0b013e3283659087
Habets, P. E., Franco, D., Ruijter, J. M., Sargeant, A. J., Pereira, J. A., and Moorman, A. F. (1999). RNA content di ers in slow and fast muscle fibers: implications for interpretation of changes in muscle gene expression. J. Histochem. Cytochem. 47, 995–1004. doi: 10.1177/002215549904700803
Haddad, F., Zaldivar, F., Cooper, D. M., and Adams, G. R. (2005). IL-6-induced skeletal muscle atrophy. J. Appl. Physiol. 98, 911–917. doi: 10.1152/japplphysiol. 01026.2004
Hall, Z. W., and Ralston, E. (1989). Nuclear domains in muscle cells. Cell 59, 771–772. doi: 10.1016/0092-8674(89)90597-7
Hameed, M., Orrell, R. W., Cobbold, M., Goldspink, G., and Harridge, S. D. (2003). Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J. Physiol. 547, 247–254. doi: 10.1113/jphysiol. 2002.032136
Hammond, H. K., White, F. C., Bhargava, V., and Shabetai, R. (1992). Heart size and maximal cardiac output are limited by the pericardium. Am. J. Physiol. 263, H1675–H1681. doi: 10.1152/ajpheart.1992.263.6.H1675
Hikida, R. S., Staron, R. S., Hagerman, F. C., Walsh, S., Kaiser, E., Shell, S., et al. (2000). E ects of high-intensity resistance training on untrained older men. II. Muscle fiber characteristics and nucleo-cytoplasmic relationships. J. Gerontol. A Biol. Sci. Med. Sci. 55, B347–B354.
Hjorth, M., Norheim, F., Meen, A. J., Pourteymour, S., Lee, S., Holen, T., et al. (2015). The e ect of acute and long-term physical activity on extracellular matrix and serglycin in human skeletal muscle. Physiol. Rep. 3:e12473. doi: 10.14814/phy2.12473
Hornberger, T. A. (2011). Mechanotransduction and the regulation of mTORC1 signaling in skeletal muscle. Int. J. Biochem. Cell Biol. 43, 1267–1276. doi: 10.1016/j.biocel.2011.05.007
Hornberger, T. A., Chu, W. K., Mak, Y. W., Hsiung, J. W., Huang, S. A., and Chien, S. (2006). The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 103, 4741–4746. doi: 10.1073/pnas.0600678103
Hulmi, J. J., Tannerstedt, J., Selanne, H., Kainulainen, H., Kovanen, V., and Mero, A. A. (2009). Resistance exercise with whey protein ingestion a ects mTOR signaling pathway and myostatin in men. J. Appl. Physiol. 106, 1720–1729. doi: 10.1152/japplphysiol.00087.2009
Ingjer, F. (1979). Capillary supply and mitochondrial content of di erent skeletal muscle fiber types in untrained and endurance-trained men. A histochemical and ultrastructural study. Eur. J. Appl. Physiol. Occup. Physiol. 40, 197–209. doi: 10.1007/BF00426942
Jiang, M., Ma, Y., Chen, C., Fu, X., Yang, S., Li, X., et al. (2009). Androgen- responsive gene database: integrated knowledge on androgen-responsive genes. Mol. Endocrinol. 23, 1927–1933. doi: 10.1210/me.2009-0103
Kadi, F., Eriksson, A., Holmner, S., and Thornell, L. E. (1999). E ects of anabolic steroids on the muscle cells of strength-trained athletes. Med. Sci. Sports Exerc. 31, 1528–1534. doi: 10.1097/00005768-199911000-00006
Kadi, F., Schjerling, P., Andersen, L. L., Charifi, N., Madsen, J. L., Christensen, L. R., et al. (2004). The e ects of heavy resistance training and detraining on satellite cells in human skeletal muscles. J. Physiol. 558, 1005–1012. doi: 10.1113/jphysiol.2004.065904
Kerksick, C. M., Kreider, R. B., and Willoughby, D. S. (2010). Intramuscular adaptations to eccentric exercise and antioxidant supplementation. Amino Acids 39, 219–232. doi: 10.1007/s00726-009-0432-7
Kerksick, C. M., Roberts, M. D., Dalbo, V. J., Kreider, R. B., and Willoughby, D. S. (2013). Changes in skeletal muscle proteolytic gene expression after prophylactic supplementation of EGCG and NAC and eccentric damage. Food Chem. Toxicol. 61, 47–52. doi: 10.1016/j.fct.2013.01.026
Kim, J. S., Petrella, J. K., Cross, J. M., and Bamman, M. M. (2007). Load-mediated downregulation of myostatin mRNA is not su cient to promote myofiber hypertrophy in humans: a cluster analysis. J. Appl. Physiol. 103, 1488–1495. doi: 10.1152/japplphysiol.01194.2006
Knowles, O. E., Drinkwater, E. J., Urwin, C. S., Lamon, S., and Aisbett, B. (2018). Inadequate sleep and muscle strength: Implications for resistance training. J. Sci. Med. Sport. doi: 10.1016/j.jsams.2018.01.012 [Epub ahead of print].
Kostek, M. C., Delmonico, M. J., Reichel, J. B., Roth, S. M., Douglass, L., Ferrell, R. E., et al. (2005). Muscle strength response to strength training is influenced by insulin-like growth factor 1 genotype in older adults. J. Appl. Physiol. 98, 2147–2154. doi: 10.1152/japplphysiol.00817.2004
Krentz, J. R., Quest, B., Farthing, J. P., Quest, D. W., and Chilibeck, P. D. (2008). The e ects of ibuprofen on muscle hypertrophy, strength, and soreness during resistance training. Appl. Physiol. Nutr. Metab. 33, 470–475. doi: 10.1139/H08- 019
Kwon, I., Lee, Y., Cosio-Lima, L. M., Cho, J. Y., and Yeom, D. C. (2015). E ects of long-term resistance exercise training on autophagy in rat skeletal muscle of chloroquine-induced sporadic inclusion body myositis. J. Exerc. Nutr. Biochem. 19, 225–234. doi: 10.5717/jenb.2015.15090710
Li, X., Wang, S. J., Tan, S. C., Chew, P. L., Liu, L., Wang, L., et al. (2014). The A55T and K153R polymorphisms of MSTN gene are associated with the strength training-induced muscle hypertrophy among Han Chinese men. J. Sports Sci. 32, 883–891. doi: 10.1080/02640414.2013.865252
Lindstrom, M., and Thornell, L. E. (2009). 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. 132, 141–157. doi: 10.1007/s00418-009-0606-0
Louis, E., Raue, U., Yang, Y., Jemiolo, B., and Trappe, S. (2007). Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J. Appl. Physiol. 103, 1744–1751. doi: 10.1152/ japplphysiol.00679.2007
Lueders, T. N., Zou, K., Huntsman, H. D., Meador, B., Mahmassani, Z., Abel, M., et al. (2011). The alpha7beta1-integrin accelerates fiber hypertrophy and myogenesis following a single bout of eccentric exercise. Am. J. Physiol. Cell Physiol. 301, C938–C946. doi: 10.1152/ajpcell.00515.2010
Mackey, A. L., Esmarck, B., Kadi, F., Koskinen, S. O., Kongsgaard, M., Sylvestersen, A., et al. (2007). Enhanced satellite cell proliferation with resistance training in elderly men and women. Scand. J. Med. Sci. Sports 17, 34–42.
Mann, T. N., Lamberts, R. P., and Lambert, M. I. (2014). High responders and low responders: factors associated with individual variation in response to standardized training. Sports Med. 44, 1113–1124. doi: 10.1007/s40279-014- 0197- 3
Markworth, J. F., and Cameron-Smith, D. (2011). Prostaglandin F2&↵ stimulates PI3K/ERK/mTOR signaling and skeletal myotube hypertrophy. Am. J. Physiol. Cell Physiol. 300, C671–C682. doi: 10.1152/ajpcell.00549.2009
Masiero, E., and Sandri, M. (2010). Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles. Autophagy 6, 307–309. doi: 10.4161/auto. 6.2.11137
Mayhew, D. L., Kim, J. S., Cross, J. M., Ferrando, A. A., and Bamman, M. M. (2009). Translational signaling responses preceding resistance training- mediated myofiber hypertrophy in young and old humans. J. Appl. Physiol. 107, 1655–1662. doi: 10.1152/japplphysiol.91234.2008
McCall, G. E., Byrnes, W. C., Dickinson, A., Pattany, P. M., and Fleck, S. J. (1996). Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training. J. Appl. Physiol. 81, 2004–2012. doi: 10.1152/jappl.1996.81. 5.2004
McCarthy, J. J., and Esser, K. A. (2007). MicroRNA-1 and microRNA-133a expression are decreased during skeletal muscle hypertrophy. J. Appl. Physiol. 102, 306–313. doi: 10.1152/japplphysiol.00932.2006
McCarthy, J. J., Mula, J., Miyazaki, M., Erfani, R., Garrison, K., Farooqui, A. B., et al. (2011). E ective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138, 3657–3666. doi: 10.1242/dev.068858
Mitchell, C. J., Churchward-Venne, T. A., Bellamy, L., Parise, G., Baker, S. K., and Phillips, S. M. (2013). Muscular and systemic correlates of resistance training- induced muscle hypertrophy. PLoS One 8:e78636. doi: 10.1371/journal.pone. 0078636
Mitchell, C. J., Churchward-Venne, T. A., Parise, G., Bellamy, L., Baker, S. K., Smith, K., et al. (2014). Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training-induced muscle hypertrophy in young men. PLoS One 9:e89431. doi: 10.1371/journal.pone.0089431
Mitchell, C. J., Churchward-Venne, T. A., West, D. W., Burd, N. A., Breen, L., Baker, S. K., et al. (2012). Resistance exercise load does not determine training- mediated hypertrophic gains in young men. J. Appl. Physiol. 113, 71–77. doi: 10.1152/japplphysiol.00307.2012
Mobley, C. B., Fox, C. D., Thompson, R. M., Healy, J. C., Santucci, V., Kephart, W. C., et al. (2016). Comparative e ects of whey protein versus L-leucine on skeletal muscle protein synthesis and markers of ribosome biogenesis following resistance exercise. Amino Acids 48, 733–750. doi: 10.1007/s00726-015- 2121-z
Mobley, C. B., Haun, C. T., Roberson, P. A., Mumford, P. W., Kephart, W. C., Romero, M. A., et al. (2018a). Biomarkers associated with low, moderate, and high vastus lateralis muscle hypertrophy following 12 weeks of resistance training. PLoS One 13:e0195203. doi: 10.1371/journal.pone.01 95203
Mobley, C. B., Haun, C. T., Roberson, P. A., Mumford, P. W., Romero, M. A., Kephart, W. C., et al. (2017). E ects 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 9:E972. doi: 10.3390/nu9090972
Mobley, C. B., Holland, A. M., Kephart, W. C., Mumford, P. W., Lowery, R. P., Kavazis, A. N., et al. (2018b). Progressive resistance-loaded voluntary wheel running increases hypertrophy and di erentially a ects muscle protein synthesis, ribosome biogenesis, and proteolytic markers in rat muscle. J. Anim. Physiol. Anim. Nutr. 102, 317–329. doi: 10.1111/jpn.12691
Morissette, M. R., Cook, S. A., Buranasombati, C., Rosenberg, M. A., and Rosenzweig, A. (2009). Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt. Am. J. Physiol. Cell Physiol. 297, C1124–C1132. doi: 10.1152/ ajpcell.00043.2009
Munoz-Canoves, P., Scheele, C., Pedersen, B. K., and Serrano, A. L. (2013). Interleukin-6 myokine signaling in skeletal muscle: a double-edged sword? FEBS J. 280, 4131–4148. doi: 10.1111/febs.12338
Murach, K. A., Fry, C. S., Kirby, T. J., Jackson, J. R., Lee, J. D., White, S. H., et al. (2018). Starring or supporting role? Satellite cells and skeletal muscle fiber size regulation. Physiology 33, 26–38. doi: 10.1152/physiol.00019.2017
Nader, G. A., Mcloughlin, T. J., and Esser, K. A. (2005). mTOR function in skeletal muscle hypertrophy: increased ribosomal RNA via cell cycle regulators. Am. J. Physiol. Cell Physiol. 289, C1457–C1465. doi: 10.1152/ajpcell.00165. 2005
Nakada, S., Ogasawara, R., Kawada, S., Maekawa, T., and Ishii, N. (2016). Correlation between ribosome biogenesis and the magnitude of hypertrophy in overloaded skeletal muscle. PLoS One 11:e0147284. doi: 10.1371/journal.pone. 0147284
Nederveen, J. P., Joanisse, S., Seguin, C. M., Bell, K. E., Baker, S. K., Phillips, S. M., et al. (2015). The e ect of exercise mode on the acute response of satellite cells in old men. Acta Physiol. 215, 177–190. doi: 10.1111/apha.12601
Nederveen, J. P., Snijders, T., Joanisse, S., Wavell, C. G., Mitchell, C. J., Johnston, L. M., et al. (2017). Altered muscle satellite cell activation following 16 wk of resistance training in young men. Am. J. Physiol. Regul. Integr. Comp. Physiol. 312, R85–R92. doi: 10.1152/ajpregu.00221.2016
Norrby, M., and Tagerud, S. (2010). Mitogen-activated protein kinase-activated protein kinase 2 (MK2) in skeletal muscle atrophy and hypertrophy. J. Cell. Physiol. 223, 194–201. doi: 10.1002/jcp.22023
Ogasawara, R., Akimoto, T., Umeno, T., Sawada, S., Hamaoka, T., and Fujita, S. (2016). MicroRNA expression profiling in skeletal muscle reveals di erent regulatory patterns in high and low responders to resistance training. Physiol. Genomics 48, 320–324. doi: 10.1152/physiolgenomics.00124. 2015
Ogborn, D., and Schoenfeld, B. J. (2014). The role of fiber types in muscle hypertrophy: implications for loading strategies. Strength Cond. J. 36, 20–25. doi: 10.1519/SSC.0000000000000030
O’Reilly, C., Mckay, B., Phillips, S., Tarnopolsky, M., and Parise, G. (2008). Hepatocyte growth factor (HGF) and the satellite cell response following muscle lengthening contractions in humans. Muscle Nerve 38, 1434–1442. doi: 10.1002/ mus.21146
Pasiakos, S. M., and Carbone, J. W. (2014). Assessment of skeletal muscle proteolysis and the regulatory response to nutrition and exercise. IUBMB Life 66, 478–484. doi: 10.1002/iub.1291
Pesta, D., Hoppel, F., Macek, C., Messner, H., Faulhaber, M., Kobel, C., et al. (2011). Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R1078– R1087. doi: 10.1152/ajpregu.00285.2011
Petrella, J. K., Kim, J. S., Cross, J. M., Kosek, D. J., and Bamman, M. M. (2006). E cacy of myonuclear addition may explain di erential myofiber growth among resistance-trained young and older men and women. Am. J. Physiol. Endocrinol. Metab. 291, E937–E946. doi: 10.1152/ajpendo.00190.2006
Petrella, J. K., Kim, J. S., Mayhew, D. L., Cross, J. M., and Bamman, M. M. (2008). Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J. Appl. Physiol. 104, 1736–1742. doi: 10.1152/japplphysiol.01215.2007
Phillips, B. E., Williams, J. P., Gustafsson, T., Bouchard, C., Rankinen, T., Knudsen, S., et al. (2013). Molecular networks of human muscle adaptation to exercise and age. PLoS Genet. 9:e1003389. doi: 10.1371/journal.pgen.100 3389
Phillips, S. M., Tipton, K. D., Ferrando, A. A., and Wolfe, R. R. (1999). Resistance training reduces the acute exercise-induced increase in muscle protein turnover. Am. J. Physiol. 276, E118–E124. doi: 10.1152/ajpendo.1999.276.1.E118
Popadic Gacesa, J. Z., Momcilovic, M., Veselinovic, I., Brodie, D. A., and Grujic, N. G. (2012). Bradykinin type 2 receptor -9/-9 genotype is associated with triceps brachii muscle hypertrophy following strength training in young healthy men. BMC Musculoskelet. Disord. 13:217. doi: 10.1186/1471-2474- 13-217
Porter, C., Reidy, P. T., Bhattarai, N., Sidossis, L. S., and Rasmussen, B. B. (2015). Resistance exercise training alters mitochondrial function in human skeletal muscle. Med. Sci. Sports Exerc. 47, 1922–1931. doi: 10.1249/MSS. 0000000000000605
Potts, G. K., Mcnally, R. M., Blanco, R., You, J. S., Hebert, A. S., Westphall, M. S., et al. (2017). A map of the phosphoproteomic alterations that occur after a bout of maximal-intensity contractions. J. Physiol. 595, 5209–5226. doi: 10.1113/JP273904
Prior, S. J., Ryan, A. S., Blumenthal, J. B., Watson, J. M., Katzel, L. I., and Goldberg, A. P. (2016). Sarcopenia is associated with lower skeletal muscle capillarization and exercise capacity in older adults. J. Gerontol. A Biol. Sci. Med. Sci. 71, 1096–1101. doi: 10.1093/gerona/glw017
Puthucheary, Z., Skipworth, J. R., Rawal, J., Loosemore, M., Van Someren, K., and Montgomery, H. E. (2011). The ACE gene and human performance: 12 years on. Sports Med. 41, 433–448. doi: 10.2165/11588720-000000000-00000
Raj, D. S., Moseley, P., Dominic, E. A., Onime, A., Tzamaloukas, A. H., Boyd, A., et al. (2008). Interleukin-6 modulates hepatic and muscle protein synthesis during hemodialysis. Kidney Int. 73, 1054–1061. doi: 10.1038/ki.2008.21
Raue, U., Trappe, T. A., Estrem, S. T., Qian, H. R., Helvering, L. M., Smith, R. C., et al. (2012). Transcriptome signature of resistance exercise adaptations: mixed muscle and fiber type specific profiles in young and old adults. J. Appl. Physiol. 112, 1625–1636. doi: 10.1152/japplphysiol.00435.2011
Reidy, P. T., Borack, M. S., Markofski, M. M., Dickinson, J. M., Fry, C. S., Deer, R. R., et al. (2017a). Post-absorptive muscle protein turnover a ects resistance training hypertrophy. Eur. J. Appl. Physiol. 117, 853–866. doi: 10.1007/s00421- 017- 3566- 4
Reidy, P. T., Fry, C. S., Igbinigie, S., Deer, R. R., Jennings, K., Cope, M. B., et al. (2017b). Protein supplementation does not a ect myogenic adaptations to resistance training. Med. Sci. Sports Exerc. 49, 1197–1208. doi: 10.1249/MSS. 0000000000001224
Reidy, P. T., and Rasmussen, B. B. (2016). Role of ingested amino acids and protein in the promotion of resistance exercise-induced muscle protein anabolism. J. Nutr. 146, 155–183. doi: 10.3945/jn.114.203208
Roberts, M. D., Dalbo, V. J., Sunderland, K. L., Poole, C. N., Hassell, S. E., Bemben, D., et al. (2010). IGF-1 splice variant and IGF-1 peptide expression patterns in young and old human skeletal muscle prior to and following sequential exercise bouts. Eur. J. Appl. Physiol. 110, 961–969. doi: 10.1007/
s00421- 010- 1588- 2
Roberts, M. D., Holland, A. M., Kephart, W. C., Mobley, C. B., Mumford, P. W.,
Lowery, R. P., et al. (2016). A putative low-carbohydrate ketogenic diet elicits mild nutritional ketosis but does not impair the acute or chronic hypertrophic responses to resistance exercise in rodents. J. Appl. Physiol. 120, 1173–1185. doi: 10.1152/japplphysiol.00837.2015
Rommel, C., Bodine, S. C., Clarke, B. A., Rossman, R., Nunez, L., Stitt, T. N., et al. (2001). Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3, 1009– 1013. doi: 10.1038/ncb1101-1009
Salvadego, D., Domenis, R., Lazzer, S., Porcelli, S., Rittweger, J., Rizzo, G., et al. (2013). Skeletal muscle oxidative function in vivo and ex vivo in athletes with marked hypertrophy from resistance training. J. Appl. Physiol. 114, 1527–1535. doi: 10.1152/japplphysiol.00883.2012
Schia no, S., and Mammucari, C. (2011). Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet. Muscle 1:4. doi: 10.1186/2044-5040-1-4
Schuelke, M., Wagner, K. R., Stolz, L. E., Hubner, C., Riebel, T., Komen, W., et al. (2004). Myostatin mutation associated with gross muscle hypertrophy in a child. N. Engl. J. Med. 350, 2682–2688. doi: 10.1056/NEJMoa040933
Silva, G. J. J., Bye, A., El Azzouzi, H., and Wislo , U. (2017). MicroRNAs as important regulators of exercise adaptation. Prog. Cardiovasc. Dis. 60, 130–151. doi: 10.1016/j.pcad.2017.06.003
Sinha-Hikim, I., Artaza, J., Woodhouse, L., Gonzalez-Cadavid, N., Singh, A. B., Lee, M. I., et al. (2002). Testosterone-induced increase in muscle size in healthy young men is associated with muscle fiber hypertrophy. Am J. Physiol. Endocrinol. Metab. 283, E154–E164. doi: 10.1152/ajpendo.00502. 2001
Sinha-Hikim, I., Roth, S. M., Lee, M. I., and Bhasin, S. (2003). Testosterone-induced muscle hypertrophy is associated with an increase in satellite cell number in healthy, young men. Am. J. Physiol. Endocrinol. Metab. 285, E197–E205. doi: 10.1152/ajpendo.00370.2002
Snijders, T., Nederveen, J. P., Joanisse, S., Leenders, M., Verdijk, L. B., Van Loon, L. J., et al. (2017). Muscle fibre capillarization is a critical factor in muscle fibre hypertrophy during resistance exercise training in older men. J. Cachexia Sarcopenia Muscle 8, 267–276. doi: 10.1002/jcsm.12137
Snijders, T., Smeets, J. S., Van Kranenburg, J., Kies, A. K., Van Loon, L. J., and Verdijk, L. B. (2016). Changes in myonuclear domain size do not precede muscle hypertrophy during prolonged resistance-type exercise training. Acta Physiol. 216, 231–239. doi: 10.1111/apha.12609
Standley, R. A., Liu, S. Z., Jemiolo, B., Trappe, S. W., and Trappe, T. A. (2013). Prostaglandin E2 induces transcription of skeletal muscle mass regulators interleukin-6 and muscle RING finger-1 in humans. Prostaglandins Leukot. Essent. Fatty Acids 88, 361–364. doi: 10.1016/j.plefa.2013.02.004
Stec, M. J., Kelly, N. A., Many, G. M., Windham, S. T., Tuggle, S. C., and Bamman, M. M. (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. doi: 10.1152/ajpendo.00486. 2015
Stefanetti, R. J., Lamon, S., Wallace, M., Vendelbo, M. H., Russell, A. P., and Vissing, K. (2015). Regulation of ubiquitin proteasome pathway molecular markers in response to endurance and resistance exercise and training. Pflugers Arch. 467, 1523–1537. doi: 10.1007/s00424-014-1587-y
Stouthamer, A. H. (1973). A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie Van Leeuwenhoek 39, 545–565. doi: 10.1007/BF02578899
Terzis, G., Georgiadis, G., Stratakos, G., Vogiatzis, I., Kavouras, S., Manta, P., et al. (2008). Resistance exercise-induced increase in muscle mass correlates with p70S6 kinase phosphorylation in human subjects. Eur. J. Appl. Physiol. 102, 145–152. doi: 10.1007/s00421-007-0564-y
Tesch, P. A., Thorsson, A., and Kaiser, P. (1984). Muscle capillary supply and fiber type characteristics in weight and power lifters. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 56, 35–38.
Thalacker-Mercer, A., Stec, M., Cui, X., Cross, J., Windham, S., and Bamman, M. (2013). Cluster analysis reveals di erential transcript profiles associated with resistance training-induced human skeletal muscle hypertrophy. Physiol. Genomics 45, 499–507. doi: 10.1152/physiolgenomics.00167.2012
Thalacker-Mercer, A. E., Petrella, J. K., and Bamman, M. M. (2009). Does habitual dietary intake influence myofiber hypertrophy in response to resistance training? A cluster analysis. Appl. Physiol. Nutr. Metab. 34, 632–639. doi: 10. 1139/H09- 038
Timmerman, K. L., Dhanani, S., Glynn, E. L., Fry, C. S., Drummond, M. J., Jennings, K., et al. (2012). A moderate acute increase in physical activity enhances nutritive flow and the muscle protein anabolic response to mixed nutrient intake in older adults. Am. J. Clin. Nutr. 95, 1403–1412. doi: 10.3945/ ajcn.111.020800
Tipton, K. D., Hamilton, D. L., and Gallagher, I. J. (2018). Assessing the role of muscle protein breakdown in response to nutrition and exercise in humans. Sports Med. 48, 53–64. doi: 10.1007/s40279-017-0845-5
Trappe, S., Luden, N., Minchev, K., Raue, U., Jemiolo, B., and Trappe, T. A. (2015). Skeletal muscle signature of a champion sprint runner. J. Appl. Physiol. 118, 1460–1466. doi: 10.1152/japplphysiol.00037.2015
Trappe, T. A., Carroll, C. C., Dickinson, J. M., Lemoine, J. K., Haus, J. M., Sullivan, B. E., et al. (2011). Influence of acetaminophen and ibuprofen on skeletal muscle adaptations to resistance exercise in older adults. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R655–R662. doi: 10.1152/ajpregu.00611. 2010
Trappe, T. A., Fluckey, J. D., White, F., Lambert, C. P., and Evans, W. J. (2001). Skeletal muscle PGF(2)(alpha) and PGE(2) in response to eccentric resistance exercise: influence of ibuprofen acetaminophen. J. Clin. Endocrinol. Metab. 86, 5067–5070.
Trappe, T. A., White, F., Lambert, C. P., Cesar, D., Hellerstein, M., and Evans, W. J. (2002). E ect of ibuprofen and acetaminophen on postexercise muscle protein synthesis. Am. J. Physiol. Endocrinol. Metab. 282, E551–E556. doi: 10. 1152/ajpendo.00352.2001
Van Etten, L. M., Verstappen, F. T., and Westerterp, K. R. (1994). E ect of body build on weight-training-induced adaptations in body composition and muscular strength. Med. Sci. Sports Exerc. 26, 515–521. doi: 10.1249/00005768- 199404000- 00018
Verdijk, L. B., Snijders, T., Drost, M., Delhaas, T., Kadi, F., and Van Loon, L. J. (2014). Satellite cells in human skeletal muscle; from birth to old age. Age 36, 545–547. doi: 10.1007/s11357-013-9583-2
Verdijk, L. B., Snijders, T., Holloway, T. M., Van Kranenburg, J., and Van Loon, L. J. (2016). Resistance training increases skeletal muscle capillarization in healthy older men. Med. Sci. Sports Exerc. 48, 2157–2164. doi: 10.1249/MSS. 0000000000001019
Volek, J. S., Forsythe, C. E., and Kraemer, W. J. (2006). Nutritional aspects of women strength athletes. Br. J. Sports Med. 40, 742–748. doi: 10.1136/bjsm. 2004.016709
Walker, D. K., Fry, C. S., Drummond, M. J., Dickinson, J. M., Timmerman, K. L., Gundermann, D. M., et al. (2012). PAX7 + satellite cells in young and older adults following resistance exercise. Muscle Nerve 46, 51–59. doi: 10.1002/mus. 23266
Wang, D. T., Yin, Y., Yang, Y. J., Lv, P. J., Shi, Y., Lu, L., et al. (2014). Resveratrol prevents TNF-alpha-induced muscle atrophy via regulation of Akt/mTOR/FoxO1 signaling in C2C12 myotubes. Int. Immunopharmacol. 19, 206–213. doi: 10.1016/j.intimp.2014.02.002
Wang, M., and Lemos, B. (2017). Ribosomal DNA copy number amplification and loss in human cancers is linked to tumor genetic context, nucleolus activity, and proliferation. PLoS Genet. 13:e1006994. doi: 10.1371/journal.pgen.100 6994
Wang, X., and Proud, C. G. (2006). The mTOR pathway in the control of protein synthesis. Physiology 21, 362–369. doi: 10.1152/physiol.00024.2006
Watt, K. I., Goodman, C. A., Hornberger, T. A., and Gregorevic, P. (2018). The hippo signaling pathway in the regulation of skeletal muscle mass and function. Exerc. Sport Sci. Rev. 46, 92–96. doi: 10.1249/JES.00000000000 00142
West, D. W., Baehr, L. M., Marcotte, G. R., Chason, C. M., Tolento, L., Gomes, A. V., et al. (2016). Acute resistance exercise activates rapamycin-sensitive and -insensitive mechanisms that control translational activity and capacity in skeletal muscle. J. Physiol. 594, 453–468. doi: 10.1113/JP271365
White, J. P., Reecy, J. M., Washington, T. A., Sato, S., Le, M. E., Davis, J. M., et al. (2009). Overload-induced skeletal muscle extracellular matrix remodelling and myofibre growth in mice lacking IL-6. Acta Physiol. 197, 321–332. doi: 10.1111/j.1748-1716.2009.02029.x
Wilkinson, D. J., Franchi, M. V., Brook, M. S., Narici, M. V., Williams, J. P., Mitchell, W. K., et al. (2014). A validation of the application of D(2)O stable isotope tracer techniques for monitoring day-to-day changes in muscle protein subfraction synthesis in humans. Am. J. Physiol. Endocrinol. Metab. 306, E571– E579. doi: 10.1152/ajpendo.00650.2013
Zak, R., Rabinowitz, M., and Platt, C. (1967). Ribonucleic acids associated with myofibrils. Biochemistry 6, 2493–2499. doi: 10.1021/bi00860a028
Zamir, O., Hasselgren, P. O., Higashiguchi, T., Frederick, J. A., and Fischer, J. E. (1992). Tumour necrosis factor (TNF) and interleukin-1 (IL-1) induce muscle proteolysis through di erent mechanisms. Mediators Inflamm. 1, 247–250. doi: 10.1155/S0962935192000371