Document Type : Original Article
Authors
Assistant Professor, Department of Sport Sciences, Faculty of Sport Sciences, Shomal University, Amol, Iran.
Abstract
Background and Aim: Resistance training (RT) is the most effective strategy to prevent age-related muscle wasting and weakness, because it promotes muscle strength and function. As the loss of muscle mass contributes to sarcopenia, the effects of RT on hypertrophy and its myogenic processes is controversial in old age. The purpose of this study was to examine the effects of RT on strength, mass and protein level of myogenin in gastrocnemius muscle of elderly rats. Materials and Methods: Sixteen elderly male Sprague-Dawley rats (24-month age) divided equally to two groups (control and RT). RT group underwent 8weeks (3-days/week) of resistance training by climbing a wooden ladder with weights attached to their tails. 48h after last session, isometric force, muscle wet mass and protein level of myogenin of gastrocnemius muscle were measured in both groups. For statistical analysis, independent sample t-test was used with a significance level of 0.05. Results: Absolute and relative (to body mass) isometric force of RT group were significantly greater than those in control group. There was not any significant difference in wet muscle mass between groups. Western blot analysis of muscle tissue also showed that the levels of myogenin did not significantly differ between two groups. Conclusion: Force production capacity and muscle quality (force to muscle mass ratio) were increased following resistance training in elderly rats through events are likely caused by neuromuscular adaptations. Additionally, the results suggest that increase in strength after resistance training in aged rats cannot be explained in terms of the changing in muscle mass and myogenin expression values.
Keywords
Adamo, M. L., & Farrar, R. P. (2006). Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing Research Reviews, 5(3), 310-331.
Afsharnezhad, T., Nourshahi, M., & Parvardeh, S. (2016). Effect of resistance training on functional and histopathological changes in muscle after chronic strain Injury in elderly rat. Journal Mazandaran University Medical Sciences, 26(140), 33-44. [Persian]
Ballak, S. B., Degens, H., de Haan, A., & Jaspers, R. T. (2014). Aging related changes in determinants of muscle force generating capacity: a comparison of muscle aging in men and male rodents. Ageing Research Reviews, 14, 43-55.
Bamman, M. M., Ragan, R. C., Kim, J. S., Cross, J. M., Hill, V. J., Tuggle, S. C., & Allman, R. M. (2004). Myogenic protein expression before and after resistance loading in 26- and 64-yr-old men and women. Journal of Applied Physiology, 97(4), 1329-1337.
Borde, R., Hortobagyi, T., & Granacher, U. (2015). Dose-response relationships of resistance training in healthy old adults: A systematic review and meta-analysis. Sports Medicine, 45(12), 1693-1720.
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. N., Phillips, B. E., Szewczyk, N. J., … & Atherton, P. J. (2016). Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age-related anabolic resistance to exercise in humans. The Journal of Physiology, 594(24), 7399-7417.
Bruunsgaard, H., Bjerregaard, E., Schroll, M., & Pedersen, B. K. (2004). Muscle strength after resistance training is inversely correlated with baseline levels of soluble tumor necrosis factor receptors in the oldest old. Journal of the American Geriatrics Society, 52(2), 237-241.
Burd, N. A., West, D. W., Staples, A. W., Atherton, P. J., Baker, J. M., Moore, D. R., & Phillips, S. M. (2010). Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS One, 5(8), e12033.
Ciolac, E. G. (2013). Exercise training as a preventive tool for age-related disorders: a brief review. Clinics, 68(5), 710-717.
Ciolac, E. G., & Rodrigues-da-Silva, J. M. (2016). Resistance training as a tool for preventing and treating musculoskeletal disorders. Sports Medicine, 46(9), 1239-1248.
Dedkov, E. I., Kostrominova, T. Y., Borisov, A. B., & Carlson, B. M. (2003). MyoD and myogenin protein expression in skeletal muscles of senile rats. Cell and Tissue Research, (3), 401-416.
Domingues-Faria, C., Vasson, M. P., Goncalves-Mendes, N., Boirie, Y., & Walrand, S. (2016). Skeletal muscle regeneration and impact of aging and nutrition. Ageing Research Reviews, 26, 22-36.
Drummond, M. J., Conlee, R. K., Mack, G. W., Sudweeks, S., Schaalje, G. B., & Parcell, A. C. (2010). Myogenic regulatory factor response to resistance exercise volume in skeletal muscle. European Journal of Applied Physiology, 108(4), 771-778.
Drummond, M. J., Dreyer, H. C., Pennings, B., Fry, C. S., Dhanani, S., Dillon, E. L., … & Rasmussen, B. B. (2008). Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. Journal of Applied Physiology, 104(5), 1452-1461.
Drummond, M. J., Fry, C. S., Glynn, E. L., Timmerman, K. L., Dickinson, J. M., Walker, D. K., … & Rasmussen, B. B. (2011). Skeletal muscle amino acid transporter expression is increased in young and older adults following resistance exercise. Journal of Applied Physiology, 111(1), 135-142.
Faulkner, J. A., Larkin, L. M., Claflin, D. R., & Brooks, S. V. (2007). Age-related changes in the structure and function of skeletal muscles. Clinical and Experimental Pharmacology and Physiology, 34(11), 1091-1096.
Fujimaki, S., Hidaka, R., Asashima, M., Takemasa, T., & Kuwabara, T. (2014). Wnt protein-mediated satellite cell conversion in adult and aged mice following voluntary wheel running. Journal of Biological Chemistry, 289(11), 7399-7412.
Gault, M. L., & Willems, M. E. (2013). Aging, functional capacity and eccentric exercise training. Aging and Disease, 4(6), 351-363.
Gibson, T. M., & Gersbach, C. A. (2015). Single-molecule analysis of myocyte differentiation reveals bimodal lineage commitment. Integrative Biology, 7(6), 663-671.
Gundersen, K. (2011). Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biological Reviews, 86(3), 564-600.
Hulmi, J. J., Kovanen, V., Lisko, I., Selanne, H., & Mero, A. A. (2008). The effects of whey protein on myostatin and cell cycle-related gene expression responses to a single heavy resistance exercise bout in trained older men. European Journal of Applied Physiology, 102(2), 205-213.
Hwee, D. T., & Bodine, S. C. (2009). Age-related deficit in load-induced skeletal muscle growth. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences, 64(6), 618-628.
Iolascon, G., Di Pietro, G., Gimigliano, F., Mauro, G. L., Moretti, A., Giamattei, M. T., … & Brandi, M. L. (2014). Physical exercise and sarcopenia in older people: position paper of the Italian Society of Orthopaedics and Medicine. Clinical Cases in Mineral and Bone Metabolism, 11(3), 215-221.
Jang, Y. C., & Van Remmen, H. (2011). Age-associated alterations of the neuromuscular junction. Experimental Gerontology, 46(2-3), 193-198.
Jensky, N. E., Sims, J. K., Rice, J. C., Dreyer, H. C., & Schroeder, E. T. (2007). The influence of eccentric exercise on mRNA expression of skeletal muscle regulators. European Journal of Applied Physiology, 101(4), 473-480.
Kirby, T. J., Lee, J. D., England, J. H., Chaillou, T., Esser, K. A., & McCarthy, J. J. (2015). Blunted hypertrophic response in aged skeletal muscle is associated with decreased ribosome biogenesis. Journal of Applied Physiology, 119(4), 321-327.
Kosek, D., Kim, J., Petrella, J., Cross, J., & Bamman, M. (2006). Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanism in young vs older adults. Journal of Applied Physiology, 101(2), 531-44.
Kumar, V., Selby, A., Rankin, D., Patel, R., Atherton, P., Hildebrandt, W., … & Rennie, M. J. (2009). Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. The Journal of Physiology, 587(1), 211-217.
Lee, J. D., Fry, C. S., Mula, J., Kirby, T. J., Jackson, J. R., Liu, F., … & Peterson, C. A. (2016). Aged muscle demonstrates fiber-type adaptations in response to mechanical overload, in the absence of myofiber hypertrophy, independent of satellite cell abundance. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences, 71(4), 461-467.
Legerlotz, K., & Smith, H. K. (2008). Role of MyoD in denervated, disused, and exercised muscle. Muscle & Nerve: Official Journal of the American Association of Electrodiagnostic Medicine, 38(3), 1087-1100.
McKay, B. R., O'Reilly, C. E., Phillips, S. M., Tarnopolsky, M. A., & Parise, G. (2008). Co-expression of IGF-1 family members with myogenic regulatory factors following acute damaging muscle-lengthening contractions in humans. The Journal of Physiology, 586(22), 5549-5560.
Mero, A. A., Hulmi, J. J., Salmijarvi, H., Katajavuori, M., Haverinen, M., Holviala, J., … & Selanne, H. (2013). Resistance training induced increase in muscle fiber size in young and older men. European Journal of Applied Physiology, 113(3), 641-650.
Millay, D. P., Sutherland, L. B., Bassel-Duby, R., & Olson, E. N. (2014). Myomaker is essential for muscle regeneration. Genes & Development, 28(15), 1641-1646.
Peterson, M. D., Rhea, M. R., Sen, A., & Gordon, P. M. (2010). Resistance exercise for muscular strength in older adults: a meta-analysis. Ageing Research Reviews, 9(3), 226-237.
Phillips, B. E., Williams, J. P., Greenhaff, P. L., Smith, K., & Atherton, P. J. (2017). Physiological adaptations to resistance exercise as a function of age. Journal of Clinical Investigation Insight, 2(17), p95581.
Popov, D. V., Lysenko, E. A., Bachinin, A. V., Miller, T. F., Kurochkina, N. S., Kravchenko, I. V., … & Vinogradova, O. L. (2015). Influence of resistance exercise intensity and metabolic stress on anabolic signaling and expression of myogenic genes in skeletal muscle. Muscle Nerve, 51(3), 434-442.
Psilander, N., Damsgaard, R., & Pilegaard, H. (2003). Resistance exercise alters MRF and IGF-1 mRNA content in human skeletal muscle. Journal of Applied Physiology, 95(3), 1038-44.
Raue, U., Slivka, D., Jemiolo, B., Hollon, C., & Trappe, S. (2006). Myogenic gene expression at rest and after a bout of resistance exercise in young (18-30 yr) and old (80-89 yr) women. Journal of Applied Physiology, 101(1), 53-59.
Schultz, E., Chamberlain, C., McCormick, K. M., & Mozdziak, P. E. (2006). Satellite cells express distinct patterns of myogenic proteins in immature skeletal muscle. Developmental Dynamics: an Official Publication of the American Association of Anatomists, 235(12), 3230-3239.
Shavlakadze, T., McGeachie, J., & Grounds, M. D. (2009). Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice. Biogerontology, 11(3), 363-376.
Sjogaard, G., Zebis, M. K., Kiilerich, K., Saltin, B., & Pilegaard, H. (2013). Exercise training and work task induced metabolic and stress-related mRNA and protein responses in myalgic muscles. BioMed Research International, 2013, 1-12.
Snijders, T., Nederveen, J. P., McKay, B. R., Joanisse, S., Verdijk, L. B., van Loon, L. J. C., & Parise, G. (2015). Satellite cells in human skeletal muscle plasticity. Frontiers in Physiology, 6, 283.
Snijders, T., Verdijk, L. B., Beelen, M., McKay, B. R., Parise, G., Kadi, F., & van Loon, L. J. (2012). A single bout of exercise activates skeletal muscle satellite cells during subsequent overnight recovery. Experimental Physiology, 97(6), 762-773.
Snijders, T., Verdijk, L. B., Smeets, J. S., McKay, B. R., Senden, J. M., Hartgens, F., … & van Loon, L. J. (2014). The skeletal muscle satellite cell response to a single bout of resistance-type exercise is delayed with aging in men. Age, 36(4), 96-99.
Spillane, M., Schwarz, N., Leddy, S., Correa, T., Minter, M., Longoria, V., & Willoughby, D. S. (2011). Effects of 28 days of resistance exercise while consuming commercially available pre- and post-workout supplements, NO-Shotgun(R) and NO-Synthesize(R) on body composition, muscle strength and mass, markers of protein synthesis, and clinical safety markers in males. Nutrition & Metabolism, 8(1), 78.
Stefanetti, R., Zacharewicz, E., Della Gatta, P., Garnham, A., Russell, A., & Lamon, S. (2014). Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise. Frontiers in Physiology, 5, 1-30.
Suetta, C., Aagaard, P., Rosted, A., Jakobsen, A. K., Duus, B., Kjaer, M., & Magnusson, S. P. (2004). Traininginduced changes in muscle CSA, muscle strength, EMG, and rate of force development in elderly subjects after long-term unilateral disuse. Journal of Applied Physiology, 97(5), 1954-1961.
Thomson, D. M., & Gordon, S. E. (2005). Diminished overload-induced hypertrophy in aged fast-twitch skeletal muscle is associated with AMPK hyperphosphorylation. Journal of Applied Physiology, 98(2), 557-564.
Willoughby, D., & Nelson, M. (2002). Myosin heavy-chain mrna expression after a single bout session of heavy-resistance exercise. Medicine and Science in Sports and Exercise, 34(8), 1262-9.
Xu, Q., & Wu, Z. (2000). The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. Journal of Biological Chemistry, 275(47), 36750-36757.
Zanou, N., & Gailly, P. (2013). Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways. Cellular and Molecular Life Sciences, 70(21), 4117-4130.
Afsharnezhad, T., Nourshahi, M., & Parvardeh, S. (2016). Effect of resistance training on functional and histopathological changes in muscle after chronic strain Injury in elderly rat. Journal Mazandaran University Medical Sciences, 26(140), 33-44. [Persian]
Ballak, S. B., Degens, H., de Haan, A., & Jaspers, R. T. (2014). Aging related changes in determinants of muscle force generating capacity: a comparison of muscle aging in men and male rodents. Ageing Research Reviews, 14, 43-55.
Bamman, M. M., Ragan, R. C., Kim, J. S., Cross, J. M., Hill, V. J., Tuggle, S. C., & Allman, R. M. (2004). Myogenic protein expression before and after resistance loading in 26- and 64-yr-old men and women. Journal of Applied Physiology, 97(4), 1329-1337.
Borde, R., Hortobagyi, T., & Granacher, U. (2015). Dose-response relationships of resistance training in healthy old adults: A systematic review and meta-analysis. Sports Medicine, 45(12), 1693-1720.
Brook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. N., Phillips, B. E., Szewczyk, N. J., … & Atherton, P. J. (2016). Synchronous deficits in cumulative muscle protein synthesis and ribosomal biogenesis underlie age-related anabolic resistance to exercise in humans. The Journal of Physiology, 594(24), 7399-7417.
Bruunsgaard, H., Bjerregaard, E., Schroll, M., & Pedersen, B. K. (2004). Muscle strength after resistance training is inversely correlated with baseline levels of soluble tumor necrosis factor receptors in the oldest old. Journal of the American Geriatrics Society, 52(2), 237-241.
Burd, N. A., West, D. W., Staples, A. W., Atherton, P. J., Baker, J. M., Moore, D. R., & Phillips, S. M. (2010). Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS One, 5(8), e12033.
Ciolac, E. G. (2013). Exercise training as a preventive tool for age-related disorders: a brief review. Clinics, 68(5), 710-717.
Ciolac, E. G., & Rodrigues-da-Silva, J. M. (2016). Resistance training as a tool for preventing and treating musculoskeletal disorders. Sports Medicine, 46(9), 1239-1248.
Dedkov, E. I., Kostrominova, T. Y., Borisov, A. B., & Carlson, B. M. (2003). MyoD and myogenin protein expression in skeletal muscles of senile rats. Cell and Tissue Research, (3), 401-416.
Domingues-Faria, C., Vasson, M. P., Goncalves-Mendes, N., Boirie, Y., & Walrand, S. (2016). Skeletal muscle regeneration and impact of aging and nutrition. Ageing Research Reviews, 26, 22-36.
Drummond, M. J., Conlee, R. K., Mack, G. W., Sudweeks, S., Schaalje, G. B., & Parcell, A. C. (2010). Myogenic regulatory factor response to resistance exercise volume in skeletal muscle. European Journal of Applied Physiology, 108(4), 771-778.
Drummond, M. J., Dreyer, H. C., Pennings, B., Fry, C. S., Dhanani, S., Dillon, E. L., … & Rasmussen, B. B. (2008). Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. Journal of Applied Physiology, 104(5), 1452-1461.
Drummond, M. J., Fry, C. S., Glynn, E. L., Timmerman, K. L., Dickinson, J. M., Walker, D. K., … & Rasmussen, B. B. (2011). Skeletal muscle amino acid transporter expression is increased in young and older adults following resistance exercise. Journal of Applied Physiology, 111(1), 135-142.
Faulkner, J. A., Larkin, L. M., Claflin, D. R., & Brooks, S. V. (2007). Age-related changes in the structure and function of skeletal muscles. Clinical and Experimental Pharmacology and Physiology, 34(11), 1091-1096.
Fujimaki, S., Hidaka, R., Asashima, M., Takemasa, T., & Kuwabara, T. (2014). Wnt protein-mediated satellite cell conversion in adult and aged mice following voluntary wheel running. Journal of Biological Chemistry, 289(11), 7399-7412.
Gault, M. L., & Willems, M. E. (2013). Aging, functional capacity and eccentric exercise training. Aging and Disease, 4(6), 351-363.
Gibson, T. M., & Gersbach, C. A. (2015). Single-molecule analysis of myocyte differentiation reveals bimodal lineage commitment. Integrative Biology, 7(6), 663-671.
Gundersen, K. (2011). Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biological Reviews, 86(3), 564-600.
Hulmi, J. J., Kovanen, V., Lisko, I., Selanne, H., & Mero, A. A. (2008). The effects of whey protein on myostatin and cell cycle-related gene expression responses to a single heavy resistance exercise bout in trained older men. European Journal of Applied Physiology, 102(2), 205-213.
Hwee, D. T., & Bodine, S. C. (2009). Age-related deficit in load-induced skeletal muscle growth. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences, 64(6), 618-628.
Iolascon, G., Di Pietro, G., Gimigliano, F., Mauro, G. L., Moretti, A., Giamattei, M. T., … & Brandi, M. L. (2014). Physical exercise and sarcopenia in older people: position paper of the Italian Society of Orthopaedics and Medicine. Clinical Cases in Mineral and Bone Metabolism, 11(3), 215-221.
Jang, Y. C., & Van Remmen, H. (2011). Age-associated alterations of the neuromuscular junction. Experimental Gerontology, 46(2-3), 193-198.
Jensky, N. E., Sims, J. K., Rice, J. C., Dreyer, H. C., & Schroeder, E. T. (2007). The influence of eccentric exercise on mRNA expression of skeletal muscle regulators. European Journal of Applied Physiology, 101(4), 473-480.
Kirby, T. J., Lee, J. D., England, J. H., Chaillou, T., Esser, K. A., & McCarthy, J. J. (2015). Blunted hypertrophic response in aged skeletal muscle is associated with decreased ribosome biogenesis. Journal of Applied Physiology, 119(4), 321-327.
Kosek, D., Kim, J., Petrella, J., Cross, J., & Bamman, M. (2006). Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanism in young vs older adults. Journal of Applied Physiology, 101(2), 531-44.
Kumar, V., Selby, A., Rankin, D., Patel, R., Atherton, P., Hildebrandt, W., … & Rennie, M. J. (2009). Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. The Journal of Physiology, 587(1), 211-217.
Lee, J. D., Fry, C. S., Mula, J., Kirby, T. J., Jackson, J. R., Liu, F., … & Peterson, C. A. (2016). Aged muscle demonstrates fiber-type adaptations in response to mechanical overload, in the absence of myofiber hypertrophy, independent of satellite cell abundance. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences, 71(4), 461-467.
Legerlotz, K., & Smith, H. K. (2008). Role of MyoD in denervated, disused, and exercised muscle. Muscle & Nerve: Official Journal of the American Association of Electrodiagnostic Medicine, 38(3), 1087-1100.
McKay, B. R., O'Reilly, C. E., Phillips, S. M., Tarnopolsky, M. A., & Parise, G. (2008). Co-expression of IGF-1 family members with myogenic regulatory factors following acute damaging muscle-lengthening contractions in humans. The Journal of Physiology, 586(22), 5549-5560.
Mero, A. A., Hulmi, J. J., Salmijarvi, H., Katajavuori, M., Haverinen, M., Holviala, J., … & Selanne, H. (2013). Resistance training induced increase in muscle fiber size in young and older men. European Journal of Applied Physiology, 113(3), 641-650.
Millay, D. P., Sutherland, L. B., Bassel-Duby, R., & Olson, E. N. (2014). Myomaker is essential for muscle regeneration. Genes & Development, 28(15), 1641-1646.
Peterson, M. D., Rhea, M. R., Sen, A., & Gordon, P. M. (2010). Resistance exercise for muscular strength in older adults: a meta-analysis. Ageing Research Reviews, 9(3), 226-237.
Phillips, B. E., Williams, J. P., Greenhaff, P. L., Smith, K., & Atherton, P. J. (2017). Physiological adaptations to resistance exercise as a function of age. Journal of Clinical Investigation Insight, 2(17), p95581.
Popov, D. V., Lysenko, E. A., Bachinin, A. V., Miller, T. F., Kurochkina, N. S., Kravchenko, I. V., … & Vinogradova, O. L. (2015). Influence of resistance exercise intensity and metabolic stress on anabolic signaling and expression of myogenic genes in skeletal muscle. Muscle Nerve, 51(3), 434-442.
Psilander, N., Damsgaard, R., & Pilegaard, H. (2003). Resistance exercise alters MRF and IGF-1 mRNA content in human skeletal muscle. Journal of Applied Physiology, 95(3), 1038-44.
Raue, U., Slivka, D., Jemiolo, B., Hollon, C., & Trappe, S. (2006). Myogenic gene expression at rest and after a bout of resistance exercise in young (18-30 yr) and old (80-89 yr) women. Journal of Applied Physiology, 101(1), 53-59.
Schultz, E., Chamberlain, C., McCormick, K. M., & Mozdziak, P. E. (2006). Satellite cells express distinct patterns of myogenic proteins in immature skeletal muscle. Developmental Dynamics: an Official Publication of the American Association of Anatomists, 235(12), 3230-3239.
Shavlakadze, T., McGeachie, J., & Grounds, M. D. (2009). Delayed but excellent myogenic stem cell response of regenerating geriatric skeletal muscles in mice. Biogerontology, 11(3), 363-376.
Sjogaard, G., Zebis, M. K., Kiilerich, K., Saltin, B., & Pilegaard, H. (2013). Exercise training and work task induced metabolic and stress-related mRNA and protein responses in myalgic muscles. BioMed Research International, 2013, 1-12.
Snijders, T., Nederveen, J. P., McKay, B. R., Joanisse, S., Verdijk, L. B., van Loon, L. J. C., & Parise, G. (2015). Satellite cells in human skeletal muscle plasticity. Frontiers in Physiology, 6, 283.
Snijders, T., Verdijk, L. B., Beelen, M., McKay, B. R., Parise, G., Kadi, F., & van Loon, L. J. (2012). A single bout of exercise activates skeletal muscle satellite cells during subsequent overnight recovery. Experimental Physiology, 97(6), 762-773.
Snijders, T., Verdijk, L. B., Smeets, J. S., McKay, B. R., Senden, J. M., Hartgens, F., … & van Loon, L. J. (2014). The skeletal muscle satellite cell response to a single bout of resistance-type exercise is delayed with aging in men. Age, 36(4), 96-99.
Spillane, M., Schwarz, N., Leddy, S., Correa, T., Minter, M., Longoria, V., & Willoughby, D. S. (2011). Effects of 28 days of resistance exercise while consuming commercially available pre- and post-workout supplements, NO-Shotgun(R) and NO-Synthesize(R) on body composition, muscle strength and mass, markers of protein synthesis, and clinical safety markers in males. Nutrition & Metabolism, 8(1), 78.
Stefanetti, R., Zacharewicz, E., Della Gatta, P., Garnham, A., Russell, A., & Lamon, S. (2014). Ageing has no effect on the regulation of the ubiquitin proteasome-related genes and proteins following resistance exercise. Frontiers in Physiology, 5, 1-30.
Suetta, C., Aagaard, P., Rosted, A., Jakobsen, A. K., Duus, B., Kjaer, M., & Magnusson, S. P. (2004). Traininginduced changes in muscle CSA, muscle strength, EMG, and rate of force development in elderly subjects after long-term unilateral disuse. Journal of Applied Physiology, 97(5), 1954-1961.
Thomson, D. M., & Gordon, S. E. (2005). Diminished overload-induced hypertrophy in aged fast-twitch skeletal muscle is associated with AMPK hyperphosphorylation. Journal of Applied Physiology, 98(2), 557-564.
Willoughby, D., & Nelson, M. (2002). Myosin heavy-chain mrna expression after a single bout session of heavy-resistance exercise. Medicine and Science in Sports and Exercise, 34(8), 1262-9.
Xu, Q., & Wu, Z. (2000). The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. Journal of Biological Chemistry, 275(47), 36750-36757.
Zanou, N., & Gailly, P. (2013). Skeletal muscle hypertrophy and regeneration: interplay between the myogenic regulatory factors (MRFs) and insulin-like growth factors (IGFs) pathways. Cellular and Molecular Life Sciences, 70(21), 4117-4130.
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