Cited by 242Muscle metabolism and nutritionMuscle Physiology and DisordersSports Performance and Training

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Resistance exercise-induced increase in muscle mass correlates with p70S6 kinase phosphorylation in human subjects

Terzis, Gerasimos, Georgiadis, Giorgos, Stratakos, Grigoris, Vogiatzis, Ioannis, Kavouras, Stavros, Manta, Panagiota, Mascher, Henrik, Blomstrand, Eva·2007·European Journal of Applied Physiology

DOI 10.1007/s00421-007-0564-y

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Abstract

The purpose of the present study was to investigate the possible relationship between a change in Thr(389) phosphorylation of p70S6 kinase (p70(S6k)) after a single resistance training session and an increase in skeletal muscle mass following short-term resistance training. Eight male subjects performed an initial resistance training session in leg press, six sets of 6RM with 2 min between sets. Muscle biopsies were obtained from the vastus lateralis before (T1) and 30 min after the initial training session (T2). Six of these subjects completed a 14-week resistance-training programme, three times per week (nine exercises, six sets, 6RM). A third muscle biopsy was obtained at the end of the 14-week training period (T3). One repetition maximum (1RM) squat, bench press and leg press strength as well as fat-free mass (FFM, with dual energy X-ray absorptiometry) were determined at T1 and T3. The results show that the increase in Thr(389) phosphorylation of p70(S6k) after the initial training session was closely correlated with the percentage increase in whole body FFM (r = 0.89, P < 0.01), FFM(leg) (r = 0.81, P < 0.05), 1RM squat (r = 0.84, P < 0.05), and type IIA muscle fibre cross sectional area (r = 0.82, P < 0.05) after 14 weeks of resistance training. These results may suggest that p70(S6k) phosphorylation is involved in the signalling events leading to an increase in protein accretion in human skeletal muscle following resistance training, at least during the initial training period.

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Skeletal muscle protein balance and metabolism in the elderly
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“While the phosphorylation status of signaling proteins is often difficult to correlate with changes in protein turnover [129], increases in the phosphorylation of ribosomal p70S6 Kinase 1 (S6K1) is a good marker for muscle hypertrophy following resistance exercise training [130,131].”
The degree of p70S6k and S6 phosphorylation in human skeletal muscle in response to resistance exercise depends on the training volume
Terzis, G., Spengos, K., Mascher, H., Georgiadis, G., Manta, P., & Blomstrand, E. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1527-2 · Cited by 110
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BackgroundMethodResultInfluentialSelf-citation
Resistance exercise induced mTORC1 signaling is not impaired by subsequent endurance exercise in human skeletal muscle
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The effects of aging, physical training, and a single bout of exercise on mitochondrial protein expression in human skeletal muscle
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MicroRNAs in skeletal muscle and their regulation with exercise, ageing, and disease
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“Low muscle hypertrophy response to resistance exercise training in healthy young subjects is referred to as anabolic resistance (Baar and Esser, 1999; Terzis et al., 2008); a phenomenon also linked to age-related muscle wasting or sarcopenia in the elderly.”
Background
Intake of a Ketone Ester Drink during Recovery from Exercise Promotes mTORC1 Signaling but Not Glycogen Resynthesis in Human Muscle
Vandoorne, T., Smet, S. D., Ramaekers, M., Thienen, R. V., Bock, K. D., Clarke, K., & Hespel, P. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00310 · Cited by 116
“While evaluation of muscle protein synthesis via key proteins involved in protein translation has been shown to be a reliable procedure (Baar and Esser, 1999; Bodine et al., 2001; Terzis et al., 2008; Drummond et al., 2009), a dissociation between S6K1/4EBP-1 phosphorylation and muscle protein synthesis might still be…”
BackgroundInfluential
Physiological Differences Between Low Versus High Skeletal Muscle Hypertrophic Responders to Resistance Exercise Training: Current Perspectives and Future Research Directions
Roberts, M. D., Haun, C. T., Mobley, C. B., Mumford, P. W., Romero, M. A., Roberson, P. A., Vann, C. G., & McCarthy, J. J. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00834 · Cited by 107
“associated with muscle hypertrophy following chronic resistance exercise training (Baar and Esser, 1999; Terzis et al., 2008; Hulmi et al., 2009; Mayhew et al., 2009; Mitchell et al., 2013, 2014).”
BackgroundInfluential
Heat stress activates the A kt/m TOR signalling pathway in rat skeletal muscle
Yoshihara, T., Naıto, H., Kakigi, R., Ichinoseki‐Sekine, N., Ogura, Y., Sugiura, T., & Katamoto, S. (2012) · Acta Physiologica · doi:10.1111/apha.12040 · Cited by 117
“…and p70S6K phosphorylation is affected by increases in the concentration of insulin, and that the extent of p70S6K phosphorylation is related to myofibrillar protein synthesis and increases in muscle mass in human skeletal muscles (Terzis et al. 2008, Kumar et al. 2009, Esbjornsson et al. 2012).”
Background
Age-dependent changes in 8-oxoguanine-DNA glycosylase activity are modulated by adaptive responses to physical exercise in human skeletal muscle
Radak, Z. O., Bori, Z., Koltai, E., Fatouros, I. G., Jamurtas, A. Z., DOUROUDOS, I. I., Terzis, G. D., Nikolaidis, M. G., Chatzinikolaou, A., Sovatzidis, A., et al. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.04.018 · Cited by 109
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Muscle Fiber Conduction Velocity, Muscle Fiber Composition, and Power Performance
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“This suggests that the selective hypertrophy of type II muscle fibers in strength/power-trained individuals (34) may increase the range of F/S ratio.”
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Maximal lengthening contractions induce different signaling responses in the type I and type II fibers of human skeletal muscle
Tannerstedt, J., Apró, W., & Blomstrand, E. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91243.2008 · Cited by 104
Resistance exercise and nutrition to counteract muscle wasting
Little, J. P., & Phillips, S. M. (2009) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h09-093 · Cited by 102
Benefits of higher resistance-training volume are related to ribosome biogenesis
Hammarström, D., Øfsteng, S., Koll, L., Hanestadhaugen, M., Hollan, I., Apró, W., Whist, J. E., Blomstrand, E., Rønnestad, B. R., & Ellefsen, S. (2020) · The Journal of Physiology · doi:10.1113/jp278455 · Cited by 99
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BackgroundInfluentialSelf-citation
Heat stress enhances mTOR signaling after resistance exercise in human skeletal muscle
Kakigi, R., Naito, H., Ogura, Y., Kobayashi, H., Saga, N., Ichinoseki-Sekine, N., Yoshihara, T., & Katamoto, S. (2011) · The Journal of Physiological Sciences · doi:10.1007/s12576-010-0130-y · Cited by 95
“Furthermore, studies in rodent [16 ]a nd human [ 23 ] skeletal muscle have shown that S6K1 phosphorylation after resistance exercise is positively correlated with the degree of skeletal muscle hypertrophy after long-term resistance training.”
Background
mVps34 is activated following high‐resistance contractions
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“The activation of mTORC1 following resistance exercise is well correlated with the degree of hypertrophy following training in both rats and humans (Baar & Esser, 1999; Terzis et al. 2008).”
Background
Intramuscular Anabolic Signaling and Endocrine Response Following Resistance Exercise: Implications for Muscle Hypertrophy
Gonzalez, A. M., Hoffman, J. R., Stout, J. R., Fukuda, D. H., & Willoughby, D. S. (2015) · Sports Medicine · doi:10.1007/s40279-015-0450-4 · Cited by 97
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“In several studies, acute increase in the p70 ribosomal S6 kinase (p70S6K) signaling pathway following resistance exercise was found to be highly correlated with long-term increases in muscle size following resistance training (Mayhew et al. 2011; Terzis et al. 2008).”
Background
Does Aerobic Training Promote the Same Skeletal Muscle Hypertrophy as Resistance Training? A Systematic Review and Meta-Analysis
Grgić, J., McIlvenna, L. C., Fyfe, J. J., Sabol, F., Bishop, D. J., Schoenfeld, B. J., & Pedišić, Ž. (2018) · Sports Medicine · doi:10.1007/s40279-018-1008-z · Cited by 89
Concurrent exercise incorporating high-intensity interval or continuous training modulates mTORC1 signaling and microRNA expression in human skeletal muscle
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Aerobic Exercise Alters Skeletal Muscle Molecular Responses to Resistance Exercise
LUNDBERG, T. R., FERNANDEZ-GONZALO, R., GUSTAFSSON, T., & TESCH, P. A. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318256fbe8 · Cited by 86
“The activity of p70S6 kinase (p70S6K), the most well-defined effector in the mammalian target of rapamycin (mTOR) signaling pathway, correlates with increased protein synthesis and muscle mass in both animals (3) and humans (34).”
Background
Resistance exercise decreases eIF2Bε phosphorylation and potentiates the feeding-induced stimulation of p70S6K1 and rpS6 in young men
Glover, E. I., Oates, B. R., Tang, J. E., Moore, D. R., Tarnopolsky, M. A., & Phillips, S. M. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00097.2008 · Cited by 87
“In light of the strong relationship between p70 phosphorylation and hypertrophy in rodents (2) and humans (56), our observation is perhaps not surprising.”
Background
Tissue-Engineered Skeletal Muscle Models to Study Muscle Function, Plasticity, and Disease
Khodabukus, A. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.619710 · Cited by 92
“Like native muscle (Baar and Esser, 1999; Terzis et al., 2008; Drummond et al., 2009), these increases in muscle hypertrophy are associated with increased mTORC1 activity and can be inhibited by the mTOR inhibitor rapamycin.”
Background
Phosphatidic acid mediates activation of mTORC1 through the ERK signaling pathway
Winter, J. N., Fox, T. E., KESTER, M. A., Jefferson, L. S., & Kimball, S. R. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00039.2010 · Cited by 84
“Additionally, S6K1 phosphorylation is increased in humans after exercise (51), showing that mTORC1 signaling is increased by exercise.”
Background
Relationship between limb and trunk muscle hypertrophy following high‐intensity resistance training and blood flow–restricted low‐intensity resistance training
Yasuda, T., Ogasawara, R., Sakamaki, M., Bemben, M. G., & Abe, T. (2011) · Clinical Physiology and Functional Imaging · doi:10.1111/j.1475-097x.2011.01022.x · Cited by 82
Physical Activity and Telomere Biology: Exploring the Link with Aging-Related Disease Prevention
Ludlow, A. T., & Roth, S. M. (2011) · Journal of Aging Research · doi:10.4061/2011/790378 · Cited by 80
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Background
A Systematic Review with Meta-Analysis of the Effect of Resistance Training on Whole-Body Muscle Growth in Healthy Adult Males
Benito, P. J., Cupeiro, R., Ramos-Campo, D. J., Alcaraz, P. E., & Rubio-Arias, J. Á. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17041285 · Cited by 71
Inhibition of Myostatin Signaling through Notch Activation following Acute Resistance Exercise
MacKenzie, M. G., Hamilton, D. L., Pepin, M. E., Patton, A., & Baar, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068743 · Cited by 72
“This is in stark contrast to components of the mTORC1 pathway that show a tight correlation between their activation following resistance exercise and increases in muscle mass and strength following training [12,13].”
ResultInfluential
High force development augments skeletal muscle signalling in resistance exercise modes equalized for time under tension
Gehlert, S., Suhr, F., Gutsche, K., Willkomm, L., Kern, J., Jacko, D., Knicker, A. J., Schiffer, T., Wackerhage, H., & Bloch, W. (2014) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-014-1579-y · Cited by 73
“To date, several studies have found good relations between anabolic signalling, protein synthesis and hypertrophy [5, 7, 13], while others discuss this relation [39, 52, 53].”
Influential
Augmented Anabolic Responses after 8-wk Cycling with Blood Flow Restriction
Conceição, M. S., Mendes, E. M., Telles, G. D., Libardi, C. A., Castro, A., de Andrade, A. L. L., Brum, P. C., Urias, Ú., Kurauti, M. A., Júnior, J. M. C., et al. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001755 · Cited by 69
Acute molecular responses in untrained and trained muscle subjected to aerobic and resistance exercise training versus resistance training alone
Fernandez‐Gonzalo, R., Lundberg, T. R., & Tesch, P. A. (2013) · Acta Physiologica · doi:10.1111/apha.12174 · Cited by 69
“Collectively, these findings (current (Mitchell et al. 2012)) contrast the notion of a relationship between p70S6K phosphorylation and training-induced gains in muscle mass in rodents (Baar & Esser 1999) and humans (Terzis et al. 2008).”
Background
Regulatory mechanisms of skeletal muscle protein turnover during exercise
Rose, A. J., & Richter, E. A. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91375.2008 · Cited by 67
Correlation between Ribosome Biogenesis and the Magnitude of Hypertrophy in Overloaded Skeletal Muscle
Nakada, S., Ogasawara, R., Kawada, S., Maekawa, T., & Ishii, N. (2016) · PLOS ONE · doi:10.1371/journal.pone.0147284 · Cited by 64
“However, sustained overloading of muscle by synergist ablation may cause a much stronger stimulus than in physiological interventions such as electric stimulation [17] and resistance exercise [34].”
Background
Interpreting Adaptation to Concurrent Compared with Single-Mode Exercise Training: Some Methodological Considerations
Fyfe, J. J., & Loenneke, J. P. (2017) · Sports Medicine · doi:10.1007/s40279-017-0812-1 · Cited by 68
Skeletal Muscle Ribosome and Mitochondrial Biogenesis in Response to Different Exercise Training Modalities
Mesquita, P. H. C., Vann, C. G., Phillips, S. M., McKendry, J., Young, K. C., Kavazis, A. N., & Roberts, M. D. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.725866 · Cited by 62
Hybrid training of voluntary and electrical muscle contractions reduces steatosis, insulin resistance, and IL-6 levels in patients with NAFLD: a pilot study
Kawaguchi, T., Shiba, N. N., Maeda, T., Matsugaki, T., Takano, Y., Itou, M., Sakata, M., Taniguchi, E., Nagata, K., & Sata, M. (2011) · Journal of Gastroenterology · doi:10.1007/s00535-011-0378-x · Cited by 61
“Mechanisms for exercise-induced improvement of insulin resistance and NAFLD remain unclear; however, exercise itself increases energy expenditures and up-regulates resting energy expenditure through an increase in skeletal muscle mass [15, 16].”
Background
Influence of supplementation with branched-chain amino acids in combination with resistance exercise on p70S6 kinase phosphorylation in resting and exercising human skeletal muscle
Apró, W., & Blomstrand, E. (2010) · Acta Physiologica · doi:10.1111/j.1748-1708.2010.02151.x · Cited by 76
“These findings are in agreement with some (Coffey et al. 2006, Deshmukh et al. 2006, Eliasson et al. 2006) but no all (Creer et al. 2005, Blomstrand et al. 2006, Dreyer et al. 2006, Deldicque et al. 2008, Terzis et al. 2008) earlier studies of contractile activity on Akt phosphorylation.”
Result
Pre-training Skeletal Muscle Fiber Size and Predominant Fiber Type Best Predict Hypertrophic Responses to 6 Weeks of Resistance Training in Previously Trained Young Men
Haun, C. T., Vann, C. G., Mobley, C. B., Osburn, S. C., Mumford, P. W., Roberson, P. A., Romero, M. A., Fox, C. D., Parry, H. A., Kavazis, A. N., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00297 · Cited by 60
State of Knowledge on Molecular Adaptations to Exercise in Humans: Historical Perspectives and Future Directions
Lavin, K. M., Coen, P. M., Baptista, L. C. P., Bell, M. B., Drummer, D. J., Harper, S. A., Lixandrão, M. E., McAdam, J. S., O’Bryan, S. M., Ramos, S. V., et al. (2022) · Comprehensive physiology · doi:10.1002/cphy.c200033 · Cited by 78
Vitamin C Administration Attenuates Overload-Induced Skeletal Muscle Hypertrophy in Rats
Makanae, Y., Kawada, S., Sasaki, K., Nakazato, K., & Ishii, N. (2013) · Acta Physiologica · doi:10.1111/apha.12042 · Cited by 59
“Erk1/2 and p70s6k, both of which act as a mediator of skeletal muscle hypertrophy (Baar & Esser 1999, Haddad & Adams 2004, Shi et al. 2007, Terzis et al. 2008), are shown to be phosphorylated by mechanical overload (Carlson et al. 2001, Miyazaki et al. 2011).”
Background
Molecular signaling in muscle is affected by the specificity of resistance exercise protocol
Hulmi, J. J., Walker, S., Ahtiainen, J. P., Nyman, K., Kraemer, W. J., & Häkkinen, K. (2010) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2010.01198.x · Cited by 62
“An enhanced mTOR andMAPK signaling is positive for muscle size (Baar & Esser, 1999; Haddad & Adams, 2004; Terzis et al., 2008; Shi et al., 2009; Ruvinsky et al., 2009) and protein synthesis response to a bout of resistance exercise (Fluckey et al., 2006; Kumar et al., 2009).”
Background
Emerging therapies for the treatment of skeletal muscle wasting in chronic obstructive pulmonary disease
Passey, S. L., Hansen, M. J., Bozinovski, S., McDonald, C. F., Holland, A. E., & Vlahos, R. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.06.013 · Cited by 57
“Resistance or strength training involves lifting heavy weights for a prescribed number of repetitions, to build strength and increase muscle mass in individual muscles or muscle groups through upregulation of the mTOR signaling pathway (Terzis et al., 2008; Walker et al., 2011).”
Background
Resistance Exercise-Induced Hypertrophy: A Potential Role for Rapamycin-Insensitive mTOR
Ogasawara, R., Jensen, T. E., Goodman, C. A., & Hornberger, T. A. (2019) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000189 · Cited by 58
Dose-Response Relationship of Weekly Resistance-Training Volume and Frequency on Muscular Adaptations in Trained Men
Heaselgrave, S. R., Blacker, J., Smeuninx, B., McKendry, J., & Breen, L. (2018) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2018-0427 · Cited by 55
Variable resistance training promotes greater fatigue resistance but not hypertrophy versus constant resistance training
Walker, S., Hulmi, J. J., Wernbom, M., Nyman, K., Kraemer, W. J., Ahtiainen, J. P., & Häkkinen, K. (2013) · European Journal of Applied Physiology · doi:10.1007/s00421-013-2653-4 · Cited by 62
“hypertrophy (Baar and Esser 1999, McCall et al. 1999; Terzis et al. 2008), it is not surprising that hypertrophy was equivalent between the variable and constant resistance training groups.”
Background
Ibuprofen treatment blunts early translational signaling responses in human skeletal muscle following resistance exercise
Markworth, J. F., Vella, L. D., Figueiredo, V. C., & Cameron‐Smith, D. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01299.2013 · Cited by 59
“Exercise-induced p70S6K phosphorylation in human muscle significantly correlates with the magnitude of acute elevation in protein synthetic rate during postexercise recovery (4, 14, 21) and ultimately gains in muscle mass with chronic exercise training (27, 53).”
Background
Dietary protein supplementation in the elderly for limiting muscle mass loss
Lancha, A. H., Zanella, R., Tanabe, S. G. O., Andriamihaja, M., & Blachier, F. (2016) · Amino Acids · doi:10.1007/s00726-016-2355-4 · Cited by 61
“Phosphorylation of p70S6k is often correlated to increases in MPS rates and possible muscle hypertrophy (Baar and Esser 1999; Mitchell et al. 2013; Terzis et al. 2008).”
Background

Authors: Terzis, G., Georgiadis, G., Stratakos, G., Vogiatzis, I., Kavouras, S., Manta, P., Mascher, H., & Blomstrand, E.
Affiliations: National and Kapodistrian University of Athens (GR)
Harokopio University of Athens (GR)
Swedish School of Sport and Health Sciences (SE)
Corresponding author: Terzis, Gerasimos
ORCID: Terzis, Gerasimos
Stratakos, Grigoris
Vogiatzis, Ioannis
Kavouras, Stavros
Blomstrand, Eva
Venue: European Journal of Applied Physiology
Publisher: Springer Science and Business Media LLC
Published: 2007-09-14
Volume: 102
Issue: 2
Pages: 145-152
ISSN: 0020-9376 (ISSN-L)
1439-6319
1439-6327
DOI: 10.1007/s00421-007-0564-y
OpenAlex: W1964076858
Cited by: 242
References: 35
Citations by year: 2026: 4 · 2025: 4 · 2024: 5 · 2023: 3 · 2022: 9 · 2021: 5 · 2020: 11 · 2019: 11 · 2018: 19 · 2017: 16 · 2016: 20 · 2015: 16 · 2014: 17 · 2013: 24 · 2012: 18
FWCI: 6.21
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: European Journal of Applied Physiology (publishedVersion)
PubMed (publishedVersion)
Funders: National and Kapodistrian University of Athens
Topics: Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
Keywords: resistance training, p70 S6 kinase, skeletal muscle hypertrophy, fat-free mass, muscle strength, protein accretion, mTOR signaling, vastus lateralis
MeSH terms: Exercise Test, Physical Exertion, Humans, Male, Muscle Contraction, Phosphorylation, Statistics as Topic, Exercise, Muscle, Skeletal, Ribosomal Protein S6 Kinases, 70-kDa, Young Adult

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Resistance exercise-induced increase in muscle mass correlates with p70S6 kinase phosphorylation in human subjects

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