Cited by 475Muscle metabolism and nutritionMuscle Physiology and DisordersMetabolism, Diabetes, and Cancer

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Selective activation of AMPK‐PGC‐1α or PKB‐TSC2‐mTOR signaling can explain specific adaptive responses to endurance or resistance training‐like electrical muscle stimulation

Atherton, Philip J., Babraj, John A., Smith, Kenneth, Singh, Jaipaul, Rennie, Michael J., Wackerhage, Henning·2005·The FASEB Journal

DOI 10.1096/fj.04-2179fje

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Abstract

Endurance training induces a partial fast-to-slow muscle phenotype transformation and mitochondrial biogenesis but no growth. In contrast, resistance training mainly stimulates muscle protein synthesis resulting in hypertrophy. The aim of this study was to identify signaling events that may mediate the specific adaptations to these types of exercise. Isolated rat muscles were electrically stimulated with either high frequency (HFS; 6x10 repetitions of 3 s-bursts at 100 Hz to mimic resistance training) or low frequency (LFS; 3 h at 10 Hz to mimic endurance training). HFS significantly increased myofibrillar and sarcoplasmic protein synthesis 3 h after stimulation 5.3- and 2.7-fold, respectively. LFS had no significant effect on protein synthesis 3 h after stimulation but increased UCP3 mRNA 11.7-fold, whereas HFS had no significant effect on UCP3 mRNA. Only LFS increased AMPK phosphorylation significantly at Thr172 by approximately 2-fold and increased PGC-1alpha protein to 1.3 times of control. LFS had no effect on PKB phosphorylation but reduced TSC2 phosphorylation at Thr1462 and deactivated translational regulators. In contrast, HFS acutely increased phosphorylation of PKB at Ser473 5.3-fold and the phosphorylation of TSC2, mTOR, GSK-3beta at PKB-sensitive sites. HFS also caused a prolonged activation of the translational regulators p70 S6k, 4E-BP1, eIF-2B, and eEF2. These data suggest that a specific signaling response to LFS is a specific activation of the AMPK-PGC-1alpha signaling pathway which may explain some endurance training adaptations. HFS selectively activates the PKB-TSC2-mTOR cascade causing a prolonged activation of translational regulators, which is consistent with increased protein synthesis and muscle growth. We term this behavior the "AMPK-PKB switch." We hypothesize that the AMPK-PKB switch is a mechanism that partially mediates specific adaptations to endurance and resistance training, respectively.

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Myostatin inhibition enhances the effects of exercise on performance and metabolic outcomes in aged mice
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Exercise-Stimulated ROS Sensitive Signaling Pathways in Skeletal Muscle
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Aerobic exercise does not compromise muscle hypertrophy response to short-term resistance training
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“Vibration Vibration [i.e., application of a mechanical oscillation to the whole body (using a vibration platform) or some parts of it (using smaller vibrating devices)] has been proposed as a training modality with potential benefits in different clinical (4, 87), which would make it useful during…”
Skeletal muscle hypertrophy with concurrent exercise training: Contrary evidence for an interference effect
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Effects of resistance training on endurance capacity and muscle fiber composition in young top‐level cyclists
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“Recent studies have shown that resistance or endurance training activate distinct cell signaling involving the Akt/mTOR or AMPK pathways, respectively (Atherton et al., 2005), and that inhibitory cross-talk exist from one pathway to the other (Baar, 2006; Nader, 2006).”
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Early Time Course of Akt Phosphorylation after Endurance and Resistance Exercise
CAMERA, D. M., EDGE, J., SHORT, M. J., HAWLEY, J. A., & COFFEY, V. G. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181d964e4 · Cited by 154
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Compatibility of Concurrent Aerobic and Strength Training for Skeletal Muscle Size and Function: An Updated Systematic Review and Meta-Analysis
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Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers
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Autophagy is essential to support skeletal muscle plasticity in response to endurance exercise
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“Although a single bout of high-frequency electrical stimulation or sprint exercise induces a transient increase in Akt (Thr-308/Ser-473) and MTOR (Ser-2448) phosphorylation during the recovery period (32, 102), no change is usually observed after endurance exercise for Akt, whatever the intensity or species (mice/rats…”
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“In light of these findings, Atherton et al. (2005) proposed the ‘‘AMPK-PKB switch’’ hypothesis as a mechanism that partially mediates specific adaptations to endurance and resistance training.”
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The Role of mTORC1 in Regulating Protein Synthesis and Skeletal Muscle Mass in Response to Various Mechanical Stimuli
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“While this study suggests a dissociation between post-stimulation protein synthesis and mTORC1 signaling, the reduced mTORC1 signaling may, in part, be due to the absence of amino acids in the incubating medium (Atherton et al. 2005).”
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Defining meal requirements for protein to optimize metabolic roles of amino acids
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“and the 4E binding protein 1 (4EBP1) (66, 69, 70).”
Contraction intensity and feeding affect collagen and myofibrillar protein synthesis rates differently in human skeletal muscle
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“Even though hypertrophy only is manifested, or more rightly so; measurable, after 4–6 weeks of intensive resistance training from the untrained state (Seynnes et al., 2007), the processes leading to hypertrophy commence already within the first exercise session (Atherton et al., 2005).”
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Role of AMP-activated protein kinase in healthy and diseased hearts
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“Although the role of AMPK activation during ischemia has not been clearly defined, AMPK activation may be beneficial in ischemia due to increased GLUT4 translocation to the plasma membrane (5) and the potential inhibition of glycogen synthesis (6), which increases glucose supply for ATP production via glycolysis (7).”
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Mechanical stimuli of skeletal muscle: implications on mTOR/p70s6k and protein synthesis
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Novel, high-intensity exercise prescription improves muscle mass, mitochondrial function, and physical capacity in individuals with Parkinson's disease
Kelly, N. A., Ford, M. P., Standaert, D. G., Watts, R. L., Bickel, C. S., Moellering, D. R., Tuggle, S. C., Williams, J. Y., Lieb, L., Windham, S. T., et al. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01277.2013 · Cited by 128
“However, because divergent cell signaling mechanisms 87 (5, 17) and transcriptional programs (64) are thought to drive RT-induced myofiber hypertrophy vs.”
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Activation of AMP-activated protein kinase by metformin protects against global cerebral ischemia in male rats: Interference of AMPK/PGC-1α pathway
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Differences in electrical stimulation thresholds between men and women
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“Frequencies of 10 and 75Hz were considered representative of low-frequency (LF) ES,(12) which is generally used to mimic endurance exercise,(13) and highfrequency (HF) ES,(14) which is generally adopted to mimic resistance exercise.(13) Following electrode positioning and instructions, current amplitude (in mA) was pr…”
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Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle
Coffey, V. G., Pilegaard, H., Garnham, A. P., O'Brien, B. J., & Hawley, J. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.91221.2008 · Cited by 116
“Moreover, the increases in isoform-specific Akt1 phosphorylation with resistance but not endurance exercise is indicative of the capacity for highintensity, low-volume contraction to promote an anabolic response in skeletal muscle (3, 9) (Fig.”
BackgroundInfluential
A Novel Bioreactor for Stimulating Skeletal Muscle In Vitro
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Phosphoproteomics of three exercise modalities identifies canonical signaling and C18ORF25 as an AMPK substrate regulating skeletal muscle function
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BackgroundInfluential
Resistance exercise induced mTORC1 signaling is not impaired by subsequent endurance exercise in human skeletal muscle
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“Furthermore, resistance exercise in rats, as well as high-frequency stimulation of skeletal muscle in vitro, has also been reported to increase Akt and mTOR phosphorylation (Bolster et al. 2003, Atherton et al. 2005).”
BackgroundInfluential

Authors: Atherton, P. J., Babraj, J. A., Smith, K., Singh, J., Rennie, M. J., & Wackerhage, H.
Affiliations: University of Nottingham (GB)
University of Dundee (GB)
University of Lancashire (GB)
ORCID: Atherton, Philip J.
Babraj, John A.
Smith, Kenneth
Singh, Jaipaul
Rennie, Michael J.
Wackerhage, Henning
Venue: The FASEB Journal
Publisher: Wiley
Published: 2005-02-16
Volume: 19
Issue: 7
Pages: 1-23
ISSN: 0892-6638 (ISSN-L)
1530-6860
DOI: 10.1096/fj.04-2179fje
OpenAlex: W2115928938
Cited by: 475
References: 62
Citations by year: 2026: 9 · 2025: 11 · 2024: 10 · 2023: 21 · 2022: 15 · 2021: 15 · 2020: 18 · 2019: 25 · 2018: 35 · 2017: 16 · 2016: 22 · 2015: 20 · 2014: 30 · 2013: 33 · 2012: 23
FWCI: 12.47
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The FASEB Journal (publishedVersion)
PubMed (publishedVersion)
CLOK (University of Central Lancashire) (submittedVersion)
Funders: National Institutes of Health (AR 49869)
Biotechnology and Biological Sciences Research Council
Diabetes UK
Tenovus
University of Central Lancashire
University of Dundee
Topics: Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Keywords: AMPK/PGC-1α signaling, neuromuscular electrical stimulation, high-frequency stimulation, low-frequency stimulation, endurance training adaptation, resistance training adaptation, muscle protein synthesis, muscle hypertrophy, mitochondrial biogenesis, UCP3, translational regulation, p70S6K, 4E-BP1
MeSH terms: Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Tuberous Sclerosis Complex 2 Protein, Adaptation, Physiological, Adenylate Kinase, Animals, Electric Stimulation, Enzyme Activation, Physical Exertion, Male, Muscle Contraction, Muscle Proteins, Myofibrils, Phosphorylation, Physical Conditioning, Animal, Physical Endurance, Protein Kinases, Sarcoplasmic Reticulum, Transcription Factors, Signal Transduction, RNA-Binding Proteins, Rats, Wistar, Muscle, Skeletal, Mitogen-Activated Protein Kinases, Tumor Suppressor Proteins, Proto-Oncogene Proteins c-akt, Rats, TOR Serine-Threonine Kinases

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Selective activation of AMPK‐PGC‐1α or PKB‐TSC2‐mTOR signaling can explain specific adaptive responses to endurance or resistance training‐like electrical muscle stimulation

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