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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BackgroundInfluential
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Background
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Background
Intense Resistance Exercise Induces Early and Transient Increases in Ryanodine Receptor 1 Phosphorylation in Human Skeletal Muscle
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“However, the metabolic and mechanical impact of 70 sec of maximum eccentric contractions differs considerably from extended endurance exercise [31], which might have contributed to the shorter time-course of increased pAMPKThr(172) in the present study.”
Background
Neuromuscular Electrical Stimulation: A New Therapeutic Option for Chronic Diseases Based on Contraction-Induced Myokine Secretion
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“In fact, NMES can activate PGC-1α (the master regulator of mitochondrial biogenesis activated by endurance exercise) as well as the target of rapamycin (mTOR), which in turn activates insulin and IGF-1 receptors (Atherton et al., 2005).”
Background
Targeting mitochondrial quality control for treating sarcopenia: lessons from physical exercise
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Result
Effects of Concurrent Strength and Endurance Training on Genes Related to Myostatin Signaling Pathway and Muscle Fiber Responses
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Background
Effect of High-Frequency Resistance Exercise on Adaptive Responses in Skeletal Muscle
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Result
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“In rat skeletal muscles, lowfrequency electrical stimulation (to mimic endurance training in humans) activated AMPK and increased eEF2 Thr56 phosphorylation [ 2 ].”
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Electrical vs Manual Acupuncture Stimulation in a Rat Model of Polycystic Ovary Syndrome: Different Effects on Muscle and Fat Tissue Insulin Signaling
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Effect of sex differences on human MEF2 regulation during endurance exercise
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Background
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“(1) found that mTOR and S6K1 phosphorylation was increased in rats 3 hours following high frequency stimulations that were designed to mimic RE.”
Untitled work
Baar (2009) · doi:10.1139/h09-035 · Cited by 36
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“Thus, phosphorylation of Akt and mTOR Ser2448 is not always consistent with each other immediately following endurance exercise in muscle.”
BackgroundResult
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“Protein kinase B (Akt/PKB) is a positive regulator of skeletal muscle mass that acts via mTORC1 to activate protein synthesis in response to exercise or feeding (5, 27).”
Background
The Degree of Hydrolysis and Peptide Profile Affect the Anti-Fatigue Activities of Whey Protein Hydrolysates in Promoting Energy Metabolism in Exercise Mice
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Background
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“Exercise (Baar et al., 2002) and in vitro electrical stimulation-induced mitochondrial biogenesis (Atherton et al., 2005; Burch et al., 2010) is thought to be primarily regulated by PGC-1a.”
Background
Impaired regeneration in calpain-3 null muscle is associated with perturbations in mTORC1 signaling and defective mitochondrial biogenesis
YALVAÇ, M. E., Amornvit, J., Braganza, C., Chen, L., Hussain, S.-R. A., Shontz, K. M., Montgomery, C. L., Flanigan, K. M., Lewis, S., & Sahenk, Z. (2017) · Skeletal Muscle · doi:10.1186/s13395-017-0146-6 · Cited by 32
“Akt/mTORC1 and AMPK was noted to act as a “switch” that controls the synthesis of myofibrillar and metabolic proteins [49, 50], implying that the cellular energy status may be crucial in mediating either a low oxidative phenotype and a large size or a high oxidative phenotype and a small size [33].”
Background
Effect of neuromuscular electrical stimulation on skeletal muscle size and function in patients with breast cancer receiving chemotherapy
Toth, M. J., Voigt, T. B., Tourville, T. W., Prior, S. M., Guigni, B. A., Schlosberg, A. V., Smith, I. B., Forest, T. J., Kaufman, P. A., Wood, M. E., et al. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00203.2020 · Cited by 33
Research in the Exercise Sciences
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“Indeed, Atherton et al. (2005) demonstrated that high-frequency electrical stimulation of rat muscle phosphorylated PI3K-Akt and mTOR, promoting an enhancement in translational efficiency.”
Background
High intensity muscle stimulation activates a systemic Nrf2-mediated redox stress response
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“Accordingly, phosphorylation of eEF2 is typically decreased in the recovery period after maximal muscle contractions to facilitate peptide chain elongation (Atherton et al., 2005).”
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“Indeed, in the experimental model system used in hat study, resistance exercise is known to modulate a numer of cell signaling pathways (Atherton et al., 2005; Coffey t al., 2006; Kramer and Goodyear, 2007) and thus it is posible that changes in one of these in addition to mTORC1 ould be necessary to stimulate eIF2B m…”
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“Some studies have found that aerobic exercise attenuates the increases in strength [2,19,20], hypertrophy [2,20] and power [2,19] that occur with resistance training alone, potentially by the attenuation of signaling through the Akt-mTOR-S6K cascade by interference from AMPK-PGC-1a signaling [21].”
Background
AMP-activated protein kinase kinase activity and phosphorylation of AMP-activated protein kinase in contracting muscle of sedentary and endurance-trained rats
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Exhaustive Training Leads to Hepatic Fat Accumulation
da Rocha, A. L., Pinto, A. P., Teixeira, G. R., Pereira, B. C., Oliveira, L. C., Caldo‐Silva, A., Morais, G. P., Cintra, D. E., Pauli, J. R., & da Silva, A. S. R. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25625 · Cited by 29
“Regarding their responses to physical training programs, while the AMPK/PGC-1alpha signaling pathway is mainly related to endurance training JOURNAL OF CELLULAR PHYSIOLOGY adaptations, the Akt/mTOR signaling pathway is mainly related to resistance training adaptations (Atherton et al., 2005).”
Background
H55N polymorphism as a likely cause of variation in citrate synthase activity of mouse skeletal muscle
Ratkevičius, A., Carroll, A. M., Kilikevičius, A., Venckūnas, T., McDermott, K. T., Gray, S. R., Wackerhage, H., & Lionikas, A. (2010) · Physiological Genomics · doi:10.1152/physiolgenomics.00066.2010 · Cited by 28
Integrative effects of resistance training and endurance training on mitochondrial remodeling in skeletal muscle
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“…and high-frequency (mimicking resistance training) electrical stimulations selectively activated AMPK/PGC-1α and Akt/mTOR signals in rodent skeletal muscle respectively, and concluded that high-frequency electrical stimulation had little effect on AMPK/ PGC-1α pathway (Atherton et al. 2005).”
Anabolic responses to acute and chronic resistance exercise are enhanced when combined with aquatic treadmill exercise
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Intradialytic neuromuscular electrical stimulation improves functional capacity and muscle strength in people receiving haemodialysis: a systematic review
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“However, aerobic exercise and RE can (but do not always) elicit divergent intramuscular signaling [172] and fractional MPS [136] responses that correspond with specific training adaptations.”
Skeletal Muscle Physiology: Plasticity and Responses to Exercise
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Activation of mTORC1 signalling in rat skeletal muscle is independent of the EC‐coupling sequence but dependent on tension per se in a dose‐response relationship
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Concomitant aerobic- and hypertrophy-related skeletal muscle cell signaling following blood flow-restricted walking
Barjaste, A., Mirzaei, B., Rahmani-nia, F., Haghniyaz, R., & Brocherie, F. (2020) · Science & Sports · doi:10.1016/j.scispo.2020.03.006 · Cited by 29
Body maintenance and repair: how food and exercise keep the musculoskeletal system in good shape
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“In experiments initiated by colleagues (Henning Wackerhage and Phil Atherton), it has been possible to gain some insight into signalling mechanisms underlying the process (Atherton et al. 2005).”
Background
Resistance exercise and skeletal muscle: protein synthesis, degradation, and controversies
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“Both human and animal studies have widely demonstrated that resistance exercise significantly increases S6K1 expression (Atherton et al. 2005; Camera et al. 2010; Koopman et al. 2006; Li et al. 2022; Terzis et al. 2008).”
Neuromuscular electrical stimulation for muscle wasting in heart failure patients
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“Likewise, increased muscle protein synthesis in response to contraction in rodent muscle occurs in parallel with increased phosphorylation of AKT, mTOR and several downstream signalling proteins in the pathway (Atherton et al. 2005).”
Background
Urolithins: A Prospective Alternative against Brain Aging
An, L., Lu, Q., Wang, K., & Wang, Y. (2023) · Nutrients · doi:10.3390/nu15183884 · Cited by 29
Targeting Mitophagy in Alzheimer’s Disease
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“Alter-nately, the high energy consumption during exercise disrupts the balance between AMP and ATP, leading to AMPK activation followed by induction of PGC-1 (cid:2) [268].”
The use of neuromuscular electrical stimulation (NMES) for managing the complications of ageing related to reduced exercise participation
O’Connor, D., Brennan, L. K., & Caulfield, B. (2018) · Maturitas · doi:10.1016/j.maturitas.2018.04.009 · Cited by 24
“In addition, increased phosphorylation of 5′AMP activated protein kinase (AMPK), which regulates cellular metabolism and can control the activity of PPAR gamma coactivator 1 alpha (PGC 1α), the master regulator of mitochondrial biogenesis [77] has been demonstrated after acute and chronic low frequency NMES [76,78].”
Background
Coordinated alpha-crystallin B phosphorylation and desmin expression indicate adaptation and deadaptation to resistance exercise-induced loading in human skeletal muscle
Jacko, D., Bersiner, K., Schulz, O., Przyklenk, A., Spahiu, F., Höhfeld, J., Bloch, W., & Gehlert, S. (2020) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00087.2020 · Cited by 24
Muscle hypertrophy following blood flow-restricted, low-force isometric electrical stimulation in rat tibialis anterior: role for muscle hypoxia
Nakajima, T., Koide, S., Yasuda, T., Hasegawa, T., Yamasoba, T., Obi, S., Toyoda, S., Nakamura, F., Inoue, T., Poole, D. C., et al. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00972.2017 · Cited by 27
“In general, high-frequency isometric electrical stimulation (60–100 Hz) can induce skeletal muscle hypertrophy (48, 64), whereas lower-frequency electrical stimulation more resembles endurance-like training (5).”
BackgroundMethod
Effects of Arachidonic Acid Supplementation on Acute Anabolic Signaling and Chronic Functional Performance and Body Composition Adaptations
De Souza, E. O., Lowery, R. P., Wilson, J. M., Sharp, M. H., Mobley, C. B., Fox, C. D., Lopez, H. L., Shields, K. A., Rauch, J. T., Healy, J. C., et al. (2016) · PLOS ONE · doi:10.1371/journal.pone.0155153 · Cited by 23
“The exercise model was selected to mimic a strength-training stimulus based on its efficacy in inducing acute increases in protein synthesis and to promote skeletal muscle hypertrophy in a chronic fashion [20, 21].”
Method
The Effects of Combining Aerobic and Heavy Resistance Training on Body Composition, Muscle Hypertrophy, and Exercise Satisfaction in Physically Active Adults
Tan, J., Krasilshchikov, O., Kuan, G., Hashim, H. A., Aldhahi, M. I., Al-Mhanna, S. B., & Badicu, G. (2023) · Healthcare · doi:10.3390/healthcare11172443 · Cited by 23
Trans-omic Analysis Reveals ROS-Dependent Pentose Phosphate Pathway Activation after High-Frequency Electrical Stimulation in C2C12 Myotubes
Hoshino, D., Kawata, K., Kunida, K., Hatano, A., Yugi, K., Wada, T., Fujii, M., Sano, T., Ito, Y., Furuichi, Y., et al. (2020) · iScience · doi:10.1016/j.isci.2020.101558 · Cited by 23
“Exercise has a wide variety of modes such as endurance exercise and resistance exercise; cellular responses are different between each exercise mode (Atherton et al., 2005).”
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Sestrin2, a Regulator of Thermogenesis and Mitohormesis in Brown Adipose Tissue
Ro, S., Semple, I. A., Ho, A., Park, H., & Lee, J. H. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00114 · Cited by 24
“Sestrin2may promotemitochondrial biogenesis through activation of AMPK (7, 12, 101, 102) and subsequent upregulation of PGC-1α activity (103, 104).”
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Autophagy in Skeletal MusclePreprint
Franco‐Romero, A., Sandri, M., & Schiaffino, S. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041565 · Cited by 23
The efficacy and prescription of neuromuscular electrical stimulation (NMES) in adult cancer survivors: a systematic review and meta-analysis
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Active and Passive Tension Interact to Promote Akt Signaling with Muscle Contraction
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Effects of leg immobilization and recovery resistance training on skeletal muscle-molecular markers in previously resistance-trained versus untrained adults
Michel, J. M., Godwin, J. S., Plotkin, D. L., McIntosh, M. C., Mattingly, M. L., Agostinelli, P. J., Mueller, B. J., Anglin, D. A., Kontos, N. J., Berry, A. C., et al. (2025) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00837.2024 · Cited by 20
A primer on global molecular responses to exercise in skeletal muscle: Omics in focus
Murach, K. A., & Bagley, J. R. (2025) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2025.101029 · Cited by 22
Muscle Hypertrophy in a Newly Developed Resistance Exercise Model for Rats
Al‐Sarraf, H., & Mouihate, A. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.851789 · Cited by 21
“However, the metabolic changes that occur at cellular, tissue and organ levels vary considerably between these types of training (Atherton et al., 2005; Coffey et al., 2006; Coffey and Hawley, 2007; Egan and Zierath, 2013).”
Background
Exercise-Induced Decline in the Density of LYVE-1-Positive Lymphatic Vessels in Human Skeletal Muscle
Gehlert, S., Theis, C., Weber, S., Schiffer, T., Hellmich, M., Platen, P., & Bloch, W. (2010) · Lymphatic Research and Biology · doi:10.1089/lrb.2009.0035 · Cited by 21
Acute and Chronic Effects of High Frequency Electric Pulse Stimulation on the Akt/mTOR Pathway in Human Primary Myotubes
Valero‐Breton, M., Warnier, G., Castro‐Sepúlveda, M., Deldicque, L., & Zbinden‐Foncea, H. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.565679 · Cited by 21
“To date, several studies have shown low frequency EPS (0.2–2 Hz) to act as an endurance exercise mimetic (Lambernd et al., 2012; Nikolić et al., 2012; Brown et al., 2015).”
BackgroundInfluential
The effect of interleukin‐6 and the interleukin‐6 receptor on glucose transport in mouse skeletal muscle
Gray, S. R., Ratkevičius, A., Wackerhage, H., Coats, P., & Nimmo, M. A. (2009) · Experimental Physiology · doi:10.1113/expphysiol.2009.048173 · Cited by 22
“The procedures were similar to those previously described (Atherton et al. 2005).”
Method
Effect of a single session of electrical stimulation on activity and expression of citrate synthase and antioxidant enzymes in rat soleus muscle
Pimenta, A. D. S., Lambertucci, R. H., Gorjão, R., Silveira, L. R., & Curi, R. (2007) · European Journal of Applied Physiology · doi:10.1007/s00421-007-0542-4 · Cited by 21
2,6-Dimethoxy-1,4-benzoquinone increases skeletal muscle mass and performance by regulating AKT/mTOR signaling and mitochondrial function
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Repeated and Interrupted Resistance Exercise Induces the Desensitization and Re-Sensitization of mTOR-Related Signaling in Human Skeletal Muscle Fibers
Jacko, D., Schaaf, K., Masur, L., Windoffer, H., Aussieker, T., Schiffer, T., Zacher, J., Bloch, W., & Gehlert, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105431 · Cited by 20
Adiponectin: key role and potential target to reverse energy wasting in chronic heart failure
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“wasting [24] by a mechanism that may involve adenosine monophosphate–activated protein kinase (AMPK) activation [25, 26].”
Whey protein sweetened with Stevia rebaudiana Bertoni (Bert.) increases mitochondrial biogenesis markers in the skeletal muscle of resistance-trained rats
Lima, Y. C., Kurauti, M. A., Alves, G. D. F., Ferezini, J., Piovan, S., Malta, A., de Almeida, F. L. A., Gomes, R. M., Mathias, P. C. D. F., Milani, P. G., et al. (2019) · Nutrition & Metabolism · doi:10.1186/s12986-019-0391-2 · Cited by 20
Nicotinamide Mononucleotide Adenylyltransferase 1 Protects Neural Cells Against Ischemic Injury in Primary Cultured Neuronal Cells and Mouse Brain with Ischemic Stroke Through AMP-Activated Protein Kinase Activation
Liang, J., Wang, P., Jia, W. P., Bao, C., & Han, D. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1569-2 · Cited by 20
Metabolic perturbations in the pathogenesis of hypertrophic cardiomyopathy
Ashrafian, H., & Watkins, H. C. (2005) · Drug Discovery Today Disease Mechanisms · doi:10.1016/j.ddmec.2005.05.014 · Cited by 20
Lopinavir impairs protein synthesis and induces eEF2 phosphorylation via the activation of AMP‐activated protein kinase
Hong‐Brown, L. Q., Brown, C. R., Huber, D. S., & Lang, C. H. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21882 · Cited by 20
“…of eEF2 and eEF2K in response to various stimuli such as low cellular energy level, hypoxia, electrical stimulation [McLeod and Proud, 2002; Atherton et al., 2005; Terai et al., 2005], hormones (e.g., serotonin, phenylephrine) and growth factors [insulin, IGF-I, Wang and Proud, 2002;…”
Background
Myotube growth is associated with cancer-like metabolic reprogramming and is limited by phosphoglycerate dehydrogenase
Stadhouders, L. E. M., Smith, J. A. B., Gabriel, B. M., Verbrugge, S. A. J., Hammersen, T. D., Kolijn, D., Vogel, I. S. P., Mohamed, A. D., de Wit, G. M. J., Offringa, C., et al. (2023) · Experimental Cell Research · doi:10.1016/j.yexcr.2023.113820 · Cited by 19
Improvement in Physical Function After Coronary Artery Bypass Graft Surgery Using a Novel Rehabilitation Intervention
Rengo, J. L., Savage, P. D., Hirashima, F., Leavitt, B. J., Ades, P. A., & Toth, M. J. (2021) · Journal of Cardiopulmonary Rehabilitation and Prevention · doi:10.1097/hcr.0000000000000576 · Cited by 19
Resistance Training Improves Hypertrophic and Mitochondrial Adaptation in Skeletal Muscle
Zhao, Y., & Wu, Y. (2023) · International Journal of Sports Medicine · doi:10.1055/a-2059-9175 · Cited by 20
“Early animal studies demonstrated that, in skeletal muscle, low-frequency electrical stimulation (mimicking endurance training) selectively enhanced AMP-activated protein kinase (AMPK)/peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α) signaling, which activates mitochondrial biogenesis, and that hig…”
Background
Acute vs. chronic hypoxia: What are the consequences for skeletal muscle mass?
Deldicque, L., & Francaux, M. (2013) · doi:10.7457/cmep.v2i1 · Cited by 19
“In order to dissect out the true molecular nature of the interference effect, study designs that incorporate truly divergent signalling paradigms are needed (Atherton et al., 2005) to overcome the clear molecular ‘noise’ that occurs during resistance and cycling exercise studies.”
Background
Eccentric resistance training and β-Hydroxy-β-methylbutyrate free acid affects muscle PGC-1α expression and serum irisin, nesfatin-1 and resistin
Shirvani, H., Rahmati-Ahmadabad, S., Broom, D. R., & Mirnejad, R. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.198424 · Cited by 19
“Resistance training increases phosphorylation of the anabolic Akt/mTOR signalling pathway, as well as activation of the translation initiation regulators p70 S6k, 4E-BP1 and eIF2B (Atherton et al., 2005).”
Background
High-load resistance exercise with superimposed vibration and vascular occlusion increases critical power, capillaries and lean mass in endurance-trained men
Mueller, S. M., Aguayo, D., Lunardi, F., Ruoss, S., Boutellier, U., Frese, S., Petersen, J. A., Jung, H. H., & Toigo, M. (2013) · European Journal of Applied Physiology · doi:10.1007/s00421-013-2752-2 · Cited by 18
“…sclerosis protein 2 (tSc2), which inhibits the mammalian target of rapamycin complex 1 (mtOrc1). the downregulation of the key component in integrating resistance training-activated signaling pathways (mtOr) inhibits the myofibrillar protein synthesis (Atherton et al. 2005; Inoki et al. 2003).”
Background
Branched-chain amino acids administration suppresses endurance exercise-related activation of ubiquitin proteasome signaling in trained human skeletal muscle
Lysenko, E. A., Vepkhvadze, T. F., Lednev, E. M., Виноградова, О. Л., & Popov, D. V. (2016) · The Journal of Physiological Sciences · doi:10.1007/s12576-016-0506-8 · Cited by 18
“The latter effect may be explained by an antagonistic relationship between the signaling pathways regulating mitochondrial biogenesis and protein synthesis [8] as well as endurance exerciseinduced activation of the ubiquitin proteasome system [9–12].”
Background
Low-frequency electrical stimulation of bilateral hind legs by belt electrodes is effective for preventing denervation-induced atrophies in multiple skeletal muscle groups in rats
Uno, H., Kamiya, S., Akimoto, R., Hosoki, K., Tadano, S., Kouzaki, K., Tamura, Y., Kotani, T., Isemura, M., & Nakazato, K. (2022) · Scientific Reports · doi:10.1038/s41598-022-25359-z · Cited by 17
Myogenic, matrix, and growth factor mRNA expression in human skeletal muscle: Effect of contraction intensity and feeding
Agergaard, J., Reitelseder, S., Pedersen, T. G., Doessing, S., Schjerling, P., Langberg, H., Miller, B. F., Aagaard, P., Kjær, M., & Holm, L. (2012) · Muscle & Nerve · doi:10.1002/mus.23667 · Cited by 17
Effect of Resistance Exercise on Muscle Metabolism and Autophagy in sIBM
Jeong, J., YANG, D.-S., Koo, J., Hwang, D.-J., Cho, J., & Kang, E. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001286 · Cited by 17
Early potential effects of resveratrol supplementation on skeletal muscle adaptation involved in exercise-induced weight loss in obese mice
Sun, J., Zhang, C., Kim, M., Su, Y., Qin, L., Dong, J., Zhou, Y., & Ding, S. (2018) · BMB Reports · doi:10.5483/bmbrep.2018.51.4.236 · Cited by 17
The order of concurrent training affects mTOR signaling but not mitochondrial biogenesis in mouse skeletal muscle
Shirai, T., Aoki, Y., Takeda, K., & Takemasa, T. (2020) · Physiological Reports · doi:10.14814/phy2.14411 · Cited by 16
“The characteristic activation pattern of AMPK involves an increase in such occurring immediately after exercise with a return to the basal level at 1 hr after exercise (Atherton et al., 2005).”
BackgroundInfluential
Similar acute physiological responses from effort and duration matched leg press and recumbent cycling tasks
Steele, J., Butler, A., Comerford, Z., Dyer, J. E., Lloyd, N., Ward, J. M., Fisher, J. P., Gentil, P., Scott, C. B., & Ozaki, H. (2018) · PeerJ · doi:10.7717/peerj.4403 · Cited by 18
“There were no significant effects by ‘condition’ for mean RMS amplitude (F(1,6) = 0.”
Background
Protein synthesis a low priority for exercising muscle
Atherton, P. J., & Rennie, M. J. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.110247 · Cited by 17
“…(MAPK) family members (e.g. ERK1/2, p38) (Williamson et al. 2003); proteins of the canonical insulin receptor signalling pathway (e.g. Akt, mTOR) (Atherton et al. 2005); contraction-induced Ca2+-dependent pathways (e.g. PKC, CamK) (Rose et al. 2005) and AMPK (Frosig et al. 2004) to name but a…”
BackgroundResult
Signaling Responses After Varying Sequencing of Strength and Endurance Training in a Fed State
Jones, T. W., Walshe, I. H., Hamilton, D. L., Howatson, G., Russell, M., Price, O. J., Gibson, A. S. C., & French, D. N. (2016) · International Journal of Sports Physiology and Performance · doi:10.1123/ijspp.2015-0534 · Cited by 18
Anabolic and Catabolic Signaling Pathways That Regulate Skeletal Muscle Mass
McCarthy, J. J., & Murach, K. A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813922-6.00024-2 · Cited by 17
An electrical stimulation intervention protocol to prevent disuse atrophy and muscle strength decline: an experimental study in rat
Shi, H., Li, F., Zhang, F., Wei, X., Liu, C., & Duan, R. (2023) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-023-01208-6 · Cited by 15

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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