Obesity Impairs Skeletal Muscle Regeneration Through Inhibition of AMPK
Open accessAbstract
Obesity is increasing rapidly worldwide and is accompanied by many complications, including impaired muscle regeneration. The obese condition is known to inhibit AMPK activity in multiple tissues. We hypothesized that the loss of AMPK activity is a major reason for hampered muscle regeneration in obese subjects. We found that obesity inhibits AMPK activity in regenerating muscle, which was associated with impeded satellite cell activation and impaired muscle regeneration. To test the mediatory role of AMPKα1, we knocked out AMPKα1 and found that both proliferation and differentiation of satellite cells are reduced after injury and that muscle regeneration is severely impeded, reminiscent of hampered muscle regeneration seen in obese subjects. Transplanted satellite cells with AMPKα1 deficiency had severely impaired myogenic capacity in regenerating muscle fibers. We also found that attenuated muscle regeneration in obese mice is rescued by AICAR, a drug that specifically activates AMPK, but AICAR treatment failed to improve muscle regeneration in obese mice with satellite cell–specific AMPKα1 knockout, demonstrating the importance of AMPKα1 in satellite cell activation and muscle regeneration. In summary, AMPKα1 is a key mediator linking obesity and impaired muscle regeneration, providing a convenient drug target to facilitate muscle regeneration in obese populations.
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The AMPKα1 catalytic subunit potentiates myogenic expression, myogenesis, and muscle regeneration.
“This AMPK-mediated muscle cell regeneration is supported by the fact that AMPKα1 catalytic subunit potentiates myogenic expression, myogenesis, and muscle regeneration [59].”
From Mitochondrial Adaptation in Skeletal Muscle: Impact of Obesity, Caloric Restriction, and Dietary Compounds (2024) · cites this paper as [59]
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Self-citationRYAN, T. E., Schmidt, C. A., Green, T. D., Spangenburg, E. E., Neufer, P. D., & McClung, J. M. (2016) · Diabetes · doi:10.2337/db16-0387 · Cited by 55 · see citing works
“These findings are consistent with previous reports demonstrating that chronic HFD impairs muscle regeneration in nonischemic models of muscle injury (50,51).”
ResultDietary Regulation of Adult Stem Cells
Mana, M., Kuo, E. Y.-S., & Yilmaz, Ö. H. (2017) · Current Stem Cell Reports · doi:10.1007/s40778-017-0072-x · Cited by 55 · see citing works
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Self-citationZhao, L., Zou, T., Gomez, N. A., Wang, B., Zhu, M. J., & Du, . (2018) · Nutrition and Diabetes · doi:10.1038/s41387-018-0049-6 · Cited by 54 · see citing works
Self-citationDuan, Q., Song, P., Ye, D., & Zou, M. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13833 · Cited by 50 · see citing works
“Indeed, obesity is known to decrease or inhibit AMPKα in animals (Decleves et al., 2011; Davies et al., 2014; Fu et al., 2016b) and patients (Xu et al., 2012).”
BackgroundIkeda, Y., Satoh, A., Horinouchi, Y., Hamano, H., Watanabe, H., Imao, M., Imanishi, M., Zamami, Y., Takechi, K., Izawa‐Ishizawa, Y., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201802724rr · Cited by 49 · see citing works
“Skeletal muscle regeneration is suppressed duringmuscle wasting because of aging in humans (41) in addition to diabetes (37) andCKD (40) inmice.”
BackgroundWilding, J. P. H., Zourikian, N., Minno, M. N. D. D., Khair, K., Marquardt, N., Benson, G. M., Ozelo, M. C., & Hermans, C. R. J. R. (2018) · Obesity Reviews · doi:10.1111/obr.12746 · Cited by 48 · see citing works
Neonatal vitamin A injection promotes cattle muscle growth and increases oxidative muscle fibers
Wang, B., Nie, W., Fu, X., de Avila, J. M., Ma, Y., Zhu, M. J., Maquivar, M., Parish, S. M., Busboom, J. R., Nelson, M. L., et al. (2018) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-018-0296-3 · Cited by 49 · see citing works
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Self-citationMolecular and biochemical regulation of skeletal muscle metabolism
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DHA alleviates diet-induced skeletal muscle fiber remodeling via FTO/m6A/DDIT4/PGC1α signaling
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The Role of AMPK in Neuromuscular Biology and Disease
Dial, A. G., Ng, S. Y., Manta, A., & Ljubicic, V. (2018) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2018.02.010 · Cited by 43 · see citing works
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Mitochondrial glycerol 3‐phosphate dehydrogenase promotes skeletal muscle regeneration
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Pyruvate dehydrogenase kinase 4 promotes ubiquitin–proteasome system‐dependent muscle atrophy
Sinam, I. S., Chanda, D., Thoudam, T., Kim, M., Kim, B., Kang, H., Lee, J. Y., Baek, S., Kim, S., Shim, B.-J., et al. (2022) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13100 · Cited by 40 · see citing works
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“In contrast, it has been suggested that a permanent reduction in the AMPK pathway leads to insulin resistance(32) and contributes to muscle dysfunction in diet-induced obesity.(33) Our results showed that phospho-AMPK and phospho-AS160 levels were elevated in the skeletal muscle of the RT mice.”
ResultResveratrol improves muscle regeneration in obese mice through enhancing mitochondrial biogenesis
Niu, W., Wang, H., Wang, B., Mao, X., & Du, M. (2021) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2021.108804 · Cited by 39 · see citing works
Systemic Regulators of Skeletal Muscle Regeneration in Obesity
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Brown Fat Promotes Muscle Growth During Regeneration
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Regeneration during Obesity: An Impaired Homeostasis
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“Realtime PCR was performed as previously described [29].”
MethodSelf-citationLiu, X., Zhao, L., Gao, Y., Chen, Y., Tian, Q., Son, J. S., Chae, S. A., de Avila, J. M., Zhu, M. J., & Du, . (2022) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13150 · Cited by 28 · see citing works
“Suppression of AMPK activity in obese mice attenuates satellite cell activity and muscle regeneration.(25) However, the role of AMPK in regulating the proliferation and subsequent apoptosis of FAPs during muscle regeneration remains unexamined.”
BackgroundSelf-citationWang, X., Zhao, D., Cui, Y., Lu, S., Gao, D., & Liu, J. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27012 · Cited by 28 · see citing works
Jun, L., Tao, Y.-X., Geetha, T., & Babu, J. R. (2024) · Current Nutrition Reports · doi:10.1007/s13668-024-00555-7 · Cited by 27 · see citing works
“This AMPK-medi-ated muscle cell regeneration is supported by the fact that AMPKα1 catalytic subunit potentiates myogenic expression, myogenesis, and muscle regeneration [59].”
BackgroundA functional role for AMPK in female fertility and endometrial regeneration
McCallum, M. L., Pru, C. A., Smith, A. R., Kelp, N., Foretz, M., Viollet, B., Du, ., & Pru, J. K. (2018) · Reproduction · doi:10.1530/rep-18-0372 · Cited by 25 · see citing works
“regeneration following damage through its inhibition of AMPK signaling (Fu et al. 2016).”
BackgroundSelf-citationGut Microbiota, Obesity and Bariatric Surgery: Current Knowledge and Future Perspectives
Cătoi, A. F., Vodnar, D. C., Corina, A., Nikolić, D., Citarrella, R., Pérez‐Martínez, P., & Rizzo, M. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666190708190437 · Cited by 25 · see citing works
Oakey, L. A., Fletcher, R. S., Elhassan, Y., Cartwright, D. M., Doig, C. L., Garten, A., Thakker, A., Maddocks, O. D. K., Zhang, T., Tennant, D. A., et al. (2019) · Wellcome Open Research · doi:10.12688/wellcomeopenres.14898.2 · Cited by 24 · see citing works
High Body Mass Index Is Associated with the Extent of Muscle Damage after Eccentric Exercise
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Zhao, J., Yang, Q., Zhang, L., Liang, X., Sun, X., Wang, B., Chen, Y., Zhu, M. J., & Du, . (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.06.149 · Cited by 21 · see citing works
“To achieve Prkaa1 conditional KO, Rosa26-Cre mice (Stock No: 004847, Jackson Lab, Bar Harbor, Maine, US) were crossed with Prkaa1flox/flox mice (Stock no: 014141) to obtain Rosa26Cre/Prkaa1 mice [16], and AMPK KO was induced by tamoxifen injection (75 μg/g body weight).”
Self-citationMallmann, B., Martin, E. M., Kim, K. S., Calderón-Apodaca, N. L., Baxter, M. F. A., Latorre, J. D., Hernández-Velasco, X., Paasch-Martínez, L., Owens, C. M., Dridi, S., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00674 · Cited by 21 · see citing works
Satellite cell function, intramuscular inflammation and exercise in chronic kidney disease
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“Lipotoxicity, caused either by high-fat diets or transgenic mouse models, prolongs muscle regeneration via impaired SC functioning [116, 117].”
BackgroundEffting, P. S., Thirupathi, A., Muller, A. P., Pereira, B. D. C., Sepa-Kishi, D. M., Marqueze, L. F., Vasconcellos, F. F., Nesi, R. T., Pereira, T. C. B., Kist, L. W., et al. (2022) · Nutrients · doi:10.3390/nu14112179 · Cited by 20 · see citing works
Muscle satellite cells are impaired in type 2 diabetic mice by elevated extracellular adenosine
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Oakey, L. A., Fletcher, R. S., Elhassan, Y., Cartwright, D. M., Doig, C. L., Garten, A., Thakker, A., Maddocks, O. D. K., Zhang, T., Tennant, D. A., et al. (2018) · Wellcome Open Research · doi:10.12688/wellcomeopenres.14898.1 · Cited by 20 · see citing works
CREG1 deficiency impaired myoblast differentiation and skeletal muscle regeneration
Song, H., Tian, X., He, L., Liu, D., Li, J., Mei, Z., Zhou, T., Liu, C., He, J., Jia, X., et al. (2024) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13427 · Cited by 19 · see citing works
“AICAR, an AMPK activity agonist, successfully improved muscle regeneration in obese mice 2,34 ; however, AMPK α 1 knockout in satellite cells abolished the positive effect of AICAR administration on skeletal muscle regeneration.”
BackgroundHa, T. K. Q., Pham, H. T. T., Cho, H. M., Tran, V. O., Yang, J., Jung, D., Williams, D. R., & Oh, W. K. (2019) · Scientific Reports · doi:10.1038/s41598-018-37808-9 · Cited by 19 · see citing works
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Natural constituents from food sources: potential therapeutic agents against muscle wasting
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Jun, L., Knight, E., Broderick, T. L., Al‐Nakkash, L., Tobin, B. L., Geetha, T., & Babu, J. R. (2024) · Nutrients · doi:10.3390/nu16121836 · Cited by 17 · see citing works
“Therefore, our study provides insights into the mechanisms by which obesity impairs muscle metabolism and into how exercise counteracts these deleterious effects.”
BackgroundAdult Muscle Stem Cells: Exploring the Links Between Systemic and Cellular Metabolism
Purohit, G., & Dhawan, J. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00312 · Cited by 17 · see citing works
Joseph, J., & Doles, J. D. (2021) · Nutrition & Metabolism · doi:10.1186/s12986-021-00565-0 · Cited by 17 · see citing works
“[86] High-fat diet fed mice Obesity Reduced muscle regeneration and reduced primary satellite cell pool”
BackgroundJin, H., Oh, H., Nah, S.-Y., & Lee, B.-Y. (2021) · Journal of Ginseng Research · doi:10.1016/j.jgr.2021.10.003 · Cited by 17 · see citing works
“459 sarcopenic obesity have resulted in increased interest in dietary components as a strategy to increase mitochondrial energy expenditure in both WAT and skeletal muscle, and prevent obesityinduced skeletal muscle loss to treat both obesity and skeletal muscle atrophy [44].”
BackgroundRole of Diet in Stem and Cancer Stem Cells
Puca, F., Fedele, M., Rasio, D., & Battista, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158108 · Cited by 17 · see citing works
“Conversely, a high-fat diet (HFD) inhibits the AMPK pathway in MuSCs, thus compromising cell activation and muscle regeneration [95].”
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The impact of ageing on lipid-mediated regulation of adult stem cell behavior and tissue homeostasis
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Alcohol intake aggravates adipose browning and muscle atrophy in cancer-associated cachexia
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Pudjihartono, N., Ho, D., Golovina, E., Fadason, T., Kempa-Liehr, A. W., & O'Sullivan, J. M. (2023) · Journal of Autoimmunity · doi:10.1016/j.jaut.2023.103046 · Cited by 14 · see citing works
Muscle regeneration and muscle stem cells in metabolic disease
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AMPKα1 regulates transcription through H2B O-GlcNAcylation during brown adipogenesis
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tBHQ Induces a Hormetic Response That Protects L6 Myoblasts against the Toxic Effect of Palmitate
Posadas-Rodríguez, P., Posadas-Rodríguez, N. E., González‐Puertos, V. Y., Toledo-Pérez, R., Ventura-Gallegos, J. L., Zentella‐Dehesa, A., Gómez-Quiroz, L. E., Königsberg, M., & Luna‐López, A. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/3123268 · Cited by 12 · see citing works
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“In addition, the lack of AMPK in SCs can block normal muscle regeneration after injury [16].”
BackgroundInfluentialDial, A. G., Rooprai, P., Lally, J., Bujak, A. L., Steinberg, G. R., & Ljubicic, V. (2018) · The FASEB Journal · doi:10.1096/fj.201700868rrr · Cited by 11 · see citing works
Kim, K., Ro, B., Damen, F. W., Gramling, D. P., Lehr, T. D., Song, Q., Goergen, C. J., & Roseguini, B. T. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00535.2020 · Cited by 11 · see citing works
Büyükdere, Y., & Akyol, A. (2023) · Nutrition Reviews · doi:10.1093/nutrit/nuad041 · Cited by 11 · see citing works
“73 Acrylamide has significantly reduced the expression levels of AMPK and acetyl-CoA carboxylase phosphorylation in male mice fed a high-fat diet for 10weeks.”
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Importance of Nutrient Availability and Metabolism for Skeletal Muscle Regeneration
Blum, J., Epstein, R., Watts, S. A., & Thalacker‐Mercer, A. E. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.696018 · Cited by 13 · see citing works
Oleate Ameliorates Palmitate-Induced Impairment of Differentiative Capacity in C2C12 Myoblast Cells
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“It can lead to weak activity ability, tumble, and increased mortality [3,4] and is jointly influenced by environmental factors and genetic factors, including hypokinesia, neuro-muscular junction damage, the change of hormone related with age (such as insulin, estrogen and testosterone, growth…”
Free Fatty Acid Impairs Myogenic Differentiation through the AMPK α -MicroRNA 206 Pathway
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Self-citationEffects of hyperoxia and hypoxia on the proliferation of C2C12 myoblasts
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Skeletal muscle RUNX1 is related to insulin sensitivity through its effect on myogenic potential
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“Deletion of AMPKα2 but not AMPKα1 was used, since it is AMPKα2 that is mainly involved in the control of muscle metabolism [20], including the effect of leptin [22], while AMPKα1 is linked to muscle development, hypertrophy and regeneration [48, 49].”
BackgroundResultMetformin regulates myoblast differentiation through an AMPK-dependent mechanism
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REV-ERB and ROR: therapeutic targets for treating myopathies
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- Authors
- Fu, X., Zhu, M., Zhang, S., Foretz, M., Viollet, B., & Du, M.
- Affiliations
- Washington State University (US)
- Centre National de la Recherche Scientifique (FR)
- INSERM U1016, Institut Cochin, Paris, France
- Corresponding author
- Du, Min
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2015-09-17
- Volume
- 65
- Issue
- 1
- Pages
- 188-200
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- PMC
- PMC4686944
- OpenAlex
- W2229640146
- Cited by
- 155
- References
- 47
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 12 · 2023: 12 · 2022: 23 · 2021: 18 · 2020: 15 · 2019: 19 · 2018: 17 · 2017: 13 · 2016: 10
- FWCI
- 5.79
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Diabetes (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Civil War Book Review (submittedVersion)
- Funders
- National Institutes of Health (1R01-HD-067449)
- Topics
- 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
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- obesity, skeletal muscle regeneration, AMPK, AMPKα1, satellite cells, satellite cell activation, muscle damage, AICAR, AMPK activation, myogenesis, therapeutic target
- MeSH terms
- Aminoimidazole Carboxamide, Animals, Cell Differentiation, Flow Cytometry, Hypoglycemic Agents, Immunohistochemistry, Obesity, Regeneration, Ribonucleotides, Immunoblotting, Mice, Knockout, Muscle, Skeletal, Reverse Transcriptase Polymerase Chain Reaction, Muscle Development, Satellite Cells, Skeletal Muscle, Cell Proliferation, Mice, AMP-Activated Protein Kinases, Diet, High-Fat
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