Time of exercise specifies the impact on muscle metabolic pathways and systemic energy homeostasis
Open accessAbstract
While the timing of food intake is important, it is unclear whether the effects of exercise on energy metabolism are restricted to unique time windows. As circadian regulation is key to controlling metabolism, understanding the impact of exercise performed at different times of the day is relevant for physiology and homeostasis. Using high-throughput transcriptomic and metabolomic approaches, we identify distinct responses of metabolic oscillations that characterize exercise in either the early rest phase or the early active phase in mice. Notably, glycolytic activation is specific to exercise at the active phase. At the molecular level, HIF1α, a central regulator of glycolysis during hypoxia, is selectively activated in a time-dependent manner upon exercise, resulting in carbohydrate exhaustion, usage of alternative energy sources, and adaptation of systemic energy expenditure. Our findings demonstrate that the time of day is a critical factor to amplify the beneficial impact of exercise on both metabolic pathways within skeletal muscle and systemic energy homeostasis.
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Physical activity or exercise is linked to muscle clock function.
“Studies are also emerging that link physical activity or exercise to muscle clock function (Wolff and Esser, 2012; Sato et al., 2019).”
From Myosteatosis in the Context of Skeletal Muscle Function Deficit: An Interdisciplinary Workshop at the National Institute on Aging (2020) · cites this paper as Sato et al., 2019
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Li, J., Grant, G. R., Hogenesch, J. B., & Hughes, M. E. (2014) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2014.10.020 · Cited by 54 · see citing works
CircadiOmics: circadian omic web portal
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Self-citationSasaki, H., Ohtsu, T., Ikeda, Y., Tsubosaka, M., & Shibata, S. (2014) · Chronobiology International · doi:10.3109/07420528.2014.935785 · Cited by 46 · see citing works
Oxygen, Metabolism, and Regeneration: Lessons from Mice
Heber‐Katz, E. (2017) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2017.08.008 · Cited by 46 · see citing works
Gan, Z., Powell, F. L., Zambon, A. C., Buchholz, K. S., Fu, Z., Ocorr, K. A., Bodmer, R., Moya, E. A., Stowe, J. C., Haddad, G. G., et al. (2017) · The Journal of Physiology · doi:10.1113/jp274556 · Cited by 13 · see citing works
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Correa-de-Araujo, R., Addison, O., Miljkovic, I., Goodpaster, B. H., Bergman, B. C., Clark, R. V., Elena, J. W., Esser, K. A., Ferrucci, L., Harris-Love, M. O., et al. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00963 · Cited by 468 · see citing works
Exercise Metabolism and Adaptation in Skeletal Muscle
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Atlas of exercise metabolism reveals time-dependent signatures of metabolic homeostasis
Sato, S., Dyar, K. A., Treebak, J. T., Jepsen, S. L., Ehrlich, A. M., Ashcroft, S. P., Trost, K., Kunzke, T., Prade, V. M., Small, L., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2021.12.016 · Cited by 203 · see citing works
Self-citationNoone, J., Mucinski, J. M., DeLany, J. P., Sparks, L. M., & Goodpaster, B. H. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2023.12.025 · Cited by 128 · see citing works
Physical Exercise: A Novel Tool to Protect Mitochondrial Health
Sorriento, D., Di Vaia, E., & Iaccarino, G. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.660068 · Cited by 118 · see citing works
Time-of-day dependent effects of contractile activity on the phase of the skeletal muscle clock
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Yuan, Y., Xu, P., Jiang, Q., Cai, X., Wang, T., Peng, W., Sun, J., Zhu, C., Zhang, C., Yue, D., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019103304 · Cited by 92 · see citing works
“…of plasma metabolites following acute endurance exercise in both clinical and animal models (Lewis et al , 2010; Huffman et al , 2014; Aguer et al , 2017; Duft et al , 2017; Starnes et al , 2017; Sato et al , 2019), which has generated a number of metabolomics “signatures” in the circulation.”
Erickson, M. L., Allen, J. M., Beavers, D. P., Collins, L. M., Davidson, K. W., Erickson, K. I., Esser, K. A., Hesselink, M. K. C., Moreau, K. L., Laber, E. B., et al. (2023) · GeroScience · doi:10.1007/s11357-022-00668-3 · Cited by 47 · see citing works
Self-citationExercise: it's only a matter of time
Saner, N. J., & Lee, M. J. (2020) · The Journal of Physiology · doi:10.1113/jp280366 · Cited by 5 · see citing works
FUNABASHI, D., DOBASHI, S., SAMESHIMA, K., SAGAYAMA, H., NISHIJIMA, T., & MATSUI, T. (2024) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000003487 · Cited by 4 · see citing works
- Authors
- Sato, S., Basse, A. L., Schönke, M., Chen, S., Samad, M., Altıntaş, A., Laker, R. C., Dalbram, E., Barrès, R., Baldi, P., Treebak, J. T., Zierath, J. R., & Sassone-Corsi, P.
- Affiliations
- Inserm (FR)
- University of Copenhagen (DK)
- Karolinska Institutet (SE)
- University of California, Irvine (US)
- ORCID
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2019-07
- Volume
- 30
- Issue
- 1
- Pages
- 92-110.e4
- ISSN
- 1550-4131 (ISSN-L)
- OpenAlex
- W2939723348
- Cited by
- 298
- References
- 93
- Citations by year
- 2026: 42 · 2025: 48 · 2024: 41 · 2023: 44 · 2022: 44 · 2021: 31 · 2020: 39 · 2019: 8 · 2012: 1
- FWCI
- 16.84
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Diabetesförbundet (DIA2015-052)
- Novo Nordisk Fonden (NNF14OC0009941, NNF14OC0011493)
- National Institutes of Health (GM123558)
- Della Martin Foundation
- Vetenskapsrådet (2015-00165)
- Institut National de la Santé et de la Recherche Médicale
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- exercise timing, circadian rhythm, skeletal muscle metabolism, energy homeostasis, glycolysis, HIF-1α, metabolic oscillations, energy expenditure, alternative energy, transcriptomics, metabolomics
- MeSH terms
- Animals, Calorimetry, Indirect, Circadian Rhythm, Energy Metabolism, Glycolysis, Homeostasis, Male, Physical Conditioning, Animal, Software, Mass Spectrometry, Blotting, Western, Lipid Peroxidation, Sequence Analysis, RNA, Muscle, Skeletal, Mice, Hypoxia-Inducible Factor 1, alpha Subunit, Transcriptome
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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