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Acute Exercise Remodels Promoter Methylation in Human Skeletal Muscle
Open accessAbstract
DNA methylation is a covalent biochemical modification controlling chromatin structure and gene expression. Exercise elicits gene expression changes that trigger structural and metabolic adaptations in skeletal muscle. We determined whether DNA methylation plays a role in exercise-induced gene expression. Whole genome methylation was decreased in skeletal muscle biopsies obtained from healthy sedentary men and women after acute exercise. Exercise induced a dose-dependent expression of PGC-1α, PDK4, and PPAR-δ, together with a marked hypomethylation on each respective promoter. Similarly, promoter methylation of PGC-1α, PDK4, and PPAR-δ was markedly decreased in mouse soleus muscles 45 min after ex vivo contraction. In L6 myotubes, caffeine exposure induced gene hypomethylation in parallel with an increase in the respective mRNA content. Collectively, our results provide evidence that acute gene activation is associated with a dynamic change in DNA methylation in skeletal muscle and suggest that DNA hypomethylation is an early event in contraction-induced gene activation.
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“A review of available data suggests that tonic immobility, peritraumatic dissociation, and dissociative PTSD may be mediated by a shared neural network involving amygdala deactivation, absence of sympathetically mediated arousal symptoms (decreased skin conductance and an absence of heart rate increases), parasympathetic activation (a decrease in heart rate in some studies, presumably reflecting a”
From Fear and the Defense Cascade (2015) · cites this paper as [121]
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“The muscle contraction that occurs during exercise also causes intracellular perturbations that disturb metabolic homeostasis, thereby promoting a broad range of adaptive responses and increasing overall resilience in response to stress.157,158”
From Fear and the Defense Cascade (2015) · cites this paper as [157]
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InfluentialMallick, R., & Duttaroy, A. K. (2023) · Neurochemistry International · doi:10.1016/j.neuint.2023.105627 · Cited by 27
“Studies suggested that brain capillaries regulate positive effects on mental health and abilities in neurogenic niches that supply growth factors (e.g., VEGF, GDF11, BDNF) to activate cellular survival pathways to induce gene transcription responsible for neuroplasticity (Chen and Russo-Neustadt,…”
BackgroundPhysical activity may drive healthy microvascular ageing via downregulation of p66Shc
Streese, L., Khan, A. W., Deiseroth, A., Hussain, S., Suades, R., Tiaden, A., Kyburz, D., Hanssen, H., & Cosentino, F. (2020) · European Journal of Preventive Cardiology · doi:10.1177/2047487319880367 · Cited by 21
“Genome-wide studies suggest that regular exercise modulates gene expression in healthy men and women by affecting methylation levels.(11,12) Moreover, we recently demonstrated that 12 weeks of high-intensity interval training (HIIT) improved retinal microvascular phenotype in older individuals with increased CV risk v…”
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High-Throughput Approaches onto Uncover (Epi)Genomic Architecture of Type 2 Diabetes
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“Three hours post-ET, there is a correlation between higher mRNA levels and hypomethylation levels of PCG-1α, indicating that methylation alterations play a role in transcription activation (Barrès et al. 2012).”
InfluentialEpigenetic Alterations in Sports-Related Injuries
Tarnowski, M., Tomasiak, P., Tkacz, M., Zgutka, K., & Piotrowska, K. (2022) · Genes · doi:10.3390/genes13081471 · Cited by 28
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Archacka, K., Ciemerych, M. A., Florkowska, A., & Romańczuk, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111568 · Cited by 22
“However, it seems that physical activity can regulate the expression of various genes by affecting DNA methylation [99], histone modifications [100], miRNA, or lncRNA expression [101–105].”
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Accelerometer-measured Physical Activity, Reproductive Hormones, and DNA Methylation
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Krishna, S. M., Trollope, A. F., & Golledge, J. (2015) · Clinical Science · doi:10.1042/cs20140491 · Cited by 22
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A primer on global molecular responses to exercise in skeletal muscle: Omics in focus
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“In this regard, high-intensity exercise, that is 80% maximal aerobic capacity (VO2max), was linked to promoter hypomethylation of several oxidative genes, fostering oxidative metabolism [75].”
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Caillaud, C., Mechta, M., Ainge, H., Madsen, A. N., Ruell, P., Mas, E., Bisbal, C., Mercier, J., Twigg, S., Mori, T., et al. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0010 · Cited by 19
Self-citationTrajectories of cardiovascular ageing—from molecular mechanisms to clinical implementation
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“…Some of these ncRNAs, such as the miRNA miR-21 and the lncRNA H19, were also associated to CVD and CBVD. 40,44,45 Since epigenetic mechanisms can be manipulated by pharmacological agents, 46,47 lifestyle interventions, 48 or diet, 49 they represent a promising target for ageing-oriented treatments.”
Zhang, J., Tian, Z., Qin, C., & Momeni, M. R. (2024) · Human Cell · doi:10.1007/s13577-024-01057-y · Cited by 21
“Barres et al. [13] looked into the correlation between epigenetic change, Type 2 Diabetes, and physical activity.”
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“It has been reported that acute exercise induced immediate hypomethylation of several genes in skeletal muscle biopsies obtained from healthy individuals (Barres et al., 2012).”
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APOBEC2 negatively regulates myoblast differentiation in muscle regeneration.
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An Old Problem: Aging and Skeletal-Muscle-Strain Injury
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“Another publication provides very interesting observations linking the acute increase in PPARb mRNA with changes in DNA methylation (43).”
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“DNA methylation was recently shown to be a dynamic process that is altered in somatic adult cells in response to environmental factors such as exercise (31).”
BackgroundEpigenetic Advances on Somatic Embryogenesis of Agronomical and Important Crops
Nic-Can, G. I., & De‐la‐Peña, C. (2014) · Springer eBooks · doi:10.1007/978-3-319-07971-4_6 · Cited by 14
“On the other hand, we found that phenolic compounds, such as caffeine, which has been reported to induce DNA hypomethylation (Barrès et al. 2012), hydroxybenzoic acid and trans-cinnamic acid affect DNA methylation and inhibit the SE process in C.”
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Hepatic Gadd45β promotes hyperglycemia and glucose intolerance through DNA demethylation of PGC-1α
Wu, L., Jiao, Y., Li, Y., Jiang, J., Zhao, L., Li, M., Li, B., Yan, Z., Chen, X., Li, X., et al. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20201475 · Cited by 17
Yokoyama, M., Saito, I., Ueno, M., Kato, H., Yoshida, A., Kawamura, R., Maruyama, K., Takata, Y., Osawa, H., Tanigawa, T., et al. (2020) · Journal of Diabetes Investigation · doi:10.1111/jdi.13274 · Cited by 17
Factors Influencing Epigenetic Mechanisms: Is There A Role for Bariatric Surgery?
Metere, A., & Graves, C. E. (2020) · Microarrays · doi:10.3390/ht9010006 · Cited by 17
“Several studies have demonstrated that exercise and nutritional status induce acute changes in DNA methylation patterns in human skeletal muscle [24] and adipose tissue [25], therefore remodeling the epigenome of somatic tissues.”
BackgroundLei, C., Jiao, Y., He, B., Wang, G.-S., Wang, Q., & Wang, J.-C. (2016) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/j.pupt.2016.02.001 · Cited by 17
Jiménez‐Maldonado, A., Cortés, J. C., Castro-Rodríguez, E. M., Montero, S., Muñı́z, J., Rodríguez‐Hernández, A., Lemus, M., & de Álvarez-Buylla, E. R. (2015) · Muscle & Nerve · doi:10.1002/mus.24757 · Cited by 17
“Similarly, exercise reduces the global DNA methylation level in skeletal muscle.(43) We do not reject the possibility that chronic exercise could lower the DNA methylation level in rats, as it led to increased Bdnf muscular transcription in our study (Fig.”
BackgroundEpigenetic crosstalk a molecular language in human metabolic disorders
Sandoval, J. (2015) · Frontiers in Bioscience-Scholar · doi:10.2741/s424 · Cited by 16
“Additionally, another factor to take into account is exercise because it ameliorates metabolic dysfunction and prevents chronic disease throughout epigenetic remodeling (56) (57, 58).”
BackgroundMănescu, D. C. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27020792 · Cited by 17
Extrinsic and intrinsic factors influencing metabolic memory in type 2 diabetes
Vasishta, S., Umakanth, S., Adiga, P. K., & Joshi, M. B. (2021) · Vascular Pharmacology · doi:10.1016/j.vph.2021.106933 · Cited by 21
Opposite Epigenetic Associations With Alcohol Use and Exercise Intervention
Chen, J., Hutchison, K. E., Bryan, A. D., Filbey, F. M., Calhoun, V. D., Claus, E. D., Lin, D., Jing Sui （Beijing Normal University）， my correct affiliation is beijing normal university, N. Q. U. O. S. A. T., Du, Y., & Liu, J. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00594 · Cited by 28
“In skeletal muscle, a decrease of global methylation has been noted after acute exercise (54) and most genes were hypermethylated after a 6-months exercise intervention (55).”
BackgroundKorb, A., Bertoldi, K., Lovatel, G. A., Delevatti, R. S., Elsner, V. R., de Meireles, L. C. F., Kruel, L. F. M., & Siqueira, I. R. (2018) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2018.04.037 · Cited by 21
Sookoian, S., & Pirola, C. (2017) · Hepatobiliary surgery and nutrition · doi:10.21037/hbsn.2017.01.07 · Cited by 16
“Furthermore, recent evidence indicates that transient PPARγ promoter methylation occurs after common events of ordinary life, for instance, physical exercise or caffeine consumption (18).”
BackgroundTranscriptional expression changes of glucose metabolism genes after exercise in thoroughbred horses
Gim, J., Ayarpadikannan, S., Eo, J., Kwon, Y., Choi, Y., Lee, H., Park, K., Yang, Y. M., Cho, B.-W., & Kim, H. (2014) · Gene · doi:10.1016/j.gene.2014.06.051 · Cited by 15
Impaired muscle stem cell function and abnormal myogenesis in acquired myopathies
Deprez, A., Orfi, Z., Rieger, L., & Dumont, N. A. (2022) · Bioscience Reports · doi:10.1042/bsr20220284 · Cited by 23
Lin, Y. L., Zhu, Z. X., Ai, C. H., Xiong, Y. Y., Liu, T. D., Lin, H., & Xia, J. H. (2022) · Marine Biotechnology · doi:10.1007/s10126-022-10188-y · Cited by 20
“It has been shown that low-level methylation of the ppargc1a promoter promotes activation of the gene and increases transcript levels (Santos et al. 2020; Barres et al. 2012).”
BackgroundKrammer, U. D. B., Sommer, A., Tschida, S., Mayer, A., Lilja, S., Switzeny, O. J., Hippe, B., Rust, P., & Haslberger, A. G. (2022) · Sports · doi:10.3390/sports10050073 · Cited by 16
“[31], who also discovered no difference in methylation 48 h after a three-week training program.”
BackgroundAxsom, J., Schmidt, H. D., Matura, L. A., & Libonati, J. R. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.686270 · Cited by 20
“Many of these epigenetic changes target key metabolic genes, including pgc-1alpha (Barres et al., 2012; Denham, 2018).”
BackgroundSmall, L., Ingerslev, L., Manitta, E., Laker, R., Hansen, A. N., Deeney, B., Carrié, A., Couvert, P., & Barrès, R. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009325 · Cited by 15
“Yet, it was speculated that de novo DNA methyltransferase activity was needed to remethylate exercise-demethylated gene promoters and shut down transcription [3].”
BackgroundMethodInfluentialSelf-citationNew Mechanisms of Vascular Dysfunction in Cardiometabolic Patients: Focus on Epigenetics
Ambrosini, S., Mohammed, S. A., Lüscher, T. F., Costantino, S., & Paneni, F. (2020) · High Blood Pressure & Cardiovascular Prevention · doi:10.1007/s40292-020-00400-2 · Cited by 19
Metabolism and chromatin dynamics in health and disease
Rodriguez, H., Rafehi, H., Bhave, M. R., & El‐Osta, A. (2016) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2016.09.004 · Cited by 18
Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications
Álvarez-Venegas, R., Peña, C. D. L., & Casas-Mollano, J. A. (2014) · Cambridge International Law Journal · doi:10.1007/978-3-319-07971-4 · Cited by 15
The Effect of Maternal Diet and Physical Activity on the Epigenome of the Offspring
Panagiotidou, A., Chatzakis, C., Ververi, A., Eleftheriades, M. I., & Sotiriadis, A. (2024) · Genes · doi:10.3390/genes15010076 · Cited by 20
Human skeletal muscle methylome after low carbohydrate energy balanced exercise
Gorski, P., Turner, D., Iraki, J., Morton, J., Sharples, A., & Areta, J. (2023) · bioRxiv · doi:10.1101/2023.01.19.524676 · Cited by 14
“(16, 19), high-intensity (15) and aerobic exercise (18, 23, 24).”
BackgroundNgwa, J. S., Nwulia, E. A., Ntekim, O. E., Bedada, F. B., Kwabi‐Addo, B., Nadarajah, S., Johnson, S. P., Southerland, W. M., Kwagyan, J., & Obisesan, T. O. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.752403 · Cited by 15
“For example, acute intensity exercise can alter the methylation of exercise-responsive genes, resulting in DNA hypomethylation in skeletal muscle (Barres et al., 2012).”
BackgroundTurner, D., Gorski, P., Seaborne, R. A., Viggars, M., Murphy, M., Jarvis, J., Martin, N., Stewart, C., & Sharples, A. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30328 · Cited by 14
“Given that DNA methylation and gene expression are altered after a single bout of resistance (Seaborne et al., 2018b, 2018a) or endurance (Barrès et al., 2012) exercise in vivo, it was hypothesized that acute mechanical loading of fibrin‐bioengineered SkM would evoke methylation and transcriptional…”
BackgroundInfluentialImplementing Precision Medicine in Human Frailty through Epigenetic Biomarkers
García‐Giménez, J. L., Mena, S., Tarazona‐Santabalbina, F. J., Viña, J., Gómez‐Cabrera, M. C., & Pallardó, F. V. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18041883 · Cited by 17
“Exercise-associated decrease in whole genome methylation has been found in muscle biopsies in healthy sedentary individuals after an acute bout of exercise [120,121].”
Altıntaş, A., Laker, R. C., Garde, C., Barrès, R., & Zierath, J. R. (2020) · Epigenomics · doi:10.2217/epi-2019-0391 · Cited by 15
Self-citationTranscriptional memory in skeletal muscle. Don't forget (to) exercise
Beiter, T., Niess, A. M., & Moser, D. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29535 · Cited by 30
“…enhanced transcriptional activity and temporally diminished methylation levels at the promoter regions of a selected set of known metabolic driver genes, including peroxisome proliferator‐activated receptor γ (PPARG) and its “Jack of many trades” cofactor PGC‐1α (PPARGC1A; Barres et al., 2012).”
BackgroundThe Nuclear Receptor Nor-1 Is a Pleiotropic Regulator of Exercise-Induced Adaptations
Pearen, M. A., & Muscat, G. E. O. (2018) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000143 · Cited by 16
Scribbans, T. D., Edgett, B. A., Bonafiglia, J. T., Baechler, B. L., Quadrilatero, J., & Gurd, B. J. (2017) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2016-0455 · Cited by 20
“…genes are acutely up-regulated following supramaximal interval exercise in humans (Psilander et al. 2010, Little et al. 2011), genes targeted by PGC-1α are not systematically increased following lower intensities of exercise (Barrès et al. 2012, Stepto et al. 2012, Popov et al. 2015).”
BackgroundResultInfluentialInheritance of Cytosine Methylation
Tillo, D., Mukherjee, S., & Vinson, C. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25350 · Cited by 16
Senesi, P., Luzi, L., Montesano, A., & Terruzzi, I. (2013) · Endocrine · doi:10.1007/s12020-013-0142-5 · Cited by 14
“[55] demonstrated that acute exercise leads to transient changes in DNA methylation in key genes of skeletal muscle metabolism.”
BackgroundMănescu, D., Plăstoi, C., Petre, R.-L., Margarit, I. R., Mănescu, A. M., & Pîrvan, A. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27041817 · Cited by 13
“The biomarker axes, predicted directions in overdrive, and suggested sampling windowsaregroundedinpublishedevidenceonAMPK–mTORsignaling/autophagy,NAD + partitioning,redoxcontrol, and exercise-induced epigenetic/miRNA remodeling [1,3,6,10,17,19,30,38,61,62,66,68,69,73–78,80,”
Pataky, M. W., Heppelmann, C. J. H., Sevits, K. J., Asokan, A. K., Kumar, A. P., Klaus, K. A., Dasari, S., Kunz, H., Strub, M. D., Robinson, M. M., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-60049-0 · Cited by 19
“Previous reports show that although muscle DNA methylation decreases within 20min of acute exercise 35 , at least an hour is needed for detectable changes in the exercise-induced transcription of most mRNA 36,37 .”
Skin Rejuvenation by Modulation of DNA Methylation
Grönniger, E., Max, H., & Lyko, F. (2024) · Experimental Dermatology · doi:10.1111/exd.70005 · Cited by 13
Hunter, D., James, L., Hussey, B., Ferguson, R., Lindley, M., & Mastana, S. (2023) · Genes · doi:10.3390/genes14020478 · Cited by 13
Zaidan, H., Wnuk, A., Aderka, I. M., Kajta, M., & Gaisler‐Salomon, I. (2023) · Stress · doi:10.1080/10253890.2023.2201325 · Cited by 15
“…to affect global methylation patterns (Blaze et al., 2018, 2013; Doherty et al., 2016; Mychasiuk et al., 2016; Rodrigues et al., 2015), as well as methylation of stress-associated gene promoters in brain, blood and germline cells (Barrès et al., 2012; Day & sweatt, 2010; Miller & sweatt, 2007).”
BackgroundGoing nuclear: Molecular adaptations to exercise mediated by myonuclei
Koopmans, P. J., Zwetsloot, K. A., & Murach, K. A. (2022) · Sports Medicine and Health Science · doi:10.1016/j.smhs.2022.11.005 · Cited by 16
Characterizing skeletal muscle dysfunction in women with polycystic ovary syndrome
McDonnell, T., Cussen, L., McIlroy, M., & O’Reilly, M. (2022) · Therapeutic Advances in Endocrinology and Metabolism · doi:10.1177/20420188221113140 · Cited by 15
Metadata
- Authors
- Barrès, R., Yan, J., Egan, B., Treebak, J. T., Rasmussen, M., Fritz, T., Caidahl, K., Krook, A., O'Gorman, D. J., & Zierath, J. R.
- Affiliations
- University of Copenhagen (DK)
- Karolinska University Hospital (SE)
- Corresponding author
- Zierath, Juleen R.
- ORCID
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2012-03
- Volume
- 15
- Issue
- 3
- Pages
- 405-411
- ISSN
- 1550-4131 (ISSN-L)
- OpenAlex
- W2113728034
- Cited by
- 965
- References
- 32
- Citations by year
- 2026: 65 · 2025: 64 · 2024: 61 · 2023: 39 · 2022: 67 · 2021: 73 · 2020: 53 · 2019: 67 · 2018: 75 · 2017: 79 · 2016: 65 · 2015: 77 · 2014: 76 · 2013: 75 · 2012: 28
- FWCI
- 32.94
- 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)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- DNA methylation, promoter hypomethylation, acute exercise, skeletal muscle, PGC-1α, PDK4, PPARδ, gene expression regulation, muscle contraction, caffeine, soleus muscle, L6 myotubes, epigenetic regulation
- MeSH terms
- Adult, Animals, Female, Humans, Male, Mice, Inbred C57BL, Exercise, Muscle, Skeletal, DNA Methylation, Mice, Young Adult
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