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CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function
Open accessAbstract
MyoD , a master regulator of myogenesis, exhibits a circadian rhythm in its mRNA and protein levels, suggesting a possible role in the daily maintenance of muscle phenotype and function. We report that MyoD is a direct target of the circadian transcriptional activators CLOCK and BMAL1, which bind in a rhythmic manner to the core enhancer of the MyoD promoter. Skeletal muscle of Clock Δ19 and Bmal1 −/− mutant mice exhibited ∼30% reductions in normalized maximal force. A similar reduction in force was observed at the single-fiber level. Electron microscopy (EM) showed that the myofilament architecture was disrupted in skeletal muscle of Clock Δ19 , Bmal1 −/− , and MyoD −/− mice. The alteration in myofilament organization was associated with decreased expression of actin, myosins, titin, and several MyoD target genes. EM analysis also demonstrated that muscle from both Clock Δ19 and Bmal1 −/− mice had a 40% reduction in mitochondrial volume. The remaining mitochondria in these mutant mice displayed aberrant morphology and increased uncoupling of respiration. This mitochondrial pathology was not seen in muscle of MyoD −/− mice. We suggest that altered expression of both Pgc-1α and Pgc-1β in Clock Δ19 and Bmal1 −/− mice may underlie this pathology. Taken together, our results demonstrate that disruption of CLOCK or BMAL1 leads to structural and functional alterations at the cellular level in skeletal muscle. The identification of MyoD as a clock-controlled gene provides a mechanism by which the circadian clock may generate a muscle-specific circadian transcriptome in an adaptive role for the daily maintenance of adult skeletal muscle.
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“The functional significance of disrupting the molecular clock has been shown in genetic mouse models (i.e., Clock mutant mice and the Bmal1 KO mouse), which display reduced glucose tolerance, mitochondrial respiratory function, and skeletal muscle contractile function [20,21].”
From Exercise mitigates sleep-loss-induced changes in glucose tolerance, mitochondrial function, sarcoplasmic protein synthesis, and diurnal rhythms (2021) · cites this paper as [21]
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“Considering the negative metabolic consequences, such as reduction in insulin sensitivity and mitochondrial function, attributed to both circadian misalignment and sleep loss [21,67] and the potential benefits of exercise in this context [17,68], further research is warranted.”
From Exercise mitigates sleep-loss-induced changes in glucose tolerance, mitochondrial function, sarcoplasmic protein synthesis, and diurnal rhythms (2021) · cites this paper as [21]
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Self-citationGenome Architecture Leads a Bifurcation in Cell IdentityPreprint
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Molecular and Phenotypic Changes in FLExDUX4 Mice
Murphy, K. M., Zhang, A., Bittel, A. J., & Chen, Y. (2023) · Journal of Personalized Medicine · doi:10.3390/jpm13071040 · Cited by 6
“Misregulation in circadian rhythm signaling in young FLExDUX4 mice could contribute to impaired muscle maintenance, as MyoD1 is a documented Clock transcriptional target [92].”
BackgroundAlbuquerque, T., Neves, A. R., Paul, M., Biswas, S., Vuelta, E., García‐Tuñón, I., Sánchez‐Martín, M., Quintela, T., & Costa, D. R. B. (2023) · Journal of Functional Biomaterials · doi:10.3390/jfb14070362 · Cited by 6
“Other authors have successfully knocked down Bmal1 [48,49].”
Backgroundvan Ooijen, G., Martin, S. F., Barrios-Llerena, M. E., Hindle, M., Bihan, T. L., O'Neill, J. S., & Millar, A. J. (2013) · BMC Cell Biology · doi:10.1186/1471-2121-14-46 · Cited by 7
“*** [36-41], rhythmic expression in following mouse cell types: liver (l), aorta (a), brown adipose (ba), adrenal gland (ag), distal colon (d), heart (h), kidney (k), NIH3T3 (n), brain stem (bs), SCN (s), lung (lu), hypothalamus (hy), pituitary (p), skeletal muscle (sm).”
BackgroundKawada, T., Takamori, Y., Nakade, M., Tsuji, F., Krejčí, M., Noji, T., Takeuchi, H., & Harada, T. (2016) · International Journal of Psychological Studies · doi:10.5539/ijps.v8n3p154 · Cited by 6
“Recently, a mutant mouse created by a reduction of the BMAL1 gene that encodes proteins regulating circadian rhythm was reported to show about a 30% of reduction in muscle force and 40% reduction in mitochondrial volume (Andrews et al., 2010).”
BackgroundYu, Z., Sunchu, B., Fok, W. C., Alshaikh, N., & Pérez, V. (2015) · SpringerPlus · doi:10.1186/s40064-015-0909-7 · Cited by 6
“For example, clock genes are involved in regulating glucose metabolism in the liver (Rudic et al. 2004; Lamia et al. 2008; Zhang et al. 2010), and are essential for the maintenance of normal mitochondrial biogenesis and respiratory function in skeletal muscle (Andrews et al. 2010).”
BackgroundParaoxonase 1 (PON1) and pomegranate influence circadian gene expression and period length
Loizides‐Mangold, U., Koren-Gluzer, M., Skarupelova, S., Makhlouf, A., Hayek, T., Aviram, M., & Dibner, C. (2016) · Chronobiology International · doi:10.3109/07420528.2016.1154067 · Cited by 6
“In Clock and Bmal1 mutant mice, the observed effects include alteration in myofilament organization and reduction in mitochondrial volume and respiration (Andrews et al., 2010).”
BackgroundBao, L., Wang, J., Bin, S.-Y., Li, Y., Chu, W., & Zhang, J. (2018) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2018.07.006 · Cited by 6
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Khatri, S., Das, S., Singh, A., Ahmad, M. F., Kashiv, M., Laxman, S., & Kolthur‐Seetharam, U. (2025) · The FASEB Journal · doi:10.1096/fj.202402930r · Cited by 5
“Although muscle activity and mitochondrial functions have been independently shown to display circadian dependence, 20 whether mitochondrial energetics contributes to muscle capacity in a time- of- the- day-dependent manner has not been investigated, thus far.”
Circadian disruption in astronauts: Causes, molecular mechanisms, and neurocognitive consequences
Tomaraei, S. N., Ahmed, M., & Nami, M. (2025) · Chronobiology International · doi:10.1080/07420528.2025.2569695 · Cited by 5
“PER 2 mutations correlate with altered sleep onset and recovery responses, while BMAL 1 deletions connect to memory deficits and skeletal muscle abnormalities (Andrews et al. 2010; Marcheva et al. 2010).”
Mănescu, D. C., Stoian, M., Rădulescu, M. L., Dinciu, C. C., Mărgărit, I. R., Năstase, M., & Mănescu, C. O. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27104415 · Cited by 7
“Loss of BMAL1 or CLOCK signaling in muscle reduces specific force, disrupts sarcomeric organization, lowers mitochondrial volume and respiration, and impairs insulin-stimulated glucose uptake, partly through effects on GLUT4, TBC1D1, pyruvate dehydrogenase control, and SIRT1-linked pathways [62–67].”
InfluentialBrangaccio, J. A., Phipps, A. M., Gemoets, D. E., Sniffen, J., & Thompson, A. K. (2024) · Experimental Brain Research · doi:10.1007/s00221-024-06777-z · Cited by 5
“…(Bailey and Heitkemper 2001), sleep/wake cycle (Santhi et al. 2016), and torque/force production (Freivalds et al. 1983; Gauthier et al. 1996, 2001; Martin et al. 1999; Guette et al. 2005b; Lagerquist et al. 2006; Sedliak et al. 2008; Andrews et al. 2010; Hodge et al. 2019; Douglas et al. 2021).”
BackgroundCircadian rhythms, feeding patterns and metabolic regulation: implications for critical care
Smith, H., & Betts, J. A. (2024) · Proceedings of The Nutrition Society · doi:10.1017/s002966512400750x · Cited by 6
“Loss of key clock proteins, such as Bmal1 , leads to an accelerated sarcopenic phenotype with age in mice (36) , and impairs various aspects essential for proper muscle performance, including sarcomeric structure, mitochondrial morphology and muscle contractile activities (37) .”
Analyses of the circadian clock genes expression in whole embryos and maternal major tissues of mice
Cao, X., Yan, Y., Luo, X., Yang, X., Cui, H., Yang, Y., & Li, H. (2022) · Journal of Molecular Histology · doi:10.1007/s10735-022-10065-x · Cited by 5
“Positive proof is growing that links inflammation, cancer and metabolic disease with altered the expression of circadian clock gene in peripheral tissues, for example skeletal muscle (Andrews et al. 2010).”
BackgroundZhu, X., Liu, J., Cai, M., Bao, L., Pan, Y., Wu, P., Chu, W., & Zhang, J. (2022) · British Journal Of Nutrition · doi:10.1017/s0007114522003646 · Cited by 5
“When circadian clocks are disrupted, the type of muscle fibre, the structure of sarcomeric and the function of the muscle are all affected(31,32).”
Pinto, A. P., Muñoz, V. R., Tavares, M. E. A., Neto, I. V. D. S., dos Santos, J. R., Rodrigues, G. S., Carolino, R. O. G., Alberici, L. C., Simabuco, F. M., Teixeira, G. R., et al. (2024) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.70001 · Cited by 4
“59 BMAL1 plays an important role in sustaining metabolic homeostasis, decreasing glucose and insulin sensitivity 60 and compromising mitochondrial respiration 61 in the liver and skeletal muscle of tissue-specific knock-out (KO) mice.”
Choi, Y., Lee, S., & Kim, E. (2025) · Nutrients · doi:10.3390/nu17223571 · Cited by 4
“In skeletal muscle, these molecular oscillations regulate mitochondrial oxidative phosphorylation, antioxidant defense, and myogenic differentiation [26–30].”
Shaping mitochondria through fed–fast and circadian cycles
Khatri, S., Kazi, R. S., & Kolthur‐Seetharam, U. (2023) · Biochemical Journal · doi:10.1042/bcj20220378 · Cited by 4
Potential role of Akt in the regulation of fibroblast growth factor 21 by berberine
Hirai, T., Wang, W., Murono, N., Iwasa, K., & Inoue, M. (2023) · Journal of Natural Medicines · doi:10.1007/s11418-023-01755-1 · Cited by 4
Douglas, C. M., Bird, J. E., Kopinke, D., & Esser, K. A. (2024) · PLoS ONE · doi:10.1371/journal.pone.0300348 · Cited by 5
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“MyoD may act as a molecular link between the circadian clock and skeletal muscle maintenance (Andrews et al. 2010).”
BackgroundInfluentialBioinformatics and Systems Biology of Circadian Rhythms: BIO_CYCLE and CircadiOmics
Samad, M., Agostinelli, F., & Baldi, P. (2012) · Methods in molecular biology · doi:10.1007/978-1-0716-2249-0_5 · Cited by 4
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Evodiamine promotes differentiation and inhibits proliferation of C2C12 muscle cells
Yao, X., Yu, T., Zhao, C., Li, Y., Peng, Y., Xi, F., & Yang, G. (2017) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2017.3321 · Cited by 4
“Based on these findings, Evo does not have any influence on the mRNA expression of MyoD , a skeletal muscle‑specific early transcription factor that has a transcriptional regulation effect on the myogenic program (20).”
New Aquaculture Technology Based on Host-Symbiotic Co-metabolism
Mekuchi, M., Asakura, T., & Kikuchi, J. (2019) · Springer eBooks · doi:10.1007/978-981-13-8134-8_13 · Cited by 4
Oribello, J. (2021) · San José State University ScholarWorks (San Jose State University) · doi:10.31979/etd.d4e7-x2g3 · Cited by 4
A familial natural short sleep mutation in dec2 extends healthspan and lifespan in Drosophila
Pandey, P., Wall, P. K., Lopez, S. R., Zunica, E. R. M., Dubuisson, O. S., Dantas, W. S., Davuluri, G., Taylor, A. L., Wall, T. K., Juge, H. J., et al. (2025) · iScience · doi:10.1016/j.isci.2025.113388 · Cited by 4
Progress in understanding how clock genes regulate aging and associated metabolic processes
Su, Y., Wang, M., Chen, J., Bao, Y., Wen, R., Ren, H., & Luan, Z. (2025) · Frontiers in Physiology · doi:10.3389/fphys.2025.1654369 · Cited by 4
Fitzgerald, L. S., Spurrier, C. S. R., Lau, N., Melamed, M. D., Burnett, L. A., Meyer, G. A., Gui, C., Hevener, A. L., Sanford, J. A., & Schenk, S. (2025) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00027.2025 · Cited by 3
Physical inactivity and breakfast skipping caused visceral fat accumulation in rats
Nakajima, S., Hanzawa, F., Ikeda, S., & Oda, H. (2024) · Scientific Reports · doi:10.1038/s41598-024-68058-7 · Cited by 4
“The Bmal1 knock-out and Clock mutation mice were decreased muscle strength and mitochondrial volume 54 , and the Rev-erba deficient mice were decreased muscle mass with the enhancement of muscle atrophy-related genes 55 .”
Kahn, R. E., Zhu, P., Roy, I., Peek, C. B., Hawley, J. A., & Dayanidhi, S. (2025) · The FASEB Journal · doi:10.1096/fj.202402145rr · Cited by 5
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Are Obese Mothers of Children Aged 1-6 Years Evening-Typed?
Nakade, M., Hiraoka, M., Kawasaki, K., 上里拓也, Wada, K., Krejčí, M., Noji, T., Taniwaki, N., Takeuchi, H., & Harada, T. (2015) · International Journal of Psychological Studies · doi:10.5539/ijps.v7n2p121 · Cited by 3
“Recently, a mutant mouse created by a reduction of the BMAL1 gene that encodes proteins regulating circadian rhythm was reported to show about a 30% of reduction in muscle force and 40% reduction in mitochondrial volume (Andrews et al., 2010).”
BackgroundThe effect of voluntary exercise on light cycle stress-induced metabolic resistance
Moon, H. Y., & Jeong, I. C. (2023) · Physical Activity and Nutrition · doi:10.20463/pan.2023.0022 · Cited by 3
Acute exercise modulates Trim63 and Bmal1 in the skeletal muscle of IL-10 knockout mice
da Mata, G. E., Brícola, R. S., Ribeiro, D. N., Simabuco, F. M., Pauli, J. R., de Freitas, E. C., Ropelle, E. R., da Silva, A. S. R., & Pinto, A. P. (2023) · Cytokine · doi:10.1016/j.cyto.2023.156484 · Cited by 4
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“…and muscle Arnt-like protein-1 ( BMAL1 ) and circadian locomotor output cycles kaput ( CLOCK ) directly target myogenic differentiation 1 ( MyoD , a master regulator of myogenesis), and their disruption can result in structural and functional alterations of skeletal muscle (Andrews et al., 2010).”
Metadata
- Authors
- Andrews, J. L., Zhang, X., McCarthy, J. J., McDearmon, E. L., Hornberger, T. A., Russell, B., Campbell, K. S., Arbogast, S., Reid, M. B., Walker, J. R., Hogenesch, J. B., Takahashi, J. S., & Esser, K. A.
- Affiliations
- University of Illinois Chicago (US)
- University of Kentucky (US)
- Northwestern University (US)
- Genomics Institute of the Novartis Research Foundation (US)
- University of Pennsylvania (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-10-18
- Volume
- 107
- Issue
- 44
- Pages
- 19090-19095
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2973897
- OpenAlex
- W2053866174
- Cited by
- 389
- References
- 49
- Citations by year
- 2026: 30 · 2025: 29 · 2024: 31 · 2023: 28 · 2022: 36 · 2021: 26 · 2020: 25 · 2019: 19 · 2018: 27 · 2017: 23 · 2016: 32 · 2015: 20 · 2014: 19 · 2013: 17 · 2012: 15
- FWCI
- 6.39
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (5p50mh074924-05)
- National Heart, Lung, and Blood Institute (HL45721, R01HL045721)
- National Institute of Mental Health (U01MH061915, P50 MH-074924, U01 MH 61915)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R03AR053641, R21AR050717, AR050717, R01AR055246, AR-053641)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Keywords
- circadian clock, clocks, Bmal1, MyoD, skeletal muscle, myogenesis, clock-controlled genes, mitochondrial dysfunction, uncoupled respiration, PGC-1α, PGC-1β, muscle force, muscle phenotype
- MeSH terms
- Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Animals, Gene Expression Regulation, Mice, Inbred BALB C, Mitochondria, Muscle, Transcription Factors, Trans-Activators, MyoD Protein, Mice, Knockout, Muscle, Skeletal, Gene Expression Profiling, Muscle Development, Mice, Electron Microscope Tomography, CLOCK Proteins, ARNTL Transcription Factors, Circadian Clocks
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