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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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Citations
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Self-citationHealth Consequences of Circadian Disruption in Humans and Animal Models
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Endocrine Crosstalk Between Skeletal Muscle and the Brain
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BackgroundCircadian timing of metabolism in animal models and humans
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Self-citationDemonstration of a day-night rhythm in human skeletal muscle oxidative capacity
van Moorsel, D., Hansen, J., Havekes, B., Scheer, F. A. J. L., Jörgensen, J. A., Hoeks, J., Schrauwen-Hinderling, V. B., Duez, H., Lefebvre, P., Schaper, N. C., et al. (2016) · Molecular Metabolism · doi:10.1016/j.molmet.2016.06.012 · Cited by 218
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“, fluctuations in [Ca(2) ]) and circadian rhythms (3) may contribute to the functional specialization of mitochondria and the establishment of a cytoarchitectural environment conducive to optimal compartmentalization of energy exchange.”
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Piovezan, R. D., Abucham, J., dos Santos, R. V. T., de Mello, M. T., Tufik, S., & Poyares, D. R. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.07.003 · Cited by 222
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BackgroundCircadian rhythms in mitochondrial respiration
de Goede, P., Wefers, J., Brombacher, E. C., Schrauwen, P., & Kalsbeek, A. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0196 · Cited by 211
“Global Bmal1 KO as well as ClockΔ19-mutant mice showed reduced contractile muscle force and profound reductions in muscle mitochondrial volume and respiratory function, which were associated with altered expression levels of Pgc1a and Pgc1b (Andrews et al. 2010).”
BackgroundInfluentialCircadian Rhythms, the Molecular Clock, and Skeletal Muscle
Harfmann, B. D., Schroder, E. A., & Esser, K. A. (2015) · Journal of Biological Rhythms · doi:10.1177/0748730414561638 · Cited by 211
“Specifically, a significant reduction in state III respiration (ADPstimulated, mmol O2/min/mg protein) in mitochondria isolated from gastrocnemius muscle was observed (Andrews et al., 2010).”
InfluentialSelf-citationCircadian regulation of metabolism
Bailey, S. M., Udoh, U. S., & Young, M. E. (2014) · Journal of Endocrinology · doi:10.1530/joe-14-0200 · Cited by 219
“Investigation of skeletal muscle mitochondria in Bmal1 null and Clock mutant mice reveal reduced volume, altered morphology, and increased uncoupled respiration (Andrews et al. 2010).”
BackgroundCircadian Etiology of Type 2 Diabetes Mellitus
Javeed, N., & Matveyenko, A. V. (2018) · Physiology · doi:10.1152/physiol.00003.2018 · Cited by 219
“Significantly, whole body deletion of Bmal1 is characterized by a striking reduction in skeletal muscle mass, function, and mitochondrial density, which is reversed upon muscle-specific transgenic rescue (2, 63, 90).”
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“Thus, ablation of BMAL1 in mice resulted in decreased fatty acid oxidation and mitochondrial oxygen consumption rates (9, 10).”
BackgroundNohara, K., Mallampalli, V. K. P. S., Nemkov, T. G., Wirianto, M., Yang, J., Ye, Y., Sun, Y., Han, L., Esser, K. A., Mileykovskaya, E., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11926-y · Cited by 185
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“For instance, the skeletal muscle defects seen in Bmal1−/− mice (Andrews et al., 2010) are likely a causative factor in their low activity.”
BackgroundSelf-citationCircadian metabolism in the light of evolution
Gerhart-Hines, Z., & Lazar, M. A. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1007 · Cited by 178
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“The intrinsic molecular clock is most known for its role in regulating cellular metabolism even under constant lighting or feeding conditions [19-26].”
Self-citationPhysiological and Molecular Dissection of Daily Variance in Exercise Capacity
Ezagouri, S., Zwighaft, Z., Sobel, J., Baillieul, S., Doutreleau, S., Ladeuix, B., Golik, M., Vergès, S., & Asher, G. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.03.012 · Cited by 177
“As expected, and in line with previous reports of circadian gene expression profiles from skeletal muscle of mice and humans (Andrews et al., 2010; McCarthy et al., 2007; Perrin et al., 2018; Zhang et al., 2014), we observed considerable changes in gene expression in gastrocnemius of sedentary mice between the early a…”
ResultDevelopment of dilated cardiomyopathy in Bmal1-deficient mice
Lefta, M., Campbell, K. S., Feng, H.-Z., Jin, J.-P., & Esser, K. A. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00238.2012 · Cited by 158
“The germline Bmal1 / mice were previously backcrossed over 10 generations to the C57BL6 background (2).”
Self-citationAcute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle
Picard, M. A., Gentil, B. J., McManus, M. J., White, K., Louis, K. S., Gartside, S. E., Wallace, D. C., & Turnbull, D. M. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00819.2013 · Cited by 145
Intrinsic muscle clock is necessary for musculoskeletal health
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“Our previous work has demonstrated that muscle force per unit cross section (specific force) measured in vitro is significantly reduced in the EDL muscles/muscle fibres of the 12- to 14-week-old Bmal1 KO mouse compared to wild-type controls (Andrews et al. 2010).”
BackgroundMethodInfluentialSelf-citationTranscriptomic analyses reveal rhythmic and CLOCK-driven pathways in human skeletal muscle
Perrin, L., Loizides-Mangold, U., Chanon, S., Gobet, C., Hulo, N., Isenegger, L., Weger, B. D., Migliavacca, E., Charpagne, A., Betts, J. A., et al. (2018) · eLife · doi:10.7554/elife.34114 · Cited by 139
“Previous studies have reported similar observations in either Bmal1-specific muscle KO, or in ClockD19 mutant mice (Kennaway et al., 2007; Dyar et al., 2014; Harfmann et al., 2016).”
BackgroundInfluentialDiurnal Regulation of Lipid Metabolism and Applications of Circadian Lipidomics
Gooley, J. J., & Chua, E. C.-P. (2014) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2014.04.001 · Cited by 140
Circadian disruption in the pathogenesis of metabolic syndrome
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BackgroundEnvironmental 24-hr Cycles Are Essential for Health
Lucassen, E. A., Coomans, C. P., van Putten, M., de Kreij, S. R., van Genugten, J. H. L. T., Sutorius, R. P. M., de Rooij, K. E., van der Velde, M., Verhoeve, S. L., Smit, J. W. A., et al. (2016) · Current Biology · doi:10.1016/j.cub.2016.05.038 · Cited by 131
“Previous studies have linked circadian rhythm with muscle function by examining mice with mutations in their clock genes; specifically, these mice develop structural muscle changes [1, 29, 30] and diminished muscle function [1, 31].”
BackgroundLoss of Bmal1 leads to uncoupling and impaired glucose-stimulated insulin secretion in β-cells
Lee, J., Kim, M.-S., Li, R., Liu, V. Y., Fu, L., Moore, D. D., Ma, K., & Yechoor, V. K. (2011) · Islets · doi:10.4161/isl.3.6.18157 · Cited by 124
“Andrews et al.37 showed a decreased mitochondrial volume associated with a slightly decreased expression of PGC1-α and -β along with a decrease in state III respiration in skeletal muscle of Bmal1-/- mice.”
BackgroundImpaired Glucocorticoid Production and Response to Stress in Arntl-Deficient Male Mice
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Sleep, circadian biology and skeletal muscle interactions: Implications for metabolic health
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“For example, altered sarcomere structure, mitochondrial pathologies, and impaired muscle function have been observed in skeletal muscle of rodents with circadian misalignment [41], while disturbed metabolism and peripheral insulin resistance have been reported in humans [36].”
BackgroundCircadian Control of Mitochondria in Reactive Oxygen Species Homeostasis
Mezhnina, V., Ebeigbe, O. P., Poe, A., & Kondratov, R. V. (2022) · Antioxidants and Redox Signaling · doi:10.1089/ars.2021.0274 · Cited by 123
“Reduced mitochondrial volume, diminished respiration rate, and increased oxidative damage were found in circadian clock mutants (4, 95, 99, 131, 162), which impacted their physiology.”
Requirement for NF-κB in maintenance of molecular and behavioral circadian rhythms in micePreprint
Hong, H., Maury, E., Ramsey, K. M., Perelis, M., Marcheva, B., Omura, C., Kobayashi, Y., Guttridge, D. C., Barish, G. D., & Bass, J. T. (2018) · Genes & Development · doi:10.1101/gad.319228.118 · Cited by 117
“While clock genes operate in many metabolic (Andrews et al. 2010; Perelis et al. 2015) and immune (Yu etal.2013)tissues,genome-wideregulationofclockcycles hasbeenbestcharacterizedinthecontextoflivermetabo-lism (Hughes et al. 2012; Koike et al. 2012; Vollmers et al. 2012).”
CRY1/2 Selectively Repress PPARδ and Limit Exercise Capacity
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Circadian Regulation of Hippocampal-Dependent Memory: Circuits, Synapses, and Molecular Mechanisms
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What time is it? Deep learning approaches for circadian rhythms
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“To mine these new datasets, here we develop and apply machine learning methods to address two questions: (i) which molecular species are periodic? and (ii) what time or phase is”
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“The circadian characteristics of human skeletal myotubes were in accordance with those reported for human primary thyrocytes, pancreatic islets, skin fibroblasts [28,31,35], and for mouse skeletal muscle assessed in vivo [21,22].”
BackgroundKoritala, B. S. C., Porter, K. I., Arshad, O. A., Gajula, R. P., Mitchell, H. D., Arman, T., Manjanatha, M. G., Teeguarden, J., Dongen, H. P. A. V., McDermott, J., et al. (2021) · Journal of Pineal Research · doi:10.1111/jpi.12726 · Cited by 110
Brain and Muscle Arnt-like 1 is a Key Regulator of Myogenesis
Chatterjee, S., Nam, D., Guo, B., Kim, J. M., Winnier, G. E., Lee, J., Berdeaux, R., Yechoor, V. K., & Ma, K. (2013) · Journal of Cell Science · doi:10.1242/jcs.120519 · Cited by 107
“, 2012) indicated that Bmal1 may activate MyoD promoter through a distal enhancer region, they examined involvement of Bmal1 in the regulation of muscle strength and mitochondrial function in mature post-mitotic myofibers (Andrews et al., 2010).”
BackgroundResultInfluentialAoyama, S., & Shibata, S. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00063 · Cited by 108
“Disruption of myofiber architecture (Andrews et al., 2010)”
BackgroundInfluentialNutrient sensing and the circadian clock
Peek, C. B., Ramsey, K. M., Marcheva, B., & Bass, J. T. (2012) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2012.02.003 · Cited by 109
Coupled network of the circadian clocks: a driving force of rhythmic physiology
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Metabolism and exercise: the skeletal muscle clock takes centre stage
Martin, R. A., Viggars, M. R., & Esser, K. A. (2023) · Nature Reviews Endocrinology · doi:10.1038/s41574-023-00805-8 · Cited by 109
Self-citationStem cells and the circadian clock
Weger, M., Diotel, N., Dorsemans, A.-C., Dickmeis, T., & Weger, B. D. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.09.012 · Cited by 101
“Also, expression of the differentiation promoting factor MYOD is under BMAL1 regulation (Andrews et al., 2010), and overexpression of MyoD in Bmal1 KO cells, alone or in concert with WNT activation, enhances expression of the muscle differentiation marker myosin heavy chain (Chatterjee et al.”
BackgroundPrice, K. H., Dziema, H., Aten, S., Loeser, J., Norona, F. E., Hoyt, K. R., & Obrietan, K. H. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.04.027 · Cited by 94
How does sleep help recovery from exercise-induced muscle injuries?
Chennaoui, M., Vanneau, T., Trignol, A., Arnal, P. J., Gomez-Mérino, D., Baudot, C., Perez, J. M., Pochettino, S., Eirale, C., & Chalabi, H. (2021) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2021.05.007 · Cited by 109
Clock mediates liver senescence by controlling ER stress
Yuan, G., Hua, B., Cai, T., Xu, L., Li, E., Huang, Y., Sun, N., Yan, Z., Lü, C., & Qian, R. (2017) · Aging · doi:10.18632/aging.101353 · Cited by 90
“Using Jessica L’s method [15], we constructed mouse Bmal1:Clock or Bmal1:Clock vectors and the Pdia3 luciferase vector and co-transfected them into 293T cells (Figure 4D).”
MethodCLOCK and BMAL1 Regulate Muscle Insulin Sensitivity via SIRT1 in Male Mice
Liu, J., Zhou, B. Z., Yan, M., Huang, R., Wang, Y., He, Z., Yang, Y., Dai, C., Wang, Y., Zhang, F., et al. (2016) · Endocrinology · doi:10.1210/en.2015-2027 · Cited by 90
“CLOCK/BMAL1 has been reported to bind to the core enhancer of MyoD and upregulate its transcription and expression and to be necessary for the maintenance of skeletal muscle phenotype and function (52).”
Consequences of Circadian and Sleep Disturbances for the Cardiovascular System
Alibhai, F. J., Tsimakouridze, E. V., Reitz, C. J., Pyle, W. G., & Martino, T. A. (2015) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2015.01.015 · Cited by 93
“In a similar light, Andrews and colleagues have shown links between skeletal muscles and the circadian clock mechanism.(154) Thus collectively, these studies indicate that the circadian mechanism plays an important and previously unrecognized role in contractile muscle composition and performance.”
BackgroundThe functional significance of the skeletal muscle clock: lessons from Bmal1 knockout models
Schiaffino, S., Blaauw, B., & Dyar, K. A. (2016) · Skeletal Muscle · doi:10.1186/s13395-016-0107-5 · Cited by 92
“It was suggested that these changes are due to loss of function of the muscle-specific regulatory factor MyoD, because similar changes were found in Myod1 null mice and Myod1 was reported to be a target of BMAL1 and to lose its circadian oscillation in Bmal1 KO mice [26].”
BackgroundResultInfluentialCircadian networks in human embryonic stem cell‐derived cardiomyocytes
Dierickx, P., Vermunt, M. W., Muraro, M. J., Creyghton, M. P., Doevendans, P. A., van Oudenaarden, A., Geijsen, N., & Laake, L. W. V. (2017) · EMBO Reports · doi:10.15252/embr.201743897 · Cited by 85
Circadian Regulation of Adult Stem Cell Homeostasis and Aging
Benitah, S. A., & Welz, P.-S. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.05.002 · Cited by 81
“Furthermore, BMAL1 directly or indirectly seems to regulate the expression of MyoD, a central regulator of myogenesis, leading to disrupted myofilament architecture in skeletal muscle of Bmal1-KO mice (Andrews et al., 2010, Schiaffino et al., 2016).”
BackgroundCircadian Rhythms, Skeletal Muscle Molecular Clocks, and Exercise
Schroder, E. A., & Esser, K. A. (2013) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3182a58a70 · Cited by 84
“The CRY and PER proteins constitute the negative arm of the core molecular clock by forming multimers that inhibit CLOCK:BMAL1 transcriptional activity on translocation to the nucleus.”
BackgroundInfluentialSelf-citationWu, C., Kandarian, S. C., & Jackman, R. W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016171 · Cited by 85
“[43].”
The Circadian Nature of Mitochondrial Biology
Manella, G., & Asher, G. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00162 · Cited by 81
“Dependency of mitochondrial morphology on clock genes was also reported in mouse skeletal muscle (28) and heart (17) and is linked to impaired mitochondrial function in these organs.”
Time of Day and Muscle Strength: A Circadian Output?
Douglas, C. M., Hesketh, S. J., & Esser, K. A. (2020) · Physiology · doi:10.1152/physiol.00030.2020 · Cited by 80
Self-citationKornfeld, S. F., Biggar, K. K., & Storey, K. B. (2012) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2012.09.001 · Cited by 80
“As one of the myogenic regulator factors, MyoD is a key regulator of muscle differentiation and maintenance as shown through knockout experiments in mice [31].”
Backgrounddo Amaral, I. P. G., & Johnston, I. A. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00367.2011 · Cited by 80
“mouse, myoD is a direct target of CLOCK and BMAL, which bind in a rhythmic fashion to the core enhancer in the myoD promoter (2, 32).”
InfluentialCircadian regulation of metabolic homeostasis: causes and consequences
Young, M. E., & McGinnis, G. R. (2016) · Nature and Science of Sleep · doi:10.2147/nss.s78946 · Cited by 82
Circadian clock and the onset of cardiovascular events
Takeda, N., & Maemura, K. (2016) · Hypertension Research · doi:10.1038/hr.2016.9 · Cited by 82
De Gasperi, R., Hamidi, S., Harlow, L. M., Ksiezak-Reding, H., Bauman, W. A., & Cardozo, C. P. (2017) · Scientific Reports · doi:10.1038/s41598-017-13105-9 · Cited by 75
Circadian Rhythms, the Molecular Clock, and Skeletal Muscle
Lefta, M., Wolff, G., & Esser, K. A. (2011) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-385940-2.00009-7 · Cited by 77
“PGC1α/β mRNA and protein levels in skeletal muscle oscillate with a circadian period (Andrews et al., 2010; Liu et al., 2007; McCarthy et al., 2007).”
InfluentialSelf-citationAoyama, S., Kim, H., Hirooka, R., Tanaka, M., Shimoda, T., Chijiki, H., Kojima, S., Sasaki, K., Takahashi, K., Makino, S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2021.109336 · Cited by 77
Saner, N. J., Lee, M. J.-C., Kuang, J., Pitchford, N. W., Roach, G. D., Garnham, A., Genders, A. J., Stokes, T., Schroder, E. A., Huo, Z., et al. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101110 · Cited by 68
“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.”
BackgroundSelf-citationPathophysiology of sarcopenia: Genetic factors and their interplay with environmental factors
Aslam, M. A., Ma, E. B., & Huh, J. Y. (2023) · Metabolism · doi:10.1016/j.metabol.2023.155711 · Cited by 76
Brain and muscle Arnt-like 1 promotes skeletal muscle regeneration through satellite cell expansion
Chatterjee, S., Yin, H., Nam, D., Li, Y., & Ma, K. (2014) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.08.041 · Cited by 74
Lowe, M. G., Lage, J., Paatela, E., Munson, D., Hostager, R., Yuan, C., Katoku-Kikyo, N., Ruíz-Estévez, M., Asakura, Y., Staats, J., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.077 · Cited by 69
“However, previous works on the circadian regulation of myogenesis were primarily concerned with transcriptional activation of MyoD by Clock/Bmal1 (Andrews et al., 2010; Chatterjee et al., 2013; Lefta et al., 2011).”
BackgroundResultInfluentialExercise timing and circadian rhythms
Wolff, C. A., & Esser, K. A. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.04.020 · Cited by 69
“Endurance exercise increases PGC1α, which is a clock-controlled gene in skeletal muscle [35].”
BackgroundSelf-citationCircadian rhythms affect bone reconstruction by regulating bone energy metabolism
Luo, B., Zhou, X., Tang, Q., Yin, Y., Feng, G., Li, S., & Chen, L. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-03068-x · Cited by 72
Pastore, S., & Hood, D. A. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01505.2012 · Cited by 66
Bone-Muscle Mutual Interactions
Lara-Castillo, N., & Johnson, M. L. (2020) · Current Osteoporosis Reports · doi:10.1007/s11914-020-00602-6 · Cited by 70
Daily Rhythmicity of Clock Gene Transcripts in Atlantic Cod Fast Skeletal Muscle
Lazado, C. C., Kumaratunga, H. P. S., Nagasawa, K., Babiak, I., Giannetto, A., & Fernandes, J. M. O. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099172 · Cited by 68
“The grey box indicates that the mechanism underlying this regulatory process remains to be identified. doi:10.1371/journal.pone.0099172.g008 orthologs in central and peripheral tissues such as in goldfish ( Carassius auratus ) [29], European sea bass [10] and zebrafish [19,38].”
InfluentialGremlin-2 is a BMP antagonist that is regulated by the circadian clock
Yeung, C. C., Gossan, N. C., Lu, Y., Hughes, A. T. L., Hensman, J. J., Bayer, M. L., Kjær, M., Kadler, K. E., & Meng, Q. (2014) · Scientific Reports · doi:10.1038/srep05183 · Cited by 67
Hodge, B. A., Zhang, X., Gutierrez‐Monreal, M. A., Cao, Y., Hammers, D. W., Yao, Z., Wolff, C. A., Du, P., Kemler, D., Judge, A. R., et al. (2019) · eLife · doi:10.7554/elife.43017 · Cited by 68
“Our lab previously reported that BMAL1:CLOCK rhythmically bind to the MyoD1 promoter at the distal core-enhancer region resulting in its robust circadian expression in skeletal muscle (Andrews et al., 2010; Zhang et al., 2012).”
BackgroundMethodInfluentialSelf-citationPinealectomy interferes with the circadian clock genes expression in white adipose tissue
de Farias, T. D. S. M., de Oliveira, A. C., Andreotti, S., do Amaral, F. G., Chimin, P., de Proença, A. R. A., Torres‐Leal, F. L., Sertié, R. A. L., Campaña, A. B., Lopes, A. B., et al. (2015) · Journal of Pineal Research · doi:10.1111/jpi.12211 · Cited by 64
The role of clock genes and circadian rhythm in the development of cardiovascular diseases
Takeda, N., & Maemura, K. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1923-1 · Cited by 67
“In addition to the alteration in circadian rhythm, Bmal1-deficient mice display a wide range of organ disorders such as infertility [41], structural and functional alterations in skeletal muscle [42], arthropathy [43], sleep disorder [44] and renal dysfunction [45].”
BackgroundCircadian clock regulation of skeletal muscle growth and repair
Chatterjee, S., & Ma, K. (2016) · F1000Research · doi:10.12688/f1000research.9076.1 · Cited by 67
Ageing and osteoarthritis: a circadian rhythm connection
Gossan, N., Boot-Handford, R., & Meng, Q. (2014) · Biogerontology · doi:10.1007/s10522-014-9522-3 · Cited by 63
“Circadian genes are tissue specific (Yan et al. 2008); it has been postulated that circadian control of tissue specific master transcription factors, such as MyoD in muscle (Andrews et al. 2010) and KLF15 in heart (Jeyaraj et al. 2012), may be one explanation for this phenomena.”
BackgroundInfluence of aging on Bmal1 and Per2 expression in extra-SCN oscillators in hamster brain
Duncan, M. J., Prochot, J. R., Cook, D. H., Smith, J. T., & Franklin, K. M. (2012) · Brain Research · doi:10.1016/j.brainres.2012.11.008 · Cited by 65
“Bmal1 was examined in the present study because deletion of this gene causes profound alterations in the structure and function of skeletal muscle (Andrews et al., 2010; Kondratov et al., 2006).”
BackgroundMaster control: transcriptional regulation of mammalian Myod
Wardle, F. C. (2019) · Journal of Muscle Research and Cell Motility · doi:10.1007/s10974-019-09538-6 · Cited by 64
Mitochondrial dynamics in skeletal muscle insulin resistance and type 2 diabetes
Fealy, C. E., Mulya, A., Axelrod, C. L., & Kirwan, J. P. (2018) · Translational Research · doi:10.1016/j.trsl.2018.07.011 · Cited by 63
Metronidazole Causes Skeletal Muscle Atrophy and Modulates Muscle Chronometabolism
Manickam, R., Oh, H. Y. P., Tan, C. K., Paramalingam, E., & Wahli, W. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082418 · Cited by 66
Zhang, X., Patel, S. P., McCarthy, J. J., Rabchevsky, A. G., Goldhamer, D. J., & Esser, K. A. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1297 · Cited by 67
“Both BMAL1 and CLOCK were found to bind to the MyoD core enhancer (CE) 20 kb upstream (6).”
BackgroundResultInfluentialSelf-citationGlucose Homeostasis: Regulation by Peripheral Circadian Clocks in Rodents and Humans
Gachon, F., Loizides‐Mangold, U., Petrenko, V., & Dibner, C. (2017) · Endocrinology · doi:10.1210/en.2017-00218 · Cited by 63
Mood‐related central and peripheral clocks
Ketchesin, K. D., Becker‐Krail, D. D., & McClung, C. A. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14253 · Cited by 67
“For example, both Bmal1 KO and ClockΔ19 mutant mice have reduced muscle mitochondrial volume and respiratory function and altered levels of pgc1a and pgc1b, key genes involved in mitochondrial biogenesis (Andrews et al., 2010).”
BackgroundConnecting cellular metabolism to circadian clocks
Rey, G., & Reddy, A. B. (2013) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.01.003 · Cited by 60
Guo, W., Wong, S., Li, M., Liang, W., Liesa, M., Serra, C., Jasuja, R., Bartke, A., Kirkland, J. L., Shirihai, O., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051180 · Cited by 59
“Skeletal muscle force capacity is correlated with mitochondrial content and function [28].”
BackgroundShavlakadze, T., Anwari, T., Soffe, Z., Cozens, G. S., Mark, P. J., Gondro, C., & Grounds, M. D. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00027.2013 · Cited by 61
“A circadian pattern of expression has been previously reported for MyoD mRNA and protein, which points to its role in the maintenance of adult skeletal muscle (4, 34).”
BackgroundMiyazaki, M., Schroder, E. A., Edelmann, S. E., Hughes, M. E., Kornacker, K., Balke, C. W., & Esser, K. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027168 · Cited by 58
“Work from this lab recently reported that muscle from Bmal1 and Clock mice exhibit disrupted myofilament architecture and exhibit reduced normalized maximal force [5] demonstrating a role for the molecular clock in maintaining structure and function at the cellular level in skeletal muscle.”
InfluentialSelf-citationLiver and muscle circadian clocks cooperate to support glucose tolerance in mice
Smith, J. G., Koronowski, K. B., Mortimer, T., Sato, T., Greco, C. M., Petrus, P., Verlande, A., Chen, S., Samad, M., Deyneka, E., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112588 · Cited by 58
Ticking for Metabolic Health: The Skeletal‐Muscle Clocks
Gutierrez‐Monreal, M. A., Harmsen, J., Schrauwen, P., & Esser, K. A. (2020) · Obesity · doi:10.1002/oby.22826 · Cited by 63
“Since this early observation, studies have demonstrated that Myod1 is a direct target of the CLOCK:BMAL1 complex (28) and have identified it as a clock cofactor regulating the expression of CCGs in skeletal muscle (29,30).”
BackgroundSelf-citationSkeletal muscle functions around the clock
Mayeuf-Louchart, A., Staels, B., & Duez, H. (2015) · Diabetes Obesity and Metabolism · doi:10.1111/dom.12517 · Cited by 60
“It has been shown that the CLOCK:BMAL1 heterodimer binds a functional E-box present in the core enhancer (CE) of the Myod1 promoter [19,30], inducing circadian oscillations in Myod1 expression.”
BackgroundLarge Polyglutamine Repeats Cause Muscle Degeneration in SCA17 Mice
Huang, S., Yang, S., Guo, J., Yan, S., Gaertig, M. A., Li, S., & Li, X. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.060 · Cited by 55
“In addition, MyoD is present in myotubes, and its level in myotubes is critical for maintaining muscle size and regeneration (Dedkov et al., 2003; Ishido et al., 2004; Legerlotz and Smith 2008; Tanaka et al., 2008; Andrews et al., 2010).”
BackgroundLSD1 Controls Timely MyoD Expression via MyoD Core Enhancer Transcription
Scionti, I., Hayashi, S., Mouradian, S., Girard, E., de Lima, J. E., Morel, V., Simonet, T., Wurmser, M., Maire, P., Ancelin, K., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.078 · Cited by 58
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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