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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Genetic mouse models with disrupted molecular clock (Clock mutant mice and Bmal1 KO mouse) display reduced glucose tolerance, mitochondrial respiratory function, and skeletal muscle contractile function.
“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]
Negative metabolic consequences, such as reduction in insulin sensitivity and mitochondrial function, are attributed to both circadian misalignment and sleep loss.
“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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Obesity and Metabolic Syndrome in Circadian <i>Clock</i> Mutant Mice
Turek, F. W., Joshu, C., Kohsaka, A., Lin, E., Ivanova, G., McDearmon, E., Laposky, A., Losee-Olson, S., Easton, A., Jensen, D. R., et al. (2005) · Science · doi:10.1126/science.1108750 · Cited by 2,485 · see citing works
Self-citationTranscriptional paradigms in mammalian mitochondrial biogenesis and function
Scarpulla, R. C. (2008) · Physiological Reviews · doi:10.1152/physrev.00025.2007 · Cited by 1,666 · see citing works
Mutagenesis and Mapping of a Mouse Gene, <i>Clock</i> , Essential for Circadian Behavior
Vitaterna, M. H., King, D. P., Chang, A.-M., Kornhauser, J. M., Lowrey, P. L., McDonald, J. D., Dove, W. F., Pinto, L. H., Turek, F. W., & Takahashi, J. S. (1994) · Science · doi:10.1126/science.8171325 · Cited by 1,632 · see citing works
Mop3 is an essential component of the master circadian pacemaker in mammals.
Bunger, M. K., Wilsbacher, L. D., Moran, S. M., Clendenin, C., Radcliffe, L. A., Hogenesch, J. B., Simon, M. C., Takahashi, J. S., & Bradfield, C. A. (2000) · Cell · doi:10.1016/s0092-8674(00)00205-1 · Cited by 1,621 · see citing works
Self-citationThe genetics of mammalian circadian order and disorder: implications for physiology and disease
Takahashi, J. S., Hong, H.-K., Ko, C. H., & McDearmon, E. L. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2430 · Cited by 1,611 · see citing works
Self-citationCircadian rhythms from multiple oscillators: lessons from diverse organisms
Bell‐Pedersen, D., Cassone, V. M., Earnest, D. J., Golden, S. S., Hardin, P. E., Thomas, T. L., & Zoran, M. J. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1633 · Cited by 1,481 · see citing works
Nakahata, Y., Kaluzova, M., Grimaldi, B., Sahar, S., Hirayama, J., Chen, D., Guarente, L. P., & Sassone-Corsi, P. (2008) · Cell · doi:10.1016/j.cell.2008.07.002 · Cited by 1,427 · see citing works
SIRT1 regulates circadian clock gene expression through PER2 deacetylation
Asher, G., Gatfield, D., Stratmann, M., Reinke, H., Dibner, C., Kreppel, F., Mostoslavsky, R., Alt, F. W., & Schibler, U. (2008) · Cell · doi:10.1016/j.cell.2008.06.050 · Cited by 1,376 · see citing works
Kondratov, R. V., Kondratova, A. A., Gorbacheva, V. Y., Vykhovanets, O. V., & Antoch, M. P. (2006) · Genes & Development · doi:10.1101/gad.1432206 · Cited by 1,188 · see citing works
Circadian Clock Feedback Cycle Through NAMPT-Mediated NAD <sup>+</sup> Biosynthesis
Ramsey, K. M., Yoshino, J., Brace, C. S., Abrassart, D., Kobayashi, Y., Marcheva, B., Hong, H.-K., Chong, J. L., Buhr, E. D., Lee, C., et al. (2009) · Science · doi:10.1126/science.1171641 · Cited by 1,126 · see citing works
Self-citationRudnicki, M. A., Braun, T. W., Hinuma, S., & Jaenisch, R. (1992) · Cell · doi:10.1016/0092-8674(92)90508-a · Cited by 984 · see citing works
Mammalian circadian biology: elucidating genome-wide levels of temporal organization
Lowrey, P. L., & Takahashi, J. S. (2004) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.5.061903.175925 · Cited by 976 · see citing works
Self-citationGreen, C. B., Takahashi, J. S., & Bass, J. (2008) · Cell · doi:10.1016/j.cell.2008.08.022 · Cited by 902 · cited 1× · see citing works
“The timing of these circadian rhythms is synchronized to the environment by external cues, with light and nutrient availability being two of the most salient entrainment cues (2).”
Self-citationMyoD1: A Nuclear Phosphoprotein Requiring a Myc Homology Region to Convert Fibroblasts to Myoblasts
Tapscott, S. J., Davis, R. L., Thayer, M. J., Cheng, P.-F., Weintraub, H. M., & Lassar, A. B. (1988) · Science · doi:10.1126/science.3175662 · Cited by 845 · see citing works
The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription
Tapscott, S. J. (2005) · Development · doi:10.1242/dev.01874 · Cited by 766 · see citing works
MyoD is required for myogenic stem cell function in adult skeletal muscle
Megeney, L. A., Kablar, B., Garrett, K., Anderson, J. E., & Rudnicki, M. A. (1996) · Genes & Development · doi:10.1101/gad.10.10.1173 · Cited by 724 · see citing works
Transcriptional coactivator PGC-1α integrates the mammalian clock and energy metabolism
Liu, C., Li, S., Liu, T., Borjigin, J., & Lin, J. D. (2007) · Nature · doi:10.1038/nature05767 · Cited by 643 · see citing works
Ripperger, J. A., & Schibler, U. (2006) · Nature Genetics · doi:10.1038/ng1738 · Cited by 593 · see citing works
Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation
Miller, B. H., McDearmon, E. L., Panda, S., Hayes, K. R., Zhang, J., Andrews, J. L., Antoch, M. P., Walker, J. R., Esser, K. A., Hogenesch, J. B., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611724104 · Cited by 509 · see citing works
Self-citationAn initial blueprint for myogenic differentiationPreprint
Blais, A., Tsikitis, M., Acosta‐Alvear, D., Sharan, R., Kluger, Y., & Dynlacht, B. D. (2005) · Genes & Development · doi:10.1101/gad.1281105 · Cited by 464 · see citing works
The Adaptive Value of Circadian Clocks
Woelfle, M. A., Ouyang, Y., Phanvijhitsiri, K., & Johnson, C. H. (2004) · Current Biology · doi:10.1016/j.cub.2004.08.023 · Cited by 375 · see citing works
Singh, I. N., Sullivan, P. G., Deng, Y., Mbye, L. H., & Hall, E. D. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600297 · Cited by 367 · see citing works
Identification of the circadian transcriptome in adult mouse skeletal muscle
McCarthy, J. J., Andrews, J. L., McDearmon, E. L., Campbell, K. S., Barber, B. K., Miller, B. H., Walker, J. R., Hogenesch, J. B., Takahashi, J. S., & Esser, K. A. (2007) · Physiological Genomics · doi:10.1152/physiolgenomics.00066.2007 · Cited by 363 · see citing works
Self-citationCircadian rhythm disorganization produces profound cardiovascular and renal disease in hamsters
Martino, T. A., Oudit, G. Y., Herzenberg, A. M., Tata, N., Koletar, M. M., Kabir, G. M., Belsham, D. D., Backx, P. H., Ralph, M. R., & Sole, M. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00829.2007 · Cited by 317 · see citing works
Force and power output of fast and slow skeletal muscles from mdx mice 6‐28 months old
Lynch, G. S., Hinkle, R. T., Chamberlain, J. S., Brooks, S. V., & Faulkner, J. A. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00591.x · Cited by 305 · see citing works
Properties, Entrainment, and Physiological Functions of Mammalian Peripheral Oscillators
Stratmann, M., & Schibler, U. (2006) · Journal of Biological Rhythms · doi:10.1177/0748730406293889 · Cited by 268 · see citing works
Comparing and Contrasting the Roles of AMPK and SIRT1 in Metabolic Tissues
Fulco, M., & Sartorelli, V. (2008) · Cell Cycle · doi:10.4161/cc.7.23.7164 · Cited by 217 · see citing works
STEREOLOGICAL ANALYSIS OF MAMMALIAN SKELETAL MUSCLE
Eisenberg, B. R., Kuda, A. M., & Peter, J. B. (1974) · The Journal of Cell Biology · doi:10.1083/jcb.60.3.732 · Cited by 216 · see citing works
The reorganization of subcellular structure in muscle undergoing fast-to-slow type transformation
Eisenberg, B. R., & Salmons, S. (1981) · Cell and Tissue Research · doi:10.1007/bf00216750 · Cited by 209 · see citing works
Plant development goes like clockwork
de Montaigu, A., Tóth, R., & Coupland, G. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.04.003 · Cited by 208 · see citing works
Progressive arthropathy in mice with a targeted disruption of theMop3/Bmal-1 locus
Bunger, M. K., Walisser, J. A., Sullivan, R., Manley, P. A., Moran, S. M., Kalscheur, V. L., Colman, R. J., & Bradfield, C. A. (2005) · genesis · doi:10.1002/gene.20102 · Cited by 207 · see citing works
Embryonic activation of the myoD gene is regulated by a highly conserved distal control element
Goldhamer, D. J., Brunk, B. P., Faerman, A., King, A., Shani, M., & Emerson, C. P. (1995) · Development · doi:10.1242/dev.121.3.637 · Cited by 177 · see citing works
Stereological analysis of mammalian skeletal muscle
Eisenberg, B. R., & Kuda, A. M. (1975) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(75)80146-8 · Cited by 150 · see citing works
Myogenic regulatory factors during regeneration of skeletal muscle in young, adult, and old rats
Marsh, D. R., Criswell, D. S., Carson, J. A., & Booth, F. W. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.83.4.1270 · Cited by 144 · see citing works
Photic and circadian expression of luciferase in mPeriod1 - luc transgenic mice in vivo
Wilsbacher, L. D., Yamazaki, S., Herzog, E. D., Song, E.-J., Radcliffe, L. A., Abe, M., Block, G. D., Spitznagel, E. L., Menaker, M., & Takahashi, J. S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012248599 · Cited by 138 · see citing works
Self-citationThe nuclear receptors Rev-erbs and RORs integrate circadian rhythms and metabolism
Duez, H., & Staels, B. (2008) · Diabetes and Vascular Disease Research · doi:10.3132/dvdr.2008.0014 · Cited by 132 · see citing works
González, E., Messi, M. L., & Delbono, O. (2000) · Journal of Membrane Biology · doi:10.1007/s002320010025 · Cited by 115 · see citing works
Asakura, A., Lyons, G. E., & Tapscott, S. J. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1290 · Cited by 113 · see citing works
History-Dependent Mechanical Properties of Permeabilized Rat Soleus Muscle Fibers
Campbell, K. S., & Moss, R. L. (2002) · Biophysical Journal · doi:10.1016/s0006-3495(02)75454-4 · Cited by 95 · see citing works
Self-citationCircadian timing in health and disease
Maywood, E. S., O'Neill, J. S., Wong, G. K. Y., Reddy, A. B., & Hastings, M. H. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)53015-8 · Cited by 89 · see citing works
Emerson, K. J., Bradshaw, W. E., & Holzapfel, C. M. (2008) · Evolution · doi:10.1111/j.1558-5646.2008.00324.x · Cited by 79 · see citing works
MyoD and myogenin protein expression in skeletal muscles of senile rats
Dedkov, E. I., Kostrominova, T. Y., Borisov, A. B., & Carlson, B. M. (2003) · Cell and Tissue Research · doi:10.1007/s00441-002-0686-9 · Cited by 77 · see citing works
Chen, J. C. J., Love, C. M., & Goldhamer, D. J. (2001) · Developmental Dynamics · doi:10.1002/dvdy.1138 · Cited by 70 · see citing works
Chen, J. C. J., Ramachandran, R., & Goldhamer, D. J. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0638 · Cited by 63 · see citing works
Hornberger, T., Mateja, R., Chin, E. R., Andrews, J., & Esser, K. (2005) · Journal of applied physiology · doi:10.1152/japplphysiol.00870.2004 · Cited by 62 · see citing works
Self-citationMutant DMPK 3′-UTR transcripts disrupt C2C12 myogenic differentiation by compromising MyoD
Amack, J. D., Reagan, S. R., & Mahadevan, M. S. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200206020 · Cited by 58 · see citing works
SLControl: PC-based data acquisition and analysis for muscle mechanics
Campbell, K. S., & Moss, R. L. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00295.2003 · Cited by 58 · see citing works
Self-citationChen, J. C. J., & Goldhamer, D. J. (2003) · Developmental Biology · doi:10.1016/j.ydbio.2003.09.018 · Cited by 56 · see citing works
Diaphragm contractile dysfunction in MyoD gene-inactivated mice
Staib, J. L., Swoap, S. J., & Powers, S. K. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00080.2002 · Cited by 33 · see citing works
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Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis
Braun, T., & Gautel, M. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3118 · Cited by 713 · see citing works
Circadian rhythms, sleep, and metabolism
Huang, W., Ramsey, K. M., Marcheva, B., & Bass, J. T. (2011) · Journal of Clinical Investigation · doi:10.1172/jci46043 · Cited by 726 · see citing works
Crosstalk between metabolism and circadian clocks
Reinke, H., & Asher, G. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0096-9 · Cited by 598 · see citing works
Growth and the regulation of myotomal muscle mass in teleost fish
Johnston, I. A., Bower, N. I., & Macqueen, D. J. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.038620 · Cited by 494 · see citing works
Woldt, E., Sebti, Y., Solt, L. A., Duhem, C., Lancel, S., Eeckhoute, J., Hesselink, M. K. C., Paquet, C., Delhaye, S., Shin, Y., et al. (2013) · Nature Medicine · doi:10.1038/nm.3213 · Cited by 454 · see citing works
Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock
Dyar, K. A., Ciciliot, S., Wright, L. E., Biensø, R. S., Tagliazucchi, G. M., Patel, V. R., Forcato, M., Paz, M. I. P., Gudiksen, A., Solagna, F., et al. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2013.10.005 · Cited by 454 · see citing works
“Changes in skeletal muscle structure and function were described in a global Bmal1 knockout model [41]; however it is unclear whether these are direct consequences of muscle Bmal1 deficiency or secondary effects due to the disruption of the circadian pacemaker or other peripheral clocks.”
BackgroundCircaDB: a database of mammalian circadian gene expression profiles
Pizarro, A., Hayer, K. E., Lahens, N. F., & Hogenesch, J. B. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1161 · Cited by 367 · see citing works
Self-citationHealth Consequences of Circadian Disruption in Humans and Animal Models
Evans, J. A., & Davidson, A. J. (2013) · Progress in Molecular Biology and Translational Science · doi:10.1016/b978-0-12-396971-2.00010-5 · Cited by 291 · see citing works
Endocrine Crosstalk Between Skeletal Muscle and the Brain
Delezie, J., & Handschin, C. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00698 · Cited by 270 · see citing works
The nuclear receptor REV-ERBα is required for the daily balance of carbohydrate and lipid metabolism
Delezie, J., Dumont, S., Dardente, H., Oudart, H., Gréchez‐Cassiau, A., Klosen, P., Teboul, M., Delaunay, F., Pévet, P., & Challet, E. (2012) · The FASEB Journal · doi:10.1096/fj.12-208751 · Cited by 252 · see citing works
“Alternatively, altered clock functioning in the absence of REV-ERB could account for impaired temporal coordination of developmental processes related to muscle and adipose physiology (58, 61).”
BackgroundDell'Orso, S., Juan, A. H., Ko, K.-D., Naz, F., Perovanovic, J., Gutierrez-Cruz, G., Feng, X., & Sartorelli, V. (2019) · Development · doi:10.1242/dev.174177 · Cited by 243 · see citing works
“For instance, the oscillation of intermediary metabolites of the NAD biosynthetic pathways may be relevant for circadian gene expression in MuSCs and skeletal muscle (Nakahata et al., 2009; Ryall et al., 2015b; Solanas et al., 2017; Andrews et al., 2010; Lowe et al., 2018).”
BackgroundCircadian timing of metabolism in animal models and humans
Dibner, C., & Schibler, U. (2015) · Journal of Internal Medicine · doi:10.1111/joim.12347 · Cited by 237 · see citing works
Roberts, M. D., McCarthy, J. J., Hornberger, T. A., Phillips, S. M., Mackey, A. L., Nader, G. A., Boppart, M. D., Kavazis, A. N., Reidy, P. T., Ogasawara, R., et al. (2023) · Physiological Reviews · doi:10.1152/physrev.00039.2022 · Cited by 214 · see citing works
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 · see citing works
Picard, M., Hepple, R. T., & Burelle, Y. (2012) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00368.2011 · Cited by 214 · see citing works
“, 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.”
BackgroundThe impact of sleep on age-related sarcopenia: Possible connections and clinical implications
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 215 · see citing works
“Indeed, core clock gene disruption in animal models leads to muscle weakness (Andrews et al., 2010).”
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 · see citing works
“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 · see citing works
“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 211 · see citing works
“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 205 · see citing works
“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).”
BackgroundWefers, J., van Moorsel, D., Hansen, J., Connell, N. J., Havekes, B., Hoeks, J., Lichtenbelt, W. D. V. M., Duez, H., Phielix, E., Kalsbeek, A., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1722295115 · Cited by 202 · see citing works
“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 190 · see citing works
Self-citationIzumo, M., Pejchal, M., Schook, A. C., Lange, R. P., Walisser, J. A., Sato, T., Wang, X., Bradfield, C. A., & Takahashi, J. S. (2014) · eLife · doi:10.7554/elife.04617 · Cited by 180 · see citing works
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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 · see citing works
Hodge, B. A., Wen, Y., Riley, L. A., Zhang, X., England, J. H., Harfmann, B. D., Schroder, E. A., & Esser, K. A. (2015) · Skeletal Muscle · doi:10.1186/s13395-015-0039-5 · Cited by 175 · see citing works
“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 173 · see citing works
“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<i>Bmal1</i>-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 · see citing works
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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 · see citing works
Intrinsic muscle clock is necessary for musculoskeletal health
Schroder, E. A., Harfmann, B. D., Zhang, X., Srikuea, R., England, J. H., Hodge, B. A., Wen, Y., Riley, L. A., Yu, Q., Christie, A., et al. (2015) · The Journal of Physiology · doi:10.1113/jp271436 · Cited by 145 · see citing works
“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 · see citing works
“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 136 · see citing works
Circadian disruption in the pathogenesis of metabolic syndrome
Maury, E., Hong, H. K., & Bass, J. (2014) · Diabetes & Metabolism · doi:10.1016/j.diabet.2013.12.005 · Cited by 132 · see citing works
“Indeed, Bmal1−/− ice develop arthropathy and myopathy [46,72], while muscle escue restored normal activity and body weight in these mice 71].”
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 129 · see citing works
“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 · see citing works
“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
Leliavski, A., Shostak, A., Husse, J., & Oster, H. (2013) · Endocrinology · doi:10.1210/en.2013-1531 · Cited by 120 · see citing works
Sleep, circadian biology and skeletal muscle interactions: Implications for metabolic health
Morrison, M., Halson, S. L., Weakley, J., & Hawley, J. A. (2022) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2022.101700 · Cited by 118 · see citing works
“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 117 · see citing works
“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., D, D. C. G., Barish, G. D., & Bass, J. T. (2018) · Genes & Development · doi:10.1101/gad.319228.118 · Cited by 114 · see citing works
“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
Jordan, S. D., Kriebs, A., Vaughan, M. E., Duglan, D., Fan, W., Henriksson, E., Huber, A., Papp, S. J., Nguyen, M., Afetian, M. E., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.06.002 · Cited by 112 · see citing works
Running on time: the role of circadian clocks in the musculoskeletal system
Dudek, M., & Meng, Q. (2014) · Biochemical Journal · doi:10.1042/bj20140700 · Cited by 110 · see citing works
Circadian Regulation of Hippocampal-Dependent Memory: Circuits, Synapses, and Molecular Mechanisms
Snider, K. H., Sullivan, K. A., & Obrietan, K. H. (2018) · Neural Plasticity · doi:10.1155/2018/7292540 · Cited by 104 · see citing works
What time is it? Deep learning approaches for circadian rhythms
Agostinelli, F., Ceglia, N., Shahbaba, B., Sassone‐Corsi, P., & Baldi, P. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw243 · Cited by 107 · see citing works
“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”
MethodPerrin, L., Loizides‐Mangold, U., Skarupelova, S., Pulimeno, P., Chanon, S., Robert, M., Bouzakri, K., Modoux, C., Roux‐Lombard, P., Vidal, H., et al. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.07.009 · Cited by 105 · see citing works
“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 106 · see citing works
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 104 · see citing works
“, 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 106 · see citing works
“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 103 · see citing works
Coupled network of the circadian clocks: a driving force of rhythmic physiology
Finger, A., Dibner, C., & Kramer, A. (2020) · FEBS Letters · doi:10.1002/1873-3468.13898 · Cited by 99 · see citing works
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 101 · see citing works
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 97 · see citing works
“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 · see citing works
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 103 · see citing works
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 · see citing works
“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 89 · see citing works
“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 86 · see citing works
“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 87 · see citing works
“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 · see citing works
Circadian Regulation of Adult Stem Cell Homeostasis and Aging.
Benitah, S., & Welz, P. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.05.002 · Cited by 80 · see citing works
“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 · see citing works
“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 82 · see citing works
“[43].”
The Circadian Nature of Mitochondrial Biology
Manella, G., & Asher, G. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00162 · Cited by 81 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
“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 80 · see citing works
Circadian clock and the onset of cardiovascular events
Takeda, N., & Maemura, K. (2016) · Hypertension Research · doi:10.1038/hr.2016.9 · Cited by 80 · see citing works
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 · see citing works
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 75 · see citing works
“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 73 · see citing works
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 · see citing works
“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 74 · see citing works
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 70 · see citing works
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 · see citing works
“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 · see citing works
“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 69 · see citing works
Pastore, S., & Hood, D. A. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01505.2012 · Cited by 66 · see citing works
Bone-Muscle Mutual Interactions
Lara-Castillo, N., & Johnson, M. L. (2020) · Current Osteoporosis Reports · doi:10.1007/s11914-020-00602-6 · Cited by 68 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 66 · see citing works
“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 66 · see citing works
Ageing and osteoarthritis: a circadian rhythm connection
Gossan, N. C., Boot-Handford, R., & Meng, Q. (2014) · Biogerontology · doi:10.1007/s10522-014-9522-3 · Cited by 65 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
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 63 · see citing works
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 62 · see citing works
“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 · see citing works
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 60 · see citing works
“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 · see citing works
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 · see citing works
“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 59 · see citing works
“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 · see citing works
“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 56 · see citing works
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 62 · see citing works
“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 57 · see citing works
“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 · see citing works
“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 · see citing works
- 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 › 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
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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