Endurance training ameliorates the metabolic and performance characteristics of circadian Clock mutant mice
Abstract
Circadian locomotor output cycles kaput (CLOCK) is a nuclear transcription factor that is a component of the central autoregulatory feedback loop that governs the generation of biological rhythms. Homozygous Clock mutant mice contain a truncated CLOCK Δ19 protein within somatic cells, subsequently causing an impaired ability to rhythmically transactivate circadian genes. The present study sought to investigate whether the Clock mutation affects mitochondrial physiology within skeletal muscle, as well as the responsiveness of these mutant animals to adapt to a chronic voluntary endurance training protocol. Within muscle, Clock mutant mice displayed 44% and 45% reductions in peroxisome proliferator-activated receptor-γ coactivator 1-α (PGC-1α) and mitochondrial transcription factor-A protein content, respectively, and an accompanying 16% decrease in mitochondrial content, as determined by cytochrome c oxidase enzyme activity. These decrements contributed to a 50% decrease in exercise tolerance in Clock mutant mice. Interestingly, the Clock mutation did not appear to alter subsarcolemmal or intermyofibrillar mitochondrial respiration within muscle or systemic glucose tolerance. Daily locomotor activity levels were similar between wild-type and Clock mutant mice throughout the training protocol. Endurance training ameliorated the decrease in PGC-1α protein expression and mitochondrial content in the Clock mutant mice, eliciting a 2.9-fold improvement in exercise tolerance. Thus our data suggest that a functional CLOCK protein is essential to ensure the maintenance of mitochondrial content within muscle although the absence of a functional CLOCK protein does not impair the ability of animals to adapt to chronic exercise.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 [20]
The same detrimental metabolic changes that occur in response to circadian misalignment and altered expression of clock genes may also be ameliorated by performing exercise.
“Furthermore, the same detrimental metabolic changes that occur in response to circadian misalignment and altered expression of clock genes may also be ameliorated by performing exercise [20,31,32].”
From Exercise mitigates sleep-loss-induced changes in glucose tolerance, mitochondrial function, sarcoplasmic protein synthesis, and diurnal rhythms (2021) · cites this paper as [20]
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
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
Damiola, F., Le Minh, N., Preitner, N., Kornmann, B., Fleury-Olela, F., & Schibler, U. (2000) · Genes & Development · doi:10.1101/gad.183500 · Cited by 2,394 · see citing works
Role of the CLOCK Protein in the Mammalian Circadian Mechanism
Gekakis, N., Staknis, D., Nguyen, H. B., Davis, F. C., Wilsbacher, L. D., King, D. P., Takahashi, J. S., & Weitz, C. J. (1998) · Science · doi:10.1126/science.280.5369.1564 · Cited by 1,997 · see citing works
Entrainment of the circadian clock in the liver by feeding
Stokkan, K.-A., Yamazaki, S., Tei, H., Sakaki, Y., & Menaker, M. (2001) · Science · doi:10.1126/science.291.5503.490 · Cited by 1,800 · 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
Biochemical Adaptations in Muscle
Holloszy, J. O. (1967) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)96046-1 · Cited by 1,517 · 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
Positional Cloning of the Mouse Circadian Gene
King, D. P., Zhao, Y., Sangoram, A. M., Wilsbacher, L. D., Tanaka, M., Antoch, M. P., Steeves, T. D. L., Vitaterna, M. H., Kornhauser, J. M., Lowrey, P. L., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)80245-7 · Cited by 1,382 · 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
Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1
Baar, K., Wende, A. R., Jones, T. E., Marison, M., Nolte, L. A., Chen, M., Kelly, D. P., & Holloszy, J. O. (2002) · The FASEB Journal · doi:10.1096/fj.02-0367com · Cited by 1,020 · see citing works
Exercise induces transient transcriptional activation of the PGC‐1α gene in human skeletal muscle
Pilegaard, H., Saltin, B., & Neufer, P. D. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.034850 · Cited by 885 · see citing works
Evaluating the glucose tolerance test in mice
Andrikopoulos, S., Blair, A. R., DeLuca, N., Fam, B. C., & Proietto, J. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90617.2008 · Cited by 824 · see citing works
Circadian oscillation of a mammalian homologue of the Drosophila period gene
Tei, H., Okamura, H., Shigeyoshi, Y., Fukuhara, C., Ozawa, R., Hirose, M., & Sakaki, Y. (1997) · Nature · doi:10.1038/39086 · Cited by 792 · see citing works
Akimoto, T., Pohnert, S. C., Li, P., Zhang, M., Gumbs, C., Rosenberg, P. B., Williams, R. S., & Yan, Z. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m408862200 · Cited by 714 · see citing works
Moore, R. Y., & Klein, D. C. (1974) · Brain Research · doi:10.1016/0006-8993(74)90188-7 · Cited by 678 · 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
Mammalian mitochondrial β -oxidation
Eaton, S. D., Bartlett, K., & Pourfarzam, M. (1996) · Biochemical Journal · doi:10.1042/bj3200345 · Cited by 425 · see citing works
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., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014523107 · Cited by 389 · see citing works
Clock controls circadian period in isolated suprachiasmatic nucleus neurons
Herzog, E. D., Takahashi, J. S., & Block, G. D. (1998) · Nature Neuroscience · doi:10.1038/3708 · Cited by 387 · see citing works
Calvo, J. A., Daniels, T. G., Wang, X., Paul, A., Lin, J., Spiegelman, B. M., Stevenson, S. C., & Rangwala, S. M. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01231.2007 · Cited by 377 · 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
Genome-Wide Expression Analysis inDrosophilaReveals Genes Controlling Circadian Behavior
Ceriani, M. F., Hogenesch, J. B., Yanovsky, M. J., Panda, S., Straume, M., & Kay, S. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-21-09305.2002 · Cited by 358 · see citing works
Comparisons of the Variability of Three Markers of the Human Circadian Pacemaker
Klerman, E. B., Gershengorn, H. B., Duffy, J. F., & Kronauer, R. E. (2002) · Journal of Biological Rhythms · doi:10.1177/074873002129002474 · Cited by 350 · see citing works
Intensity-controlled treadmill running in mice: cardiac and skeletal muscle hypertrophy
Kemi, O. J., Loennechen, J. P., Wisløff, U., & Ellingsen, Ø. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00231.2002 · Cited by 299 · see citing works
Scheduled exercise phase shifts the circadian clock in skeletal muscle
WOLFF, G., & ESSER, K. A. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318255cf4c · Cited by 291 · see citing works
Cogswell, A. M., Stevens, R. J., & Hood, D. A. (1993) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1993.264.2.c383 · Cited by 286 · see citing works
Self-citationCircadian rhythms and athletic performance
Winget, C. M., DEROSHIA, C. W., & Holley, D. C. (1985) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198510000-00002 · Cited by 257 · see citing works
Saini, C., Morf, J., Stratmann, M., Gos, P., & Schibler, U. (2012) · Genes & Development · doi:10.1101/gad.183251.111 · Cited by 248 · see citing works
Hood, D. A. (2009) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h09-045 · Cited by 242 · see citing works
Self-citationBenloucif, S., Guico, M. J., Reid, K. J., Wolfe, L. F., L’Hermite‐Balériaux, M., & Zee, P. C. (2005) · Journal of Biological Rhythms · doi:10.1177/0748730404273983 · Cited by 240 · see citing works
The ROR nuclear orphan receptor subfamily: Critical regulators of multiple biological processes
Jetten, A. M., Kurebayashi, S., & Ueda, E. (2001) · Progress in Nucleic Acid Research and Molecular Biology · doi:10.1016/s0079-6603(01)69048-2 · Cited by 232 · see citing works
Regulation of Mitochondrial Biogenesis in Muscle by Endurance Exercise
Irrcher, I., Adhihetty, P. J., Joseph, A.-M., Ljubicic, V., & Hood, D. A. (2003) · Sports Medicine · doi:10.2165/00007256-200333110-00001 · Cited by 210 · see citing works
Self-citationWibom, R., Hultman, E., Johansson, M., Matherei, K., Constantin-Teodosiu, D., & Schantz, P. G. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.73.5.2004 · Cited by 208 · see citing works
Song, X., Fiedler, M., Galuska, D., Ryder, J. W., Fernström, M., Chibalin, A., Wallberg‐Henriksson, H., & Zierath, J. R. (2002) · Diabetologia · doi:10.1007/s125-002-8245-8 · Cited by 184 · see citing works
Role of p53 in mitochondrial biogenesis and apoptosis in skeletal muscle
Saleem, A., Adhihetty, P. J., & Hood, D. A. (2008) · Physiological Genomics · doi:10.1152/physiolgenomics.90346.2008 · Cited by 182 · see citing works
Self-citationGuette, M., Gondin, J., & Martin, A. (2005) · Chronobiology International · doi:10.1081/cbi-200062407 · Cited by 171 · see citing works
The role of PGC-1α on mitochondrial function and apoptotic susceptibility in muscle
Adhihetty, P. J., Uguccioni, G., Leick, L., Hidalgo, J., Pilegaard, H., & Hood, D. A. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00070.2009 · Cited by 168 · see citing works
Self-citationGordon, J. W., Rungi, A. A., Inagaki, H., & Hood, D. A. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.1.389 · Cited by 160 · see citing works
Self-citationPGC-1β-Regulated mitochondrial biogenesis and function in myotubes is mediated by NRF-1 and ERRα
Shao, D., Liu, Y., Liu, X., Zhu, L., Cui, Y., Cui, A., Qiao, A., Kong, X., Liu, Y. U., Chen, Q., et al. (2010) · Mitochondrion · doi:10.1016/j.mito.2010.05.012 · Cited by 155 · see citing works
Oishi, K., Fukui, H., & Ishida, N. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.2054 · Cited by 140 · see citing works
Schroeder, A., Truong, D. A., Loh, D. H., Jordan, M. C., Roos, K. P., & Colwell, C. S. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.233676 · Cited by 135 · see citing works
Martino, T. A., Tata, N., Simpson, J. A., Vanderlaan, R., Dawood, F., Kabir, M. G., Khaper, N., Cifelli, C., Podobed, P., Liu, P. P., et al. (2011) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2010.11.022 · Cited by 94 · see citing works
Yamanaka, Y., Honma, S., & Honma, K.-I. (2008) · Genes to Cells · doi:10.1111/j.1365-2443.2008.01183.x · Cited by 82 · see citing works
The importance of PGC-1α in contractile activity-induced mitochondrial adaptations
Uguccioni, G., & Hood, D. A. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00292.2010 · Cited by 80 · see citing works
Self-citationConcentration dependence of the dielectric constant in mixed oxides MxOyMp′Oq
Devine, R. A. B., & Revesz, A. G. (2001) · Journal of Applied Physics · doi:10.1063/1.1375806 · Cited by 76 · 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
Time-of-day dependence of isokinetic leg strength and associated interday variability.
Wyse, J., Mercer, T. H., & Gleeson, N. (1994) · British Journal of Sports Medicine · doi:10.1136/bjsm.28.3.167 · Cited by 74 · see citing works
Working around the clock: circadian rhythms and skeletal muscle
Zhang, X., Dube, T. J., & Esser, K. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00725.2009 · Cited by 64 · see citing works
Miyazaki, 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
Hannibal, J., Hsiung, H. M., & Fahrenkrug, J. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00599.2010 · Cited by 49 · see citing works
Repeated Sprints Alter Signaling Related to Mitochondrial Biogenesis in Humans
Serpiello, F. R., McKenna, M. J., Bishop, D. J., Aughey, R. J., Caldow, M. K., Cameron‐Smith, D., & Stepto, N. K. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318240067e · Cited by 48 · see citing works
Kennaway, D. J., Owens, J. A., Voultsios, A., & Varcoe, T. J. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00223.2006 · Cited by 46 · see citing works
Role of UCP3 in state 4 respiration during contractile activity-induced mitochondrial biogenesis
Ljubicic, V., Adhihetty, P. J., & Hood, D. A. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00336.2004 · Cited by 45 · see citing works
Self-citationEffects of endurance training on apoptotic susceptibility in striated muscle
Vainshtein, A., Kazak, L., & Hood, D. A. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00020.2011 · Cited by 37 · see citing works
Self-citationAdipokines and Adipocyte Function in Clock Mutant Mice That Retain Melatonin Rhythmicity
Kennaway, D. J., Owens, J. A., Voultsios, A., & Wight, N. (2011) · Obesity · doi:10.1038/oby.2011.276 · Cited by 21 · see citing works
Feldstein, C. A., Akopian, M., Olivieri, A. O., & Garrido, D. (2012) · Clinical and Experimental Hypertension · doi:10.3109/10641963.2012.665541 · Cited by 11 · see citing works
High-intensity exercise training in mice with cardiomyocyte-specific disruption of Serca2
Ericsson, M., Andersson, K. B., Amundsen, B. H., TORP, S. H., Sjaastad, I., Christensen, G., Sejersted, O. M., & Ellingsen, Ø. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01133.2009 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Circadian control of glucose metabolism
Kalsbeek, A., la Fleur, S., & Fliers, E. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2014.03.002 · Cited by 338 · see citing works
Protein acetylation in metabolism – metabolites and cofactors
Menzies, K. J., Zhang, H., Katsyuba, E., & Auwerx, J. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.181 · Cited by 331 · see citing works
The 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
Circadian 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
The mammalian circadian clock and its entrainment by stress and exercise
Tahara, Y., Aoyama, S., & Shibata, S. (2017) · The Journal of Physiological Sciences · doi:10.1007/s12576-016-0450-7 · Cited by 198 · see citing works
Unravelling the mechanisms regulating muscle mitochondrial biogenesis
Hood, D. A., Tryon, L. D., Carter, H. N., Kim, Y., & Chen, C. C. W. (2016) · Biochemical Journal · doi:10.1042/bcj20160009 · Cited by 159 · see citing works
Self-citationDyar, K. A., Hubert, M. J., Mir, A. A., Ciciliot, S., Lutter, D., Greulich, F., Quagliarini, F., Kleinert, M., Fischer, K., Eichmann, T. O., et al. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2005886 · Cited by 154 · see citing works
Environmental 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
Gabriel, B. M., Altıntaş, A., Smith, J. A. B., Puig, L. S., Zhang, X., Basse, A. L., Laker, R. C., Gao, H., Liu, Z., Dollet, L., et al. (2021) · Science Advances · doi:10.1126/sciadv.abi9654 · Cited by 118 · see citing works
Aoyama, S., & Shibata, S. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00063 · Cited by 106 · 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
Circadian 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
Circadian 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
Fujimaki, S., & Kuwabara, T. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18102147 · Cited by 75 · see citing works
Exercise 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
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
Skeletal 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
Erlich, A. T., Tryon, L. D., Crilly, M. J., Memme, J. M., Moosavi, Z. S. M., Oliveira, A. N., Beyfuss, K. A., & Hood, D. A. (2016) · Integrative Medicine Research · doi:10.1016/j.imr.2016.05.003 · Cited by 57 · see citing works
Self-citationMitochondrial dysfunction in metabolism and ageing: shared mechanisms and outcomes?
López‐Lluch, G., Hernández‐Camacho, J. D., Fernández‐Ayala, D. J. M., & Navas, P. (2018) · Biogerontology · doi:10.1007/s10522-018-9768-2 · Cited by 57 · see citing works
Re-Setting the Circadian Clock Using Exercise against Sarcopenia
Choi, Y., Cho, J., No, M., Heo, J., Cho, E., Chang, E., Park, D., Kang, J., & Kwak, H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093106 · Cited by 52 · see citing works
Lønbro, S., Wiggins, J. M., Wittenborn, T. R., Elming, P. B., Rice, L. P., Pampo, C., Lee, J. A., Siemann, D. W., & Horsman, M. R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0215584 · Cited by 47 · see citing works
Do not neglect the role of circadian rhythm in muscle atrophy
Zhang, H., Liang, J., & Chen, N. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101155 · Cited by 46 · see citing works
Saner, N. J., Bishop, D. J., & Bartlett, J. D. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.01.001 · Cited by 41 · see citing works
Saracino, P. G., Rossetti, M. L., Steiner, J. L., & Gordon, B. S. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.12.034 · Cited by 38 · see citing works
Dalbram, E., Basse, A. L., Zierath, J. R., & Treebak, J. T. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00737.2018 · Cited by 37 · see citing works
Exercise as a Peripheral Circadian Clock Resynchronizer in Vascular and Skeletal Muscle Aging
Silva, B. S. D. A., Uzeloto, J. S., Lira, F. S., Pereira, T. S., Coelho-e-Silva, M. J., & Caseiro, A. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph182412949 · Cited by 35 · see citing works
Goljanek‐Whysall, K., Iwanejko, L., Vasilaki, A., Pekovic‐Vaughan, V., & McDonagh, B. (2016) · Mammalian Genome · doi:10.1007/s00335-016-9643-x · Cited by 31 · see citing works
Tryon, L. D., Crilly, M. J., & Hood, D. A. (2015) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00266.2014 · Cited by 32 · see citing works
Self-citationDiurnal Regulation of Peripheral Glucose Metabolism: Potential Effects of Exercise Timing
Mancilla, R., Krook, A., Schrauwen, P., & Hesselink, M. K. C. (2020) · Obesity · doi:10.1002/oby.22811 · Cited by 29 · see citing works
Time to Train: The Involvement of the Molecular Clock in Exercise Adaptation of Skeletal Muscle
Mansingh, S., & Handschin, C. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.902031 · Cited by 28 · see citing works
Chalimoniuk, M., Chrapusta, S. J., Lukáčová, N., & Langfort, J. (2015) · Brain Research · doi:10.1016/j.brainres.2015.05.020 · Cited by 25 · see citing works
Satellite cell-specific deletion of Cipc alleviates myopathy in mdx mice
Zheng, J., Lou, J., Li, Y., Qian, P., He, W., Hao, Y., Xue, T., Li, Y., & Song, Y. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110939 · Cited by 24 · see citing works
Liu, H., Liu, S., Wang, K., Zhang, T., Yin, L., Liang, J., Yang, Y., & Luo, J. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph192114194 · Cited by 24 · see citing works
From Chronodisruption to Sarcopenia: The Therapeutic Potential of Melatonin
Fernández‐Martínez, J., Ramírez‐Casas, Y., Yang, Y., Aranda‐Martínez, P., Martínez-Ruiz, L., Escames, G., & Acuña-Castroviejo, D. (2023) · Biomolecules · doi:10.3390/biom13121779 · Cited by 21 · see citing works
Coulson, S. Z., Guglielmo, C. G., & Staples, J. F. (2024) · Journal of Experimental Biology · doi:10.1242/jeb.246849 · Cited by 21 · see citing works
Yang, L., Lang, H., Zhou, M., Huang, L., Hui, S., Wang, X., Chen, K., & Mi, M. (2020) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201900991 · Cited by 20 · see citing works
Hao, Y., Xue, T., Liu, S., Geng, S., Shi, X., Qian, P., He, W., Zheng, J., Li, Y., Lou, J., et al. (2023) · MedComm · doi:10.1002/mco2.202 · Cited by 15 · see citing works
Zsuga, J., Móré, C. E., Erdei, T., Papp, C., Harsányi, S., & Gesztelyi, R. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00818 · Cited by 15 · see citing works
Chrono-Aerobic Exercise Optimizes Metabolic State in DB/DB Mice through CLOCK–Mitophagy–Apoptosis
Zhang, Z., Li, X., Zhang, J., Du, J., Zhang, Q., Ge, Z., & Ding, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169308 · Cited by 14 · see citing works
Kim, S., Ko, I., Ji, E., Jin, J., Hwang, L., Kim, S., Cho, S., Kim, C., Kim, K., & Kim, K. H. (2019) · International Neurourology Journal · doi:10.5213/inj.1938048.024 · Cited by 13 · see citing works
A Role for Exercise to Counter Skeletal Muscle Clock Disruption
Erickson, M. L., Esser, K. A., Kraus, W. E., Buford, T. W., & Redman, L. M. (2020) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000235 · Cited by 12 · see citing works
Negri, M., Pivonello, C., Amatrudo, F., Cimmino, F., Trinchese, G., Vetrani, C., Iaccarino, G., Pivonello, R., Mollica, M. P., & Colao, A. (2025) · Nutrition Reviews · doi:10.1093/nutrit/nuaf007 · Cited by 12 · see citing works
The circadian clock regulates metabolic responses to physical exercise
Cheng, Q., Lü, C., & Qian, R. (2022) · Chronobiology International · doi:10.1080/07420528.2022.2050384 · Cited by 10 · see citing works
Dial, M. B., Malek, E. M., Cooper, A. R., Neblina, G. A., Vasileva, N. I., Hines, D. J., & McGinnis, G. R. (2024) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00632.2023 · Cited by 10 · see citing works
Circadian Clock in Muscle Disease Etiology and Therapeutic Potential for Duchenne Muscular Dystrophy
Kiperman, T., & Ma, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25094767 · Cited by 9 · see citing works
Circadian Rhythm, Exercise, and Heart.
Wang, C.-Y. (2017) · Acta Cardiologica Sinica · doi:10.6515/acs20170604a · Cited by 12 · see citing works
Zhang, Z., Liu, B., & Ding, S. (2025) · The FASEB Journal · doi:10.1096/fj.202501289r · Cited by 7 · see citing works
The skeletal muscle circadian clock: current insights
Nakao, R., Nikawa, T., & Oishi, K. (2017) · ChronoPhysiology and Therapy · doi:10.2147/cpt.s116569 · Cited by 7 · see citing works
JumpDetector: An automated monitoring equipment for the locomotion of jumping insects
Zhou, F., Kang, L., & Wang, X. (2019) · Insect Science · doi:10.1111/1744-7917.12668 · Cited by 7 · see citing works
Action-Dependent Photobiomodulation on Health, Suboptimal Health, and Disease
Liu, T. C., Liu, L., Chen, J.-G., Zeng, P., & Yang, X. (2014) · International Journal of Photoenergy · doi:10.1155/2014/832706 · Cited by 5 · see citing works
Global research trends on exercise and circadian rhythm: A bibliometric analysis
Gu, Y., Xie, Y., Liu, W., Wang, Z., Seong, D.-H., & Kim, S. H. (2025) · Chronobiology International · doi:10.1080/07420528.2025.2501339 · Cited by 3 · see citing works
Clock Gene Expression Modulation by Low- and High-Intensity Exercise Regimens in Aging Mice
Vitorino, M. C. T., Corrêa, H. D. L., Cunha, V. N. D. C., de Souza, M. S., Simões, H. G., Rosa, T. D. S., Vieira, E. C., & de Andrade, R. V. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26178739 · Cited by 3 · see citing works
The 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 · see citing works
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 3 · see citing works
Reconsidering the scientific scope of global research trends on exercise and circadian rhythm
Kentiba, E., & Drazdova, V. (2025) · Chronobiology International · doi:10.1080/07420528.2025.2576489 · Cited by 1 · see citing works
Machado, F. S. M., Horta, N. A. C., Rodrigues, Q. T., Cardoso, T. S. R., Aquino, N. S. S., Szawka, R. E., Poletini, M. O., & Coimbra, C. C. (2025) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-025-03128-x · Cited by 1 · see citing works
Liu, C., Tong, Y., Pan, M., Li, Y., Yang, X., Wang, Y., & Xing, L. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1660080 · Cited by 1 · see citing works
Huang, Y., Tang, L., Li, D., Chen, L., Wu, W., Zeng, D., Zhong, Y., & Wang, M. (2026) · Mammalian Genome · doi:10.1007/s00335-026-10231-6 · Cited by 1 · see citing works
Circadian rhythm: The hidden “puppet master” behind musculoskeletal disorders
Zhong, S., Yuan, C., Li, F., Li, D., Chang, X., Zhang, B., Qi, P., Li, N., & Xie, X. (2026) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2026.101142 · Cited by 1 · see citing works
Sawai, A., & Shida, T. (2025) · Women · doi:10.3390/women5020015 · Cited by 1 · see citing works
Harfmann, B. D. (2015) · UKnowledge (University of Kentucky)
The Role of Two Homologous E3 Ligases in Muscle Physiology
Gloston, G. F. (2016) · Digital Commons-TMC (Texas Medical Center)
Circadian Rhythm and Health : Influence of Food Intake Timing and Regular Exercise
Lee, K., & Kim, S. K. (2023) · Korean Journal of Sport Science · doi:10.24985/kjss.2023.34.2.187
Restoration of circadian rhythm as novel targets against sarcopenia
Wang, T., & Hong, Z. (2026) · Chinese Medical Journal · doi:10.1097/cm9.0000000000004087
Xue, T., Zhao, Y., Wang, J., Xu, Y., Gu, Z., & Zheng, J. (2026) · Histochemistry and Cell Biology · doi:10.1007/s00418-026-02543-0
Emerging evidence suggests that circadian disruption and muscle wasting form a self-reinforcing loop
Li, F., & Liu, C. (2026) · Chronobiology International · doi:10.1080/07420528.2026.2743668
- Authors
- Pastore, S., & Hood, D. A.
- Affiliations
- York University (CA)
- Corresponding author
- Hood, David A.
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 2013-04-15
- Volume
- 114
- Issue
- 8
- Pages
- 1076-1084
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W1968877294
- Cited by
- 66
- References
- 58
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 3 · 2023: 6 · 2022: 5 · 2021: 2 · 2020: 6 · 2019: 5 · 2018: 4 · 2017: 5 · 2016: 7 · 2015: 6 · 2014: 3 · 2013: 1
- FWCI
- 3.05
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- York University
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- circadian clock, Clock mutant mice, endurance training, skeletal muscle mitochondria, PGC-1α, TFAM, exercise tolerance, glucose tolerance, mitochondrial respiration, circadian rhythm, exercise adaptation
- MeSH terms
- Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Adaptation, Physiological, Animals, Blood Glucose, Circadian Rhythm, Electron Transport Complex IV, DNA-Binding Proteins, Exercise Test, High Mobility Group Proteins, Male, Mice, Inbred C57BL, Mice, Mutant Strains, Mitochondria, Muscle, Motor Activity, Muscle Contraction, Mutation, Physical Endurance, Sarcolemma, Time Factors, Transcription Factors, Trans-Activators, Exercise Tolerance, Muscle, Skeletal, Mice, CLOCK Proteins
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 ›
Are you an author, or do you see a problem with this page? Request a review
