Circadian rhythms and exercise — re-setting the clock in metabolic disease
Abstract
Perturbed diurnal rhythms are becoming increasingly evident as deleterious events in the pathology of metabolic diseases. Exercise is well characterized as a crucial intervention in the prevention and treatment of individuals with metabolic diseases. Little is known, however, regarding optimizing the timing of exercise bouts in order to maximize their health benefits. Furthermore, exercise is a potent modulator of skeletal muscle metabolism, and it is clear that skeletal muscle has a strong circadian profile. In humans, mitochondrial function peaks in the late afternoon, and the circadian clock might be inherently impaired in myotubes from patients with metabolic disease. Timing exercise bouts to coordinate with an individual's circadian rhythms might be an efficacious strategy to optimize the health benefits of exercise. The role of exercise as a Zeitgeber can also be used as a tool in combating metabolic disease. Shift work is known to induce acute insulin resistance, and appropriately timed exercise might improve health markers in shift workers who are at risk of metabolic disease. In this Review, we discuss the literature regarding diurnal skeletal muscle metabolism and the interaction with exercise bouts at different times of the day to combat metabolic disease.
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?
Modern lifestyle circadian disruptions include poor-quality diet, improper meal timing and altered feeding-fasting behavior, sub-optimal exercise timing, disrupted sleep-wake cycles, shift work, EDC, and stress.
“These include poor-quality diet [232], improper meal timing and altered feeding-fasting behavior [233,234], sub-optimal exercise timing [235], disrupted sleep-wake cycles [236], shift work [237], EDC [238], and stress [239,240].”
From Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment (2022) · cites this paper as [235]
Exercise timing relative to circadian rhythms, fed-fasting status and post-exercise dietary composition may influence metabolic outcomes.
“exercise timing relative to circadian rhythms21, fed-fasting status22 or post-exercise dietary composition23 might influence metabolic outcomes.”
From Exerkines in health, resilience and disease (2022) · cites this paper as [21]
Cites
Annotation of functional variation in personal genomes using RegulomeDB
Boyle, A. P., Hong, E. L., Hariharan, M., Cheng, Y., Schaub, M. A., Kasowski, M., Karczewski, K. J., Park, J., Hitz, B. C., Weng, S., et al. (2012) · Genome Research · doi:10.1101/gr.137323.112 · Cited by 2,722 · see citing works
Dibner, C., Schibler, U., & Albrecht, U. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135821 · Cited by 2,421 · see citing works
Exercise Metabolism and the Molecular Regulation of Skeletal Muscle Adaptation
Egan, B., & Zierath, J. R. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2012.12.012 · Cited by 2,084 · see citing works
Self-citationCircadian physiology of metabolism
Panda, S. (2016) · Science · doi:10.1126/science.aah4967 · Cited by 1,092 · see citing works
Physiological significance of a peripheral tissue circadian clock
Lamia, K. A., Storch, K.-F., & Weitz, C. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806717105 · Cited by 1,048 · see citing works
AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation
Lamia, K. A., Sachdeva, U. M., DiTacchio, L., Williams, E. C., Alvarez, J. G., Egan, D. F., Vasquez, D. S., Juguilon, H., Panda, S., Shaw, R. J., et al. (2009) · Science · doi:10.1126/science.1172156 · Cited by 958 · see citing works
Temperature as a Universal Resetting Cue for Mammalian Circadian Oscillators
Buhr, E. D., Yoo, S.-H., & Takahashi, J. S. (2010) · Science · doi:10.1126/science.1195262 · Cited by 917 · see citing works
Diurnal transcriptome atlas of a primate across major neural and peripheral tissues
Mure, L. S., Le, H. D., Benegiamo, G., Chang, M. W., Ríos, L., Jillani, N., Ngotho, M., Kariuki, T., Dkhissi‐Benyahya, O., Cooper, H. M., et al. (2018) · Science · doi:10.1126/science.aao0318 · Cited by 783 · see citing works
Driver, H. S., & Taylor, S. R. (2000) · Sleep Medicine Reviews · doi:10.1053/smrv.2000.0110 · Cited by 769 · 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
Health effects of shift work and extended hours of work
Harrington, J. M. (2001) · Occupational and Environmental Medicine · doi:10.1136/oem.58.1.68 · Cited by 703 · 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
Gabel, K., Hoddy, K. K., Haggerty, N., Song, J., Kroeger, C. M., Trepanowski, J. F., Panda, S., & Varady, K. A. (2018) · Nutrition and Healthy Aging · doi:10.3233/nha-170036 · Cited by 631 · see citing works
Circadian time signatures of fitness and disease
Bass, J. T., & Lazar, M. A. (2016) · Science · doi:10.1126/science.aah4965 · Cited by 616 · see citing works
Sleep Restriction for 1 Week Reduces Insulin Sensitivity in Healthy Men
Buxton, O. M., Pavlova, M., Reid, E. W., Wang, W., Simonson, D. C., & Adler, G. K. (2010) · Diabetes · doi:10.2337/db09-0699 · Cited by 604 · see citing works
Sleep Duration as a Risk Factor for Diabetes Incidence in a Large US Sample
Gangwisch, J. E., Heymsfield, S. B., Boden-Albala, B., Buijs, R. M., Kreier, F., Pickering, T. G., Rundle, A. G., Zammit, G. K., & Malaspina, D. (2007) · Sleep · doi:10.1093/sleep/30.12.1667 · Cited by 573 · see citing works
Circadian Variation in Sports Performance
Atkinson, G., & Reilly, T. (1996) · Sports Medicine · doi:10.2165/00007256-199621040-00005 · Cited by 558 · see citing works
Meal frequency and timing in health and disease
Mattson, M. P., Allison, D. B., Fontana, L., Harvie, M., Longo, V. D., Malaisse, W. J., Mosley, M., Notterpek, L. M., Ravussin, É., Scheer, F. A. J. L., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1413965111 · Cited by 533 · 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
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
Peek, C. B., Levine, D. C., Cedernaes, J., Taguchi, A., Kobayashi, Y., Tsai, S. J., Bonar, N. A., McNulty, M., Ramsey, K. M., & Bass, J. T. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.09.010 · Cited by 415 · see citing works
The effects of acute exercise on sleep: a quantitative synthesis
Youngstedt, S. D., O'Connor, P. J., & Dishman, R. K. (1997) · Sleep · doi:10.1093/sleep/20.3.203 · Cited by 412 · see citing works
Modeling of a Human Circadian Mutation Yields Insights into Clock Regulation by PER2
Xu, Y., Toh, K. L., Jones, C. R., Shin, J., Fu, Y., & Ptáček, L. J. (2007) · Cell · doi:10.1016/j.cell.2006.11.043 · Cited by 405 · see citing works
Morton, R. W., Oikawa, S. Y., Wavell, C. G., Mazara, N., McGlory, C., Quadrilatero, J., Baechler, B. L., Baker, S. K., & Phillips, S. M. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00154.2016 · Cited by 404 · see citing works
Mutation of the Human Circadian Clock Gene CRY1 in Familial Delayed Sleep Phase Disorder
Patke, A., Murphy, P. J., Onat, O. E., Krieger, A. C., Özçelik, T., Campbell, S. S., & Young, M. W. (2017) · Cell · doi:10.1016/j.cell.2017.03.027 · Cited by 381 · see citing works
Night Shift Work, Genetic Risk, and Type 2 Diabetes in the UK Biobank
Vetter, C., Dashti, H. S., Lane, J. M., Anderson, S. G., Schernhammer, E. S., Rutter, M. K., Saxena, R., & Scheer, F. A. J. L. (2018) · Diabetes Care · doi:10.2337/dc17-1933 · Cited by 371 · see citing works
Circadian Control of DRP1 Activity Regulates Mitochondrial Dynamics and Bioenergetics
Schmitt, K., Grimm, A., Dallmann, R., Oettinghaus, B., Restelli, L. M., Witzig, M., Ishihara, N., Mihara, K., Ripperger, J. A., Albrecht, U., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.01.011 · Cited by 336 · see citing works
Circadian rhythms, time-restricted feeding, and healthy aging
Manoogian, E. N. C., & Panda, S. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.12.006 · Cited by 330 · see citing works
The Effect of Training at a Specific Time of Day
Chtourou, H., & Souissi, N. (2012) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31825770a7 · Cited by 329 · see citing works
The epidemiology of sleep and obesity
Ogilvie, R. P., & Patel, S. R. (2017) · Sleep Health · doi:10.1016/j.sleh.2017.07.013 · Cited by 327 · see citing works
The Circadian Rhythm of Core Temperature: Origin and some Implications for Exercise Performance
Waterhouse, J. M., Drust, B., Weinert, D., Edwards, B., Gregson, W. A., Atkinson, G., Kao, S., Aizawa, S., & Reilly, T. P. (2005) · Chronobiology International · doi:10.1081/cbi-200053477 · Cited by 308 · see citing works
The impact of daytime light exposures on sleep and mood in office workers
Figueiro, M. G., Steverson, B., Heerwagen, J., Kampschroer, K., Hunter, C. M., Gonzales, K., Plitnick, B., & Rea, M. S. (2017) · Sleep Health · doi:10.1016/j.sleh.2017.03.005 · Cited by 308 · see citing works
Periodized Nutrition for Athletes
Jeukendrup, A. E. (2017) · Sports Medicine · doi:10.1007/s40279-017-0694-2 · 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
Time- and exercise-dependent gene regulation in human skeletal muscle
Zambon, A. C., McDearmon, E. L., Salomonis, N., Vranizan, K. M., Johansen, K. L., Adey, D., Takahashi, J. S., Schambelan, M., & Conklin, B. R. (2003) · Genome Biology · doi:10.1186/gb-2003-4-10-r61 · Cited by 254 · see citing works
Exercise, Energy Balance and the Shift Worker
Atkinson, G., Fullick, S., Grindey, C., & MacLaren, D. P. M. (2008) · Sports Medicine · doi:10.2165/00007256-200838080-00005 · Cited by 250 · see citing works
Exercise can improve sleep quality: A systematic review and meta-analysis
Banno, M., Harada, Y., Taniguchi, M., Tobita, R., Tsujimoto, H., Tsujimoto, Y., Kataoka, Y., & Noda, A. (2018) · PeerJ · doi:10.7717/peerj.5172 · Cited by 246 · see citing works
Um, J. H., Yang, S., Yamazaki, S., Kang, H., Viollet, B., Foretz, M., & Chung, J. H. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.c700070200 · Cited by 244 · see citing works
The Impact of Circadian Phenotype and Time since Awakening on Diurnal Performance in Athletes
Facer‐Childs, E. R., & Brandstätter, R. (2015) · Current Biology · doi:10.1016/j.cub.2014.12.036 · Cited by 236 · see citing works
Harfmann, B. D., Schroder, E. A., Kachman, M. T., Hodge, B. A., Zhang, X., & Esser, K. A. (2016) · Skeletal Muscle · doi:10.1186/s13395-016-0082-x · Cited by 231 · see citing works
PPARs Integrate the Mammalian Clock and Energy Metabolism
Chen, L., & Yang, G. (2014) · PPAR Research · doi:10.1155/2014/653017 · Cited by 223 · see citing works
Demonstration 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
Mitochondrial Dynamics in Diabetes
Yoon, Y., Galloway, C. A., Jhun, B. S., & Yu, T. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3286 · Cited by 216 · see citing works
Circadian 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
mTOR signaling regulates central and peripheral circadian clock function
Ramanathan, C., Kathale, N. D., Liu, D., Lee, C., Freeman, D. A., Hogenesch, J. B., Cao, R., & Liu, A. C. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007369 · Cited by 206 · see citing works
Type 2 Diabetes Mellitus and Skeletal Muscle Metabolic Function
Phielix, E., & Mensink, M. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.01.020 · Cited by 198 · see citing works
Effects of vigorous late-night exercise on sleep quality and cardiac autonomic activity
Myllymäki, T., Kyröläinen, H., Savolainen, K., Joensuu, L., Jakonen, R., Juuti, T., Martinmäki, K., Kaartinen, J., Kinnunen, M.-L., & Rusko, H. K. (2010) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2010.00874.x · Cited by 189 · see citing works
The Limits of Exercise Physiology: From Performance to Health
Gabriel, B. M., & Zierath, J. R. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.04.018 · Cited by 188 · see citing works
Self-citationMaximizing Cellular Adaptation to Endurance Exercise in Skeletal Muscle
Hawley, J. A., Lundby, C., Cotter, J. D., & Burke, L. M. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.04.014 · Cited by 182 · see citing works
Circadian 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
ENCODE whole-genome data in the UCSC genome browser (2011 update)
Raney, B. J., Cline, M., Rosenbloom, K. R., Dreszer, T. R., Learned, K., Barber, G. P., Meyer, L. R., Sloan, C. A., Malladi, V. S., Roskin, K. M., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1017 · Cited by 178 · see citing works
Sources of variation in back and leg dynamometry
COLDWELLS, A., Atkinson, G., & Reilly, T. (1994) · Ergonomics · doi:10.1080/00140139408963625 · Cited by 176 · see citing works
Sports and environmental temperature: From warming-up to heating-up
Racinais, S., Cocking, S., & Périard, J. D. (2017) · Temperature · doi:10.1080/23328940.2017.1356427 · Cited by 176 · see citing works
Effects of one night's sleep deprivation on anaerobic performance the following day
Souissi, N., Sesboüé, B., Gauthier, A., Larue, J., & Davenne, D. (2003) · European Journal of Applied Physiology · doi:10.1007/s00421-003-0793-7 · Cited by 175 · see citing works
Current views on hunter‐gatherer nutrition and the evolution of the human diet
Crittenden, A. N., & Schnorr, S. L. (2017) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23148 · Cited by 169 · see citing works
Circadian Clock Control by Polyamine Levels through a Mechanism that Declines with Age
Zwighaft, Z., Aviram, R., Shalev, M., Rousso-Noori, L., Kraut‐Cohen, J., Golik, M., Brandis, A. S., Reinke, H., Aharoni, A., Kahana, C., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.09.011 · Cited by 159 · see citing works
Overcoming Current Limitations in Humanized Mouse Research
Brehm, M. A., Shultz, L. D., Luban, J., & Greiner, D. L. (2013) · The Journal of Infectious Diseases · doi:10.1093/infdis/jit319 · Cited by 154 · see citing works
Dyar, 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
Gray, S. R., VITO, G. D., Nimmo, M. A., Farina, D., & Ferguson, R. A. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00291.2005 · Cited by 150 · see citing works
Seasonal variation in the human circadian rhythm: dissociation between sleep and temperature rhythm
Honma, K., Honma, S., Kohsaka, M., & Fukuda, N. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.262.5.r885 · Cited by 149 · see citing works
Atkinson, G., COLDWELLS, A., Reilly, T. P., & Waterhouse, J. M. (1993) · Ergonomics · doi:10.1080/00140139308967882 · Cited by 142 · see citing works
Time-of-day effects in maximal anaerobic leg exercise
Bernard, T. M., Giacomoni, M., Gavarry, O., et al. (1997) · European Journal of Applied Physiology and Occupational Physiology · doi:10.1007/s004210050311 · Cited by 141 · see citing works
Phase-shifting human circadian rhythms with exercise during the night shift
Eastman, C. I. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(95)02031-4 · Cited by 140 · see citing works
Hunter-gatherer diets—a different perspective
Milton, K. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.3.665 · Cited by 140 · see citing works
Effect of Time of Day and Partial Sleep Deprivation on Short‐Term, High‐Power Output
Souissi, N., Souissi, M. A., Souissi, H., Chamari, K., Tabka, Z., Dogui, M., & Davenne, D. (2008) · Chronobiology International · doi:10.1080/07420520802551568 · Cited by 139 · see citing works
Transcriptomic 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
Enhanced Endurance Performance by Periodization of Carbohydrate Intake: “Sleep Low” Strategy
MARQUET, L.-A., BRISSWALTER, J., LOUIS, J., TIOLLIER, E., BURKE, L. M., HAWLEY, J. A., & HAUSSWIRTH, C. (2016) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000823 · Cited by 134 · see citing works
Dempsey, P. C., Blankenship, J. M., Larsen, R. N., Sacre, J. W., Sethi, P., Straznicky, N. E., Cohen, N. D., Cerin, E., Lambert, G. W., Owen, N. G., et al. (2016) · Diabetologia · doi:10.1007/s00125-016-4169-z · Cited by 129 · see citing works
Friborg, O., Bjorvatn, B., Amponsah, B., & Pallesen, S. (2011) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2011.00982.x · Cited by 128 · see citing works
Chtourou, H., Driss, T., Souissi, S., Gam, A., Chaouachi, A., & Souissi, N. (2011) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31821d5e8d · Cited by 124 · see citing works
Diurnal Rhythm of the Muscular Performance of Elbow Flexors During Isometric Contractions
Gauthier, A., Davenne, D., Martin, A., et al. (1996) · Chronobiology International · doi:10.3109/07420529609037077 · Cited by 122 · see citing works
Effects of regular training at the same time of day on diurnal fluctuations in muscular performance
Souissi, N., Gauthier, A., Sesboüé, B., et al. (2002) · Journal of Sports Sciences · doi:10.1080/026404102320761813 · Cited by 117 · see citing works
Vera, B., Dashti, H. S., Gómez-Abellán, P., Hernández-Martínez, A. M., Esteban, A., Scheer, F. A. J. L., Saxena, R., & Garaulet, M. (2018) · Scientific Reports · doi:10.1038/s41598-017-18268-z · Cited by 117 · see citing works
DIURNAL VARIATION IN WINGATE TEST PERFORMANCES: INFLUENCE OF ACTIVE WARM-UP
Souissi, N., Driss, T., Chamari, K., et al. (2010) · Chronobiology International · doi:10.3109/07420528.2010.483157 · Cited by 116 · see citing works
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
Fernandes, A. L., Lopes‐Silva, J. P., Bertuzzi, R., Casarini, D. E., Arita, D. Y., Bishop, D. J., & Lima‐Silva, A. E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109954 · Cited by 109 · see citing works
Edwards, B., Waterhouse, J. M., Reilly, T. P., & Atkinson, G. (2002) · Chronobiology International · doi:10.1081/cbi-120004227 · Cited by 106 · see citing works
Effects of sleeping with reduced carbohydrate availability on acute training responses
Lane, S. C., Camera, D. M., Lassiter, D. G., Areta, J. L., Bird, S. R., Yeo, W. K., Jeacocke, N. A., Krook, A., Zierath, J. R., Burke, L. M., et al. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00857.2014 · Cited by 102 · see citing works
Self-citationChronobiological effects on exercise performance and selected physiological responses
Deschenes, M. R., Sharma, J. V., Brittingham, K., Casa, D. J., Armstrong, L. E., & Maresh, C. M. (1998) · European Journal of Applied Physiology · doi:10.1007/s004210050329 · Cited by 101 · see citing works
Molecular mechanisms of the circadian clockwork in mammals
Robinson, I., & Reddy, A. B. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.06.005 · Cited by 100 · see citing works
Greater Effect of East versus West Travel on Jet Lag, Sleep, and Team Sport Performance
Fowler, P. M., Knez, W. L., Crowcroft, S., Mendham, A. E., Miller, J., Sargent, C., Halson, S. L., & Duffield, R. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001374 · Cited by 100 · see citing works
Küüsmaa-Schildt, M., Schumann, M., Sedliak, M., Kraemer, W. J., Newton, R. U., Malinen, J.-P., Nyman, K., HÄKKINEN, A. H., & Häkkinen, K. (2016) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2016-0271 · Cited by 99 · see citing works
Biorhythmic influences on functional capacity of human muscle and physiological responses
Deschenes, M. R., Kraemer, W. J., Bush, J. A., DOUGHTY, T. A., KIM, D., MULLEN, K. M., & RAMSEY, K. (1998) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199809000-00008 · Cited by 88 · see citing works
The 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
Villard, J., Peretti, M., Masternak, K., Barras, E., Caretti, G., Mantovani, R., & Reith, W. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.10.3364-3376.2000 · Cited by 86 · see citing works
Four days of simulated shift work reduces insulin sensitivity in humans
Bescós, R., Boden, M. J., Jackson, M. L., Trewin, A. J., Marin, E. C., Levinger, I., GARNHAM, A. P., Hiam, D., Falcão‐Tebas, F., Conte, F., et al. (2018) · Acta Physiologica · doi:10.1111/apha.13039 · Cited by 84 · see citing works
TIME-OF-DAY EFFECTS ON FATIGUE DURING A SUSTAINED ANAEROBIC TEST IN WELL-TRAINED CYCLISTS
Lericollais, R., Gauthier, A., Bessot, N., Sesboüé, B., & Davenne, D. (2009) · Chronobiology International · doi:10.3109/07420520903534492 · Cited by 83 · see citing works
Zhao, Y., Liu, M., Chan, X. Y., Tan, S. Y., Subramaniam, S., Fan, Y., Loh, E., Chang, K. T. E., Tan, T. C., & Chen, Q. (2017) · Blood · doi:10.1182/blood-2017-04-778779 · Cited by 82 · see citing works
Crosstalk between circadian rhythmicity, mitochondrial dynamics and macrophage bactericidal activity
Oliva, J., Moreno‐Altamirano, M. M. B., Pineda, B., Cauich-Sánchez, P. I., & Sánchez‐García, F. J. (2014) · Immunology · doi:10.1111/imm.12329 · Cited by 81 · see citing works
Callard, D., Davenne, D., Gauthier, A., et al. (2000) · Chronobiology International · doi:10.1081/cbi-100101075 · Cited by 81 · see citing works
Dashti, H. S., Smith, C. E., Lee, Y., Parnell, L. D., Lai, C., Arnett, D. K., Ordovás, J. M., & Garaulet, M. (2014) · Chronobiology International · doi:10.3109/07420528.2014.886587 · Cited by 80 · see citing works
Circadian Phase-Shifting Effects of Bright Light, Exercise, and Bright Light + Exercise
Moore, T. A. (2016) · Journal of Circadian Rhythms · doi:10.5334/jcr.137 · Cited by 80 · see citing works
Dyar, K. A., Ciciliot, S., Tagliazucchi, G. M., Pallafacchina, G., Tothova, J., Argentini, C., Agatea, L., Abraham, R., Ahdesmaki, M. J., Forcato, M., et al. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.09.004 · 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
High-intensity exercise attenuates postprandial lipaemia and markers of oxidative stress
Gabriel, B. M., Ratkevičius, A., Gray, P., Frenneaux, M. P., & Gray, S. R. (2012) · Clinical Science · doi:10.1042/cs20110600 · Cited by 71 · see citing works
Self-citationLowe, 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
The relations between sleep, time of physical activity, and time outdoors among adult women
Murray, K. A., Godbole, S., Natarajan, L., Full, K. M., Hipp, J., Glanz, K., Mitchell, J., Laden, F., James, P., Quante, M., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182013 · Cited by 68 · see citing works
Sato, S., Parr, E. B., Devlin, B. L., Hawley, J. A., & Sassone‐Corsi, P. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.06.008 · Cited by 63 · see citing works
MAXIMAL POWER, BUT NOT FATIGABILITY, IS GREATER DURING REPEATED SPRINTS PERFORMED IN THE AFTERNOON
Racinais, S., Perrey, S., Denis, R., et al. (2010) · Chronobiology International · doi:10.3109/07420521003668412 · Cited by 61 · see citing works
Castaingts, V., Martin, A., Hoecke, J. V., et al. (2004) · Chronobiology International · doi:10.1081/cbi-120039207 · Cited by 60 · see citing works
O’Connor, E., Kiely, C., O'Shea, D. B., Green, S., & Egaña, M. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00012.2012 · Cited by 56 · see citing works
Matsumoto, C. S., Almeida, L. O., Guimarães, D. M., Martins, M. D., Papagerakis, P., Papagerakis, S. M., Leopoldino, A. M., CASTILHO, R. M., & SQUARIZE, C. H. (2016) · Oncotarget · doi:10.18632/oncotarget.9877 · Cited by 55 · see citing works
Hansen, J., Timmers, S., Moonen‐Kornips, E., Duez, H., Staels, B., Hesselink, M. K. C., & Schrauwen, P. (2016) · Scientific Reports · doi:10.1038/srep35047 · Cited by 54 · see citing works
Regulation of Mammalian Physiology by Interconnected Circadian and Feeding Rhythms
Atger, F., Mauvoisin, D., Weger, B. D., Gobet, C., & Gachon, F. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00042 · Cited by 46 · see citing works
Gauthier, A., Davenne, D., Gentil, C., et al. (1997) · Chronobiology International · doi:10.3109/07420529709001420 · Cited by 45 · see citing works
Warm-Up Affects Diurnal Variation in Power Output
Taylor, K.-L., Cronin, J. B., Gill, N., et al. (2011) · International Journal of Sports Medicine · doi:10.1055/s-0030-1268437 · Cited by 45 · see citing works
mTOR signaling in VIP neurons regulates circadian clock synchrony and olfaction
Liu, D., Stowie, A. C., de Zavalía, N., Leise, T., Pathak, S. S., Drewes, L. R., Davidson, A. J., Amir, S., Sonenberg, N., & Cao, R. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1721578115 · Cited by 45 · see citing works
Atypical expression of circadian clock genes in denervated mouse skeletal muscle
Nakao, R., Yamamoto, S., Horikawa, K., Yasumoto, Y., Nikawa, T., Mukai, C. N., & Oishi, K. (2015) · Chronobiology International · doi:10.3109/07420528.2014.1003350 · Cited by 44 · see citing works
Blood temperature and perfusion to exercising and non‐exercising human limbs
González‐Alonso, J., Calbet, J. A. L., Boushel, R., et al. (2015) · Experimental Physiology · doi:10.1113/ep085383 · Cited by 42 · see citing works
Circadian Phenotype Composition is a Major Predictor of Diurnal Physical Performance in Teams
Facer‐Childs, E. R., & Brandstätter, R. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00208 · Cited by 42 · 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
Renström, F., Koivula, R. W., Varga, T. V., Hallmans, G., Mulder, H., Florez, J. C., Hu, F. B., & Franks, P. W. (2015) · Diabetologia · doi:10.1007/s00125-015-3533-8 · Cited by 37 · see citing works
Sedliak, M., Zeman, M., Buzgó, G., Cvečka, J., Hamar, D., Laczo, E., Okuliarová, M., Vanderka, M., Kampmiller, T., Häkkinen, K., et al. (2017) · Chronobiology International · doi:10.1080/07420528.2017.1411360 · Cited by 36 · see citing works
Atkinson, G., & Drust, B. (2005) · Clinics in Sports Medicine · doi:10.1016/j.csm.2004.11.001 · Cited by 32 · see citing works
Circadian rhythm of intracellular protein synthesis signaling in rat cardiac and skeletal muscles
Chang, S.-W., Yoshihara, T., Machida, S., & Naıto, H. (2016) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2016.12.005 · Cited by 32 · see citing works
Protein synthesis in skeletal muscle measured at different times during a 24 hour period
Reeds, P. J., Palmer, R. M., Hay, S. M., et al. (1986) · Bioscience Reports · doi:10.1007/bf01115008 · Cited by 31 · see citing works
Gray, S. R., Söderlund, K., & Ferguson, R. A. (2008) · Journal of Sports Sciences · doi:10.1080/02640410701744438 · Cited by 30 · see citing works
Boukelia, B., Fogarty, M., Davison, R. R., & Florida-James, G. D. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-016-3489-5 · Cited by 27 · see citing works
Pullinger, S. A., Oksa, J., Brocklehurst, E. L., et al. (2018) · Chronobiology International · doi:10.1080/07420528.2018.1444626 · Cited by 27 · see citing works
Lassiter, D. G., Sjögren, R. J. O., Gabriel, B. M., Krook, A., & Zierath, J. R. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.07.004 · Cited by 26 · see citing works
Self-citationPullinger, S. A., Oksa, J., Clark, L. F., et al. (2018) · Chronobiology International · doi:10.1080/07420528.2018.1454938 · Cited by 24 · see citing works
Gabriel, B. M., Pugh, J. K., Pruneta‐Deloche, V., Moulin, P., Ratkevičius, A., & Gray, S. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082669 · Cited by 19 · see citing works
Self-citationMorán‐Ramos, S., Guerrero‐Vargas, N. N., Méndez‐Hernández, R., Basualdo, M. D. C., Escobar, C., & Buijs, R. M. (2017) · Experimental Physiology · doi:10.1113/ep086026 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Exerkines in health, resilience and disease
Chow, L. S., Gerszten, R. E., Taylor, J. M., Pedersen, B. K., van Praag, H., Trappe, S., Febbraio, M. A., Galis, Z. S., Gao, Y., Haus, J. M., et al. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00641-2 · Cited by 927 · see citing works
Self-citationTranscriptomic profiling of skeletal muscle adaptations to exercise and inactivity
Pillon, N. J., Gabriel, B. M., Dollet, L., Smith, J. A. B., Sardón Puig, L., Botella, J., Bishop, D. J., Krook, A., & Zierath, J. R. (2020) · Nature Communications · doi:10.1038/s41467-019-13869-w · Cited by 457 · see citing works
Self-citationExercise Metabolism and Adaptation in Skeletal Muscle
Smith, J. A. B., Murach, K. A., Dyar, K. A., & Zierath, J. R. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00606-x · Cited by 342 · see citing works
Self-citationTime of exercise specifies the impact on muscle metabolic pathways and systemic energy homeostasis
Sato, S., Basse, A. L., Schönke, M., Chen, S., Samad, M., Altıntaş, A., Laker, R. C., Dalbram, E., Barrès, R., Baldi, P., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.03.013 · Cited by 298 · see citing works
Self-citationExercise sustains the hallmarks of health
Qiu, Y., Fernández-García, B., Lehmann, H. I., Li, G., Kroemer, G., López-Otín, C., & Xiao, J. (2023) · Journal of Sport and Health Science · doi:10.1016/j.jshs.2022.10.003 · Cited by 270 · see citing works
Food as a circadian time cue - evidence from human studies
Lewis, P., Oster, H., Korf, H. W., Foster, R. G., & Erren, T. C. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-0318-z · Cited by 207 · see citing works
Exercise Induces Tissue-Specific Adaptations to Enhance Cardiometabolic Health
Ashcroft, S. P., Stocks, B., Egan, B., & Zierath, J. R. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2023.12.008 · Cited by 149 · see citing works
Self-citationNoone, J., Mucinski, J. M., DeLany, J. P., Sparks, L. M., & Goodpaster, B. H. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2023.12.025 · Cited by 128 · see citing works
Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment
parker, J., O'Brien, C., Hawrelak, J., & Gersh, F. (2021) · doi:10.20944/preprints202112.0088.v1 · Cited by 113 · see citing works
Polycystic Ovary Syndrome: An Evolutionary Adaptation to Lifestyle and the Environment
Parker, J., O’Brien, C., Hawrelak, J., & Gersh, F. L. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19031336 · Cited by 114 · see citing works
Time-of-day dependent effects of contractile activity on the phase of the skeletal muscle clock
Kemler, D., Wolff, C. A., & Esser, K. A. (2020) · The Journal of Physiology · doi:10.1113/jp279779 · Cited by 87 · see citing works
A Time to Eat and a Time to Exercise
Parr, E. B., Heilbronn, L. K., & Hawley, J. A. (2020) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000207 · Cited by 65 · see citing works
Aging, circadian disruption and neurodegeneration: Interesting interplay
Verma, A. K., Singh, S., & Rizvi, S. I. (2023) · Experimental Gerontology · doi:10.1016/j.exger.2022.112076 · Cited by 55 · see citing works
Activity Tracker–Based Metrics as Digital Markers of Cardiometabolic Health: Cross-Sectional Study
Rykov, Y., Thach, T.-Q., Dunleavy, G., Roberts, A. C., Christopoulos, G., Soh, C. K., & Car, J. (2020) · JMIR mHealth and uHealth · doi:10.2196/16409 · Cited by 29 · see citing works
Cao, X., & Thyfault, J. P. (2023) · Experimental Gerontology · doi:10.1016/j.exger.2023.112178 · Cited by 25 · see citing works
Dynamic modulation of glucose utilisation by glucocorticoid rhythms in health and disease
Zavala, E., Gil-Gómez, C. A., Wedgwood, K. C. A., Burgess, R., Tsaneva-Atanasova, K., & Herrera-Valdez, M. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.27.968354 · Cited by 8 · see citing works
Exercise: it's only a matter of time
Saner, N. J., & Lee, M. J. (2020) · The Journal of Physiology · doi:10.1113/jp280366 · Cited by 5 · see citing works
- Authors
- Gabriel, B. M., & Zierath, J. R.
- Affiliations
- Karolinska Institutet (SE)
- University of Copenhagen (DK)
- Corresponding author
- Zierath, Juleen R.
- Venue
- Nature Reviews Endocrinology
- Published
- 2019-01-17
- Volume
- 15
- Issue
- 4
- Pages
- 197-206
- ISSN
- 1759-5029 (ISSN-L)
- 1759-5037
- OpenAlex
- W2910358458
- Cited by
- 382
- References
- 124
- Citations by year
- 2026: 67 · 2025: 46 · 2024: 64 · 2023: 60 · 2022: 55 · 2021: 38 · 2020: 37 · 2019: 15
- FWCI
- 4.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
- Funders
- Novo Nordisk
- Novo Nordisk Fonden (NNF17OC0030088, NNF14OC0011493)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Keywords
- circadian rhythm, exercise timing, metabolic disorders, skeletal muscle metabolism, circadian clock, clock-controlled genes, mitochondrial function, shift work, insulin resistance, zeitgebers, exercise intervention
- MeSH terms
- Healthy Lifestyle, Circadian Rhythm, Female, Humans, Male, Metabolic Diseases, Exercise, Exercise Tolerance, Muscle, Skeletal, Resistance Training, 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 ›
Are you an author, or do you see a problem with this page? Request a review