Scheduled exercise phase shifts the circadian clock in skeletal muscle
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PURPOSE: It has been well established in mammals that circadian behavior as well as the molecular clockwork can be synchronized to the light-dark cycle via the suprachiasmatic nucleus of the hypothalamus (SCN). In addition to light, it has been demonstrated that nonphotic time cues, such as restricting the time of food availability, can alter circadian behavior and clock gene expression in selected peripheral tissues such as the liver. Studies have also suggested that scheduled physical activity (exercise) can alter circadian rhythms in behavior and clock gene expression; however, currently, the effects of exercise alone are largely unknown and have not been explored in skeletal muscle. METHODS: Period2::Luciferase (Per2::Luc) mice were maintained under 12 h of light followed by 12 h of darkness then exposed to 2 h of voluntary or involuntary exercise during the light phase for 4 wk. Control mice were left in home cages or moved to the exercise environment (sham). A second group of mice had restricted access to food (4 h · d(-1) for 2 wk) to compare the effects of two nonphotic cues on PER2::LUC bioluminescence. Skeletal muscle, lung, and SCN tissue explants were cultured for 5-6 d to study molecular rhythms. RESULTS: In the exercised mice, the phase of peak PER2::LUC bioluminescence was shifted in the skeletal muscle and lung explants but not in the SCN suggesting a specific synchronizing effect of exercise on the molecular clockwork in peripheral tissues. CONCLUSIONS: These data provide evidence that the molecular circadian clock in peripheral tissues can respond to the time of exercise suggesting that physical activity contributes important timing information for synchronization of circadian clocks throughout the body.
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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 [31]
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Cites
Coordination of circadian timing in mammals
Reppert, S. M., & Weaver, D. R. (2002) · Nature · doi:10.1038/nature00965 · Cited by 4,379 · 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
Adverse metabolic and cardiovascular consequences of circadian misalignment
Scheer, F. A. J. L., Hilton, M. F., Mantzoros, C. S., & Shea, S. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808180106 · Cited by 2,351 · see citing works
Yoo, S.-H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H.-K., Oh, W. J., Yoo, O. J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308709101 · Cited by 2,329 · see citing works
Resetting central and peripheral circadian oscillators in transgenic rats
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R.-I., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M., & Tei, H. (2000) · Science · doi:10.1126/science.288.5466.682 · Cited by 1,907 · 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
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
Food Intake, Water Intake, and Drinking Spout Side Preference of 28 Mouse Strains
Bachmanov, A. A., Reed, D. R., Beauchamp, G. K., & Tordoff, M. G. (2002) · Behavior Genetics · doi:10.1023/a:1020884312053 · Cited by 679 · see citing works
The “other” circadian system: food as a Zeitgeber
Stephan, F. K. (2002) · Journal of Biological Rhythms · doi:10.1177/074873002129002591 · Cited by 672 · 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
Characterization of Peripheral Circadian Clocks in Adipose Tissues
Zvonic, S., Ptitsyn, A. A., Conrad, S. A., Scott, L. K., Floyd, Z. E., Kilroy, G. E., Wu, X., Goh, B. C. K., Mynatt, R. L., & Gimble, J. M. (2006) · Diabetes · doi:10.2337/diabetes.55.04.06.db05-0873 · Cited by 495 · see citing works
Obesity and shift work: chronobiological aspects
Antunes, L. C., Levandovski, R., Dantas, G., Caumo, W., & Hidalgo, M. P. (2010) · Nutrition Research Reviews · doi:10.1017/s0954422410000016 · Cited by 493 · see citing works
LOCOMOTOR ACTIVITY AND NON‐PHOTIC INFLUENCES ON CIRCADIAN CLOCKS
Mrosovsky, N. (1996) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1996.tb01278.x · Cited by 412 · see citing works
Feedback repression is required for mammalian circadian clock function
Sato, T. K., Yamada, R. G., Ukai, H., Baggs, J. E., Miraglia, L. J., Kobayashi, T., Welsh, D. K., Kay, S. A., Ueda, H. R., & Hogenesch, J. B. (2006) · Nature Genetics · doi:10.1038/ng1745 · Cited by 373 · 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
Loss of entrainment and anatomical plasticity after lesions of the hamster retinohypothalamic tract
Johnson, R. F., Moore, R. Y., & Morin, L. P. (1988) · Brain Research · doi:10.1016/0006-8993(88)90374-5 · Cited by 325 · see citing works
Anderson, R. A., Joyce, C. W., Davis, M., Reagan, J. W., Clark, M. A., Shelness, G. S., & Rudel, L. L. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.41.26747 · Cited by 302 · 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
Lerman, I. R., Harrison, B. C., Freeman, K., Hewett, T. E., Allen, D. L., Robbins, J. M., & Leinwand, L. A. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01045.2001 · Cited by 272 · see citing works
Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock
Storch, K.-F., & Weitz, C. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902063106 · Cited by 222 · see citing works
Regularly scheduled voluntary exercise synchronizes the mouse circadian clock
Edgar, D. M., & Dement, W. C. (1991) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1991.261.4.r928 · Cited by 219 · see citing works
MacLellan, J. D., Gerrits, M. F., Gowing, A., Smith, P. J. S., Wheeler, M. B., & Harper, M.-E. (2005) · Diabetes · doi:10.2337/diabetes.54.8.2343 · Cited by 213 · see citing works
Real-time luminescence reporting of circadian gene expression in mammals
Yamazaki, S., & Takahashi, J. S. (2005) · Methods in Enzymology · doi:10.1016/s0076-6879(05)93012-7 · Cited by 200 · see citing works
Cailotto, C., La Fleur, S. E., Van Heijningen, C., Wortel, J., Kalsbeek, A., Feenstra, M., Pévet, P., & Buijs, R. M. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04439.x · Cited by 191 · see citing works
Ruiter, M., La Fleur, S. E., van Heijningen, C., van der Vliet, J., Kalsbeek, A., & Buijs, R. M. (2003) · Diabetes · doi:10.2337/diabetes.52.7.1709 · Cited by 170 · see citing works
Entrainment and phase shifting of circadian rhythms in mice by forced treadmill running
Marchant, E. G., & Mistlberger, R. E. (1996) · Physiology & Behavior · doi:10.1016/s0031-9384(96)80045-x · Cited by 145 · see citing works
Kelly, D. P., Kim, J. J., Billadello, J. J., Hainline, B. E., Chu, T. W., & Strauss, A. W. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.12.4068 · Cited by 121 · see citing works
Peripheral oscillators: the driving force for food‐anticipatory activity
Escobar, C., Cailotto, C., Castellanos, A., Delgado, R. S., & Buijs, R. M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06972.x · Cited by 93 · 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
Regulatory mechanism governing the diurnal rhythm of intestinal H+/peptide cotransporter 1 (PEPT1)
Saito, H., Terada, T., Shimakura, J., Katsura, T., & Inui, K. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90317.2008 · Cited by 64 · see citing works
Food-anticipatory activity and liver per1-luc activity in diabetic transgenic rats
Davidson, A. J., Stokkan, K., Yamazaki, S., & Menaker, M. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00680-7 · Cited by 59 · see citing works
Feeding-entrained circadian rhythms in hypophysectomized rats with suprachiasmatic nucleus lesions
Davidson, A. J., & Stephan, F. K. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.277.5.r1376 · Cited by 52 · see citing works
Physical activity reduces prostate carcinogenesis in a transgenic model
Esser, K. A., Harpole, C. E., Prins, G. S., & Diamond, A. M. (2009) · The Prostate · doi:10.1002/pros.20987 · Cited by 48 · see citing works
Chuang, D., Hu, C.-W. C., Ku, L. S., et al. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)47296-6 · Cited by 40 · see citing works
Feillet, C. A., Mendoza, J., Pévet, P., & Challet, É. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06538.x · Cited by 33 · see citing works
Repeated rat exposure inhibits the circadian activity patterns of C57BL/6J mice in the home cage
Dalm, S., de Visser, L., Spruijt, B. M., & Oitzl, M. S. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.07.035 · Cited by 25 · see citing works
García-Hernández, F., Aguilar‐Roblero, R. A., & Druker-Colín, R. (1987) · Brain Research · doi:10.1016/0006-8993(87)90980-2 · Cited by 14 · see citing works
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Molecular mechanisms and physiological importance of circadian rhythms
Patke, A., Young, M. W., & Axelrod, S. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0179-2 · Cited by 1,388 · see citing works
Circadian clocks and insulin resistance
Stenvers, D. J., Scheer, F. A. J. L., Schrauwen, P., la Fleur, S. E., & Kalsbeek, A. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-018-0122-1 · Cited by 733 · see citing works
Circadian Rhythm and Sleep Disruption: Causes, Metabolic Consequences, and Countermeasures
Potter, G. D., Skene, D. J., Arendt, J., Cade, J. E., Grant, P. J., & Hardie, L. J. (2016) · Endocrine Reviews · doi:10.1210/er.2016-1083 · Cited by 729 · see citing works
Correa-de-Araujo, R., Addison, O., Miljkovic, I., Goodpaster, B. H., Bergman, B. C., Clark, R. V., Elena, J. W., Esser, K. A., Ferrucci, L., Harris-Love, M. O., et al. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00963 · Cited by 468 · see citing works
Pérez‐Martínez, P., Mikhailidis, D. P., Athyros, V. G., Bulló, M., Couture, P., Covas, M. I., de Koning, L., Delgado‐Lista, J., Díaz‐López, A., Drevon, C. A., et al. (2017) · Nutrition Reviews · doi:10.1093/nutrit/nux014 · Cited by 413 · see citing works
Circadian rhythms and exercise — re-setting the clock in metabolic disease
Gabriel, B. M., & Zierath, J. R. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-018-0150-x · Cited by 382 · 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
Exercise 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
Crouse, J. J., Carpenter, J. S., Song, Y. J. C., Hockey, S. J., Naismith, S. L., Grunstein, R. R., Scott, E. M., Merikangas, K. R., Scott, J. L., & Hickie, I. B. (2021) · The Lancet Psychiatry · doi:10.1016/s2215-0366(21)00034-1 · Cited by 266 · 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
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
Self-citationThe 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
Atlas of exercise metabolism reveals time-dependent signatures of metabolic homeostasis
Sato, S., Dyar, K. A., Treebak, J. T., Jepsen, S. L., Ehrlich, A. M., Ashcroft, S. P., Trost, K., Kunzke, T., Prade, V. M., Small, L., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2021.12.016 · Cited by 203 · see citing works
Sleep in the United States Military
Good, C. H., Brager, A. J., Capaldi, V. F., & Mysliwiec, V. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0431-7 · Cited by 191 · see citing works
Mechanisms of Communication in the Mammalian Circadian Timing System
Astiz, M., Heyde, I., & Oster, H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020343 · Cited by 172 · see citing works
Interconnections between circadian clocks and metabolism
Guan, D., & Lazar, M. A. (2021) · Journal of Clinical Investigation · doi:10.1172/jci148278 · Cited by 166 · see citing works
Mammalian circadian systems: Organization and modern life challenges
Finger, A., & Kramer, A. (2021) · Acta Physiologica · doi:10.1111/apha.13548 · Cited by 117 · see citing works
Circadian Rhythms, Exercise, and Cardiovascular Health
Hower, I. M., Harper, S. A., & Buford, T. W. (2018) · Journal of Circadian Rhythms · doi:10.5334/jcr.164 · Cited by 121 · 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
Moholdt, T. T., Parr, E. B., Devlin, B. L., Debik, J., Giskeødegård, G. F., & Hawley, J. A. (2021) · Diabetologia · doi:10.1007/s00125-021-05477-5 · Cited by 117 · see citing works
Borengasser, S. J., Kang, P., Faske, J. B., Gómez-Acevedo, H., Blackburn, M. L., Badger, T. M., & Shankar, K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0084209 · Cited by 112 · 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
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
Sasaki, H., Hattori, Y., Ikeda, Y., Kamagata, M., Iwami, S., Yasuda, S., Tahara, Y., & Shibata, S. (2016) · Scientific Reports · doi:10.1038/srep27607 · Cited by 104 · see citing works
Aoyama, S., & Shibata, S. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00063 · Cited by 106 · see citing works
de Guia, R. M., Agerholm, M., Nielsen, T. S., Consitt, L. A., Søgaard, D., Helge, J. W., Larsen, S., Brandauer, J., Houmard, J. A., & Treebak, J. T. (2019) · Physiological Reports · doi:10.14814/phy2.14139 · Cited by 99 · see citing works
Metabolic Implications of Exposure to Light at Night: Lessons from Animal and Human Studies
Fleury, G., Masís‐vargas, A., & Kalsbeek, A. (2020) · Obesity · doi:10.1002/oby.22807 · Cited by 100 · 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
The circadian clock and metabolic homeostasis: entangled networks
de Assis, L. V. M., & Oster, H. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03800-2 · Cited by 96 · 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
Time-of-Day-Dependent Physiological Responses to Meal and Exercise
Aoyama, S., & Shibata, S. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.00018 · Cited by 95 · see citing works
Circadian desynchrony and glucose metabolism
Speksnijder, E. M., Bisschop, P. H. L. T., Siegelaar, S. E., Stenvers, D. J., & Kalsbeek, A. (2024) · Journal of Pineal Research · doi:10.1111/jpi.12956 · Cited by 98 · see citing works
Circadian Synchrony: Sleep, Nutrition, and Physical Activity
Healy, K. L., Morris, A. R., & Liu, A. C. (2021) · Frontiers in Network Physiology · doi:10.3389/fnetp.2021.732243 · Cited by 90 · 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
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
Self-citationMorita, H., Kano, C., Ishii, C., Kagata, N., Ishikawa, T., Hirayama, A., Uchiyama, Y., Hara, S., Nakamura, T., & Fukuda, S. (2023) · Science Advances · doi:10.1126/sciadv.add2120 · Cited by 82 · see citing works
Time-of-Day Effects on Short-Duration Maximal Exercise Performance
Mirizio, G. G., Nunes, R. S. M., Vargas, D. A., Foster, C., & Vieira, E. C. (2020) · Scientific Reports · doi:10.1038/s41598-020-66342-w · Cited by 81 · 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
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
Yasumoto, Y., Nakao, R., & Oishi, K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116476 · Cited by 77 · see citing works
Drăgoi, C. M., Nicolae, A. C., Ungurianu, A., Margina, D. M., Grădinaru, D., & Dumitrescu, I.-B. (2024) · Cells · doi:10.3390/cells13020138 · Cited by 71 · 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
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
Pastore, S., & Hood, D. A. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01505.2012 · Cited by 66 · 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
Circadian 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
Lorsung, E., Ramanujam, K., & Cao, R. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.642745 · Cited by 63 · see citing works
Murach, K. A., Liu, Z., Jude, B., Figueiredo, V. C., Wen, Y., Khadgi, S., Lim, S., da Silva, F. M., Greene, N. P., Lanner, J. T., et al. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102515 · Cited by 60 · see citing works
Opperhuizen, A., Wang, D., Foppen, E., Jansen, R., Surovtseva, O. V., de Vries, J., Fliers, E., & Kalsbeek, A. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13377 · Cited by 62 · see citing works
Cedernaes, J., Fanelli, F., Fazzini, A., Pagotto, U., Broman, J.-E., Vogel, H., Dickson, S. L., Schiöth, H. B., & Benedict, C. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.014 · Cited by 59 · see citing works
Barriers in translating preclinical rodent exercise metabolism findings to human health
Fuller, K. N. Z., & Thyfault, J. P. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00683.2020 · Cited by 57 · see citing works
Circadian Rhythms, the Gut Microbiome, and Metabolic Disorders
Zhao, E. H., Tait, C., Minacapelli, C. D., Catalano, C., & Rustgi, V. K. (2022) · Gastro Hep Advances · doi:10.1016/j.gastha.2021.10.008 · Cited by 61 · see citing works
Fernandez‐Gonzalo, R., Tesch, P. A., Lundberg, T. R., Alkner, B. A., Rullman, E., & Gustafsson, T. P. (2020) · The FASEB Journal · doi:10.1096/fj.201902976r · Cited by 59 · see citing works
Liver 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
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
Prospects for circadian treatment of mood disorders
Hühne-Landgraf, A., Welsh, D. K., & Landgraf, D. (2018) · Annals of Medicine · doi:10.1080/07853890.2018.1530449 · Cited by 57 · see citing works
Contraction influences Per2 gene expression in skeletal muscle through a calcium‐dependent pathway
Small, L., Altıntaş, A., Laker, R. C., Ehrlich, A. M., Pattamaprapanont, P., Villarroel, J., Pillon, N. J., Zierath, J. R., & Barrès, R. (2020) · The Journal of Physiology · doi:10.1113/jp280428 · Cited by 56 · 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
Wheel-running activity modulates circadian organization and the daily rhythm of eating behavior
Pendergast, J. S., Branecky, K. L., Huang, R., Niswender, K. D., & Yamazaki, S. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00177 · Cited by 53 · see citing works
Clock proteins and training modify exercise capacity in a daytime-dependent manner
Adamovich, Y., Dandavate, V., Ezagouri, S., Manella, G., Zwighaft, Z., Sobel, J., Kuperman, Y., Golik, M., Auerbach, A., Itkin, M., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2101115118 · Cited by 51 · see citing works
The role of circadian clocks in metabolic disease.
Li, M., Li, C.-M., & Wang, Z. (2012) · Europe PMC (PubMed Central) · Cited by 52 · 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
Basse, A. L., Dalbram, E., Larsson, L., Gerhart-Hines, Z., Zierath, J. R., & Treebak, J. T. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01198 · Cited by 52 · see citing works
Hamaguchi, Y., Tahara, Y., Hitosugi, M., & Shibata, S. (2015) · Journal of Biological Rhythms · doi:10.1177/0748730415609727 · Cited by 51 · see citing works
Vitale, J. A., Bonato, M., Torre, A. L., & Banfi, G. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174318 · Cited by 51 · see citing works
Basti, A., Yalçın, M., Herms, D., Hesse, J., Aboumanify, O., Li, Y., Aretz, Z. E. H., Garmshausen, J., El‐Athman, R., Hastermann, M., et al. (2021) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2020-000876 · Cited by 49 · see citing works
Chronic phase advance alters circadian physiological rhythms and peripheral molecular clocks
Wolff, G., Duncan, M. J., & Esser, K. A. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01139.2012 · Cited by 49 · see citing works
Circadian and Circannual Regulation in the Horse: Internal Timing in an Elite Athlete
Murphy, B. A. (2019) · Journal of Equine Veterinary Science · doi:10.1016/j.jevs.2019.02.026 · Cited by 48 · see citing works
Morris, H., Gonçalves, C. F., Dudek, M., Hoyland, J. A., & Meng, Q. (2021) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2020-219515 · 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
Yalçın, M., Mundorf, A., Thiel, F., Amatriain‐Fernández, S., Kalthoff, I. S., Beucke, J., Budde, H., Garthus‐Niegel, S., Peterburs, J., & Relógio, A. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.873237 · Cited by 46 · see citing works
Mechanical loading and hyperosmolarity as a daily resetting cue for skeletal circadian clocks
Dudek, M., Pathiranage, D. R., Baño‐Otálora, B., Paszek, A., Rogers, N., Gonçalves, C. F., Lawless, C., Wang, D., Luo, Z., Yang, L., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42056-1 · Cited by 44 · see citing works
Time for Exercise? Exercise and Its Influence on the Skeletal Muscle Clock
Martin, R. A., & Esser, K. A. (2022) · Journal of Biological Rhythms · doi:10.1177/07487304221122662 · Cited by 45 · see citing works
Chrono-exercise: Time-of-day-dependent physiological responses to exercise
Kim, H., Radak, Z. O., Takahashi, M., Inami, T., & Shibata, S. (2022) · Sports Medicine and Health Science · doi:10.1016/j.smhs.2022.11.003 · 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
When should I eat: A circadian view on food intake and metabolic regulation
Chamorro, R., Jouffe, C., Oster, H., Uhlenhaut, N. H., & Meyhöfer, S. M. (2023) · Acta Physiologica · doi:10.1111/apha.13936 · Cited by 40 · 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
Durgan, D. J., Crossland, R. F., & Bryan, R. M. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16675879 · Cited by 35 · 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
Peripheral Circadian Oscillators.
Brown, A. J., Pendergast, J. S., & Yamazaki, S. (2019) · PubMed Central · Cited by 36 · see citing works
Systematic Review and Meta-Analysis of Endurance Exercise Training Protocols for Mice
Massett, M. P., Matejka, C., & Kim, H. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.782695 · Cited by 35 · 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
Yamanaka, Y., Honma, S., & Honma, K. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00389.2013 · Cited by 35 · see citing works
Galbete, C., Contreras, R., Martínez, J. A., Martínez‐González, M. Á., Guillén‐Grima, F., & Martí, A. (2012) · Chronobiology International · doi:10.3109/07420528.2012.728657 · Cited by 35 · see citing works
Circadian Regulation of Cardiac Arrhythmias and Electrophysiology
Delisle, B. P., Prabhat, A., Burgess, D. E., Ono, M., Esser, K. A., & Schroder, E. A. (2024) · Circulation Research · doi:10.1161/circresaha.123.323513 · Cited by 34 · 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
Bone adaptation to mechanical loading in mice is affected by circadian rhythms
Bouchard, A. L., Dsouza, C., Julien, C., Rummler, M., Gaumond, M.-H., Cermakian, N., & Willie, B. M. (2021) · Bone · doi:10.1016/j.bone.2021.116218 · Cited by 33 · see citing works
Exercise Training Impacts Skeletal Muscle Clock Machinery in Prediabetes
Erickson, M. L., ZHANG, H., Mey, J. T., & Kirwan, J. P. (2020) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002368 · Cited by 31 · see citing works
Diurnal 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
Panhuis, W. I. H., Schönke, M., Modder, M., Tom, H. E., Lalai, R. A., Pronk, A. C. M., Streefland, T. C. M., van Kerkhof, L. W. M., Dollé, M. E. T., Depuydt, M. A. C., et al. (2023) · EBioMedicine · doi:10.1016/j.ebiom.2023.104680 · Cited by 29 · see citing works
da Silva, F. M., Esser, K. A., Murach, K. A., & Greene, N. P. (2023) · The Journal of Physiology · doi:10.1113/jp284808 · Cited by 28 · see citing works
Effect of a single bout of exercise on clock gene expression in human leukocyte
Tanaka, Y., Ogata, H., Kayaba, M., Ando, A., Park, I., Yajima, K., Araki, A., Suzuki, C., Osumi, H., Zhang, S., et al. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00891.2019 · Cited by 28 · see citing works
Tick tock, the cartilage clock
Rogers, N., & Meng, Q. (2023) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2023.05.010 · Cited by 28 · see citing works
Brito, L. C., Marin, T. C., Azevêdo, L. M., Rosa‐Silva, J. M., Shea, S. A., & Thosar, S. S. (2022) · Comprehensive physiology · doi:10.1002/cphy.c210036 · Cited by 45 · 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
The clock regulator Bmal1 protects against muscular dystrophy
Gao, H., Xiong, X., Lin, Y., Chatterjee, S., & Ma, K. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112348 · Cited by 26 · see citing works
Zeitgebers of skeletal muscle and implications for metabolic health
Gabriel, B. M., & Zierath, J. R. (2021) · The Journal of Physiology · doi:10.1113/jp280884 · Cited by 27 · see citing works
Adaptation of the transcriptional response to resistance exercise over 4 weeks of daily training
Viggars, M. R., Sutherland, H., Lanmüller, H., Schmoll, M., Bijak, M., & Jarvis, J. C. (2022) · The FASEB Journal · doi:10.1096/fj.202201418r · Cited by 26 · see citing works
Harmsen, J., Kotte, M., Habets, I., Bosschee, F., Frenken, K. G., Jörgensen, J. A., de Kam, S. S., Moonen‐Kornips, E., Cissen, J., Doligkeit, D., et al. (2023) · The Journal of Physiology · doi:10.1113/jp285523 · Cited by 25 · see citing works
- Authors
- WOLFF, G., & ESSER, K. A.
- Affiliations
- University of Kentucky (US)
- Corresponding author
- ESSER, KARYN A.
- ORCID
- ESSER, KARYN A.
- Venue
- Medicine & Science in Sports & Exercise
- Published
- 2012-09
- Volume
- 44
- Issue
- 9
- Pages
- 1663-1670
- ISSN
- 0195-9131 (ISSN-L)
- PMC
- PMC3414645
- OpenAlex
- W2033614839
- Semantic Scholar
- 86eaf33fe84d43f35401f4e3b3b39565c983af92
- Cited by
- 291
- References
- 37
- Citations by year
- 2026: 26 · 2025: 31 · 2024: 35 · 2023: 29 · 2022: 33 · 2021: 26 · 2020: 32 · 2019: 18 · 2018: 13 · 2017: 9 · 2016: 20 · 2015: 4 · 2014: 8 · 2013: 5 · 2012: 2
- FWCI
- 2.68
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Medicine & Science in Sports & Exercise (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (submittedVersion)
- Funders
- National Institutes of Health (5t32hl086341-05)
- National Heart, Lung, and Blood Institute (T32 HL086341-02, T32-HL-086341)
- National Institute of Environmental Health Sciences (RC1ES018636, ES-018636)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR055246, AR-055246)
- 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 clock, skeletal muscle, exercise timing, phase shift, clock gene expression, dietary restriction, suprachiasmatic nucleus, lung, voluntary exercise
- MeSH terms
- Animals, Circadian Rhythm, Physical Exertion, Female, Luciferases, Male, Mice, Inbred C57BL, Physical Conditioning, Animal, Photoperiod, Muscle, Skeletal, Mice, Circadian Clocks
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