Cited by 458Circadian rhythm and melatoninMetabolism, Diabetes, and CancerAdipose Tissue and Metabolism

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Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock

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Dyar, Kenneth A., Ciciliot, Stefano, Wright, Lauren E., Biensø, Rasmus S., Tagliazucchi, Guidantonio M., Patel, Vishal R., Forcato, Mattia, Paz, Marcia I.P., Gudiksen, Anders, Solagna, Francesca, Albiero, Mattia, Moretti, Irene, Eckel-Mahan, Kristin L., Baldi, Pierre, Sassone-Corsi, Paolo, Rizzuto, Rosario, Bicciato, Silvio, Pilegaard, Henriette, Blaauw, Bert, Schiaffino, Stefano·2014·Molecular Metabolism

DOI 10.1016/j.molmet.2013.10.005PMC PMC3929910

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Abstract

Circadian rhythms control metabolism and energy homeostasis, but the role of the skeletal muscle clock has never been explored. We generated conditional and inducible mouse lines with muscle-specific ablation of the core clock gene Bmal1. Skeletal muscles from these mice showed impaired insulin-stimulated glucose uptake with reduced protein levels of GLUT4, the insulin-dependent glucose transporter, and TBC1D1, a Rab-GTPase involved in GLUT4 translocation. Pyruvate dehydrogenase (PDH) activity was also reduced due to altered expression of circadian genes Pdk4 and Pdp1, coding for PDH kinase and phosphatase, respectively. PDH inhibition leads to reduced glucose oxidation and diversion of glycolytic intermediates to alternative metabolic pathways, as revealed by metabolome analysis. The impaired glucose metabolism induced by muscle-specific Bmal1 knockout suggests that a major physiological role of the muscle clock is to prepare for the transition from the rest/fasting phase to the active/feeding phase, when glucose becomes the predominant fuel for skeletal muscle.

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Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
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MethodInfluential
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Occupational and Environmental Medicine
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Background
Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes
Marcheva, B., Ramsey, K. M., Buhr, E. D., Kobayashi, Y., Su, H., Ko, C. H., Ivanova, G., Omura, C., Mo, S., Vitaterna, M. H., et al. (2010) · Nature · doi:10.1038/nature09253 · Cited by 1,525 · cited 1×
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Background
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Samuel, V. T., Petersen, K. F., & Shulman, G. I. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60408-4 · Cited by 1,189 · cited 1×
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Background

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Skeletal muscle clock and metabolism
Li, Y., & Chen, W. (2020) · Biological Rhythm Research · doi:10.1080/09291016.2020.1816037 · Cited by 3
“Many studies have shown that the endogenous biological clock in skeletal muscle tissue can modulate the energy metabolism of the body (Dyar et al. 2014, 2018; Hodge et al. 2015).”
BackgroundInfluential
Five Padua days on muscle and mobility medicine (2024Pdm3) 27 February - 2 March, 2024 at Hotel Petrarca, Thermae of Euganean Hills, Padua, and San Luca Hall, Prato della Valle, Padua, Italy
Zampieri, S., Bersch, I., Smeriglio, P., Barbieri, E., Ganassi, M., Leeuwenburg, C., Rosati, R., Gargiulo, P., Pond, A. L., Sweeney, H. L., et al. (2023) · European Journal of Translational Myology · doi:10.4081/ejtm.2023.12161 · Cited by 5
Daytime-Dependent Effects of Thiamine on the Thiamine Pool and Pyruvate Dehydrogenase Regulation in the Brain and Heart
Aleshin, V. A., Borisova, N., Artiukhov, A. V., Tagirov, K., Solovjeva, O. N., Lavrenteva, E., Panin, N. V., Maslova, M. V., & Graf, A. V. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26178296 · Cited by 4
“…and E2 [36,78,82], whereas stronger variation in PDHC activity and phosphorylation in skeletal muscle and heart seems to be focused mostly on PDK4 [80–83, 95 ], which we show Among the measured parameters, a striking difference in thiamine ability to enter the cerebral cortex and heart in the…”
Influential
Distinct diurnal temperature rhythm patterns in critical illness myopathy: secondary analysis of two prospective trials
Mewes, D., Weber-Carstens, S., Rubarth, K., Boie, S. D., Spies, C., Kramer, A., Fielitz, J., Wollersheim, T., Ananthasubramaniam, B., Braune, F., et al. (2025) · Annals of Intensive Care · doi:10.1186/s13613-025-01582-5 · Cited by 4
“Functional circadian rhythms are important for skeletal muscle homeostasis [12–14].”
Uncovering the muscle clock–mitochondria axis through exercise
Castro-Sepulveda, M. (2025) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2025.11.001 · Cited by 2
Dual roles of circadian clock proteins in development and adult homeostasis
Choi, M., Liang, S., & Alvarez‐Dominguez, J. R. (2026) · npj Biological Timing and Sleep · doi:10.1038/s44323-025-00061-1 · Cited by 3
Chrono-Exercise Medicine: Why Biological Timing Matters for Human Health
Hesketh, S. J. (2026) · Biomedicines · doi:10.3390/biomedicines14071601 · Cited by 4
“Core clock genes including BMAL1, CLOCK, PER, and CRY form transcriptional–translational feed-back loops [6] that coordinate daily rhythms in mitochondrial metabolism [13], gene expression [14], substrate utilization [15], protein turnover [16], and contractile function [17,18].”
The Postprandial Chronobiome in Interorgan Glucose Homeostasis
Božić, J., Šantić, R., & Kumrić, M. (2026) · Comprehensive physiology · doi:10.1002/cph4.70236 · Cited by 2
“Skeletal muscle expresses an intrinsic clock that primes the fasted- to-fed transition: muscle-specific Bmal1 ablation impairs insulin-stimulated glucose uptake with reduced GLUT4 and TBC1D1 (Dyar et al. 2014), while independent muscle-clock disruption lowers glycolytic flux and elevates fasting blood glucose (Harfman…”
Influential
The hallmarks of skeletal muscle health
Vainshtein, A., Blaauw, B., Bock, K. D., Muñoz‐Cánoves, P., Olson, E. N., Ottenheijm, C. A. C., Richter, E. A., Ruas, J. L., Schaeffer, L., Spiegelman, B. M., et al. (2026) · Nature Metabolism · doi:10.1038/s42255-026-01595-9 · Cited by 4
“These regulatory layers are further temporally organized by intrinsic muscle circadian clocks, which coordinate oscillations in metabolism, proteo-stasis and transcriptional programmes across the day–night cycle 316,317 .”
L'horloge biologique du muscle
Mayeuf-Louchart, A. (2020) · médecine/sciences · doi:10.1051/medsci/2020262 · Cited by 2
Circadian rhythms in muscle health and diseases
Kelu, J. J. (2024) · International review of cytology · doi:10.1016/bs.ircmb.2024.10.002 · Cited by 2
Live-cell GLUT4 translocation assay reveals Per3 as a novel regulator of circadian insulin sensitivity in skeletal muscle cells
Sivasengh, R., Scott, A., & Gabriel, B. M. (2025) · Biology Open · doi:10.1242/bio.061941 · Cited by 3
“…be noted that knockdown efficiency of Arntl was lower than that of Per3 , which may influence the magnitude of effect on GLUT4 translocation, and Arntl /Bmal1 has previously been implicated as a key modulator of glucose tolerance and insulin sensitivity (Dyar et al., 2014; Schiaffino et al., 2016).”
Effect of chrono-nutrition–based dietary intervention on metabolic disease
Chen, Y. (2024) · Precision Nutrition · doi:10.1097/pn9.0000000000000076 · Cited by 5
“[10] At the epicenter of circadian clock is a series of well-organized transcriptional-translational feedback loop (TTFL).”
THE IMPACT OF PHYSICAL EXERCISE ON THE SKELETAL MUSCLE CLOCK GENES
Mirizio, G. G., Nunes, R. S. M., Figueroa, A. L. C., de Sousa, I., Ferreira, A. P., & Vieira, E. C. (2018) · Kinesiology · Cited by 2
Potential molecular mechanisms underlying the ameliorative effect of Cola nitida (Vent.) Schott & Endl. on insulin resistance in rat skeletal muscles.
Erukainure, O., Oyebode, O., Chuturgoon, A., Ghazi, T., Muhammad, A., Aljoundi, A., Elamin, G., Chukwuma, C. I., & Islam, M. S. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.117249 · Cited by 1
Activity and phosphatidylcholine transfer protein interactions of skeletal muscle thioesterase Them2 enable hepatic steatosis and insulin resistance
Xie, Y., Liu, X., Liu, W., Carr, L. R., Lee, L. P., Imai, N., Ortlund, E. A., & Cohen, D. E. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107855 · Cited by 1
Effects of time-of-day on the noradrenaline, adrenaline, cortisol and blood lipidome response to an ice bath
Braunsperger, A., Bauer, M., Brahim, C. B., Seep, L., Tischer, D., Peitzsch, M., Hasenauer, J., Figueroa, S. H., Worthmann, A., Heeren, J., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-85304-8 · Cited by 2
Scheduled Exercise Partially Offsets Alcohol-Induced Clock Dysfunction in Skeletal Muscle and Liver of Female Mice
Tice, A. L., Lee, C., Hickner, R. C., & Steiner, J. L. (2025) · Journal of Biological Rhythms · doi:10.1177/07487304241312461 · Cited by 1
“…handling, strength, myofiber cross-sectional area, muscle size, and fiber-type distribution; alcohol-induced clock disruption may contribute to a myriad of harmful effects in the muscle (Andrews et al., 2010; Dyar et al., 2014; Hodge et al., 2015; Chatterjee et al., 2013; Harfmann et al., 2016).”
Impacts of exercise, renin–angiotensin system modulation or both on skeletal muscle circadian gene expression
Zumbro, E. L., Baptista, L. C. P., Taylor, T. L., Hernandez, A., Banerjee, A., Sun, Y., Yang, Y., Li, Q., & Buford, T. W. (2026) · Experimental Physiology · doi:10.1113/ep092318 · Cited by 1
“Skeletal muscle processes, such as myogenesis and metabolism, are regulated by an intrinsic circadian clock (Andrews et al., 2010; Dyar et al., 2014) and have been shown to contribute to sleep quality (Ehlen et al., 2017).”
Dietary polyphenols as candidate chrononutrients: Time-dependent modulation of gut microbial rhythmicity and metabolic control in obesity
Li, S., Ma, C., Yang, Y., Xu, X., Wang, J., Li, L., Xu, Y., & Zhang, N. (2026) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2026.105732 · Cited by 1
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
“The CR of skeletal muscle regulates insulin sensitivity and glucose metabolism, providing the energy foundation for skeletal muscle to respond to daily rest-activity patterns [73].”
Circadian Regulation of Glucose Metabolism: Implications for Pathogenesis and Chronotherapy of Type 2 Diabetes
Oraebosi, M. I., Baucom, C., & Cao, R. (2026) · Diabetology · doi:10.3390/diabetology7070122 · Cited by 2
“These include glucose uptake and oxidation via the GLUT4 transporter [38], glycogen synthesis and storage [69,70], mitochondrial oxidative metabolism [71], and protein and lipid turnover [72,73].”
Tuning in to the rhythm of clock genes in skeletal muscle
Zhou, Z., Chadt, A., & Al‐Hasani, H. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.11.001 · Cited by 1
“In this issue of Molecular Metabolism, Schiaffino and coworkers present convincing evidence for the physiological importance of a functional muscle clock [5].”
For Management of Obesity and Diabetes: Is Timing the Answer?
Sellix, M. T. (2016) · Endocrinology · doi:10.1210/en.2016-1799 · Cited by 1
The Role of Omics Approaches in Muscle Research
Schiaffino, S., Reggiani, C., & Murgia, M. (2019) · Springer eBooks · doi:10.1007/978-1-4939-9802-9_1 · Cited by 1
Effect of diurnal changes on dichotic listening in younger adults with normal hearing
Prakash, P., Vismaya, K. P., Mahesh, D. S., & Prabhu, P. (2022) · Journal of Otology · doi:10.1016/j.joto.2022.06.003 · Cited by 1
“Different stimuli like consonant-vowel (CV), digits (single, double, and triple), sentences, and rhymes have been used in evaluating the dichotic listening performances (Fifer et al., 1983; Moncrieff and Wilson, 2009; Shankweiler and Studdert-Kennedy, 1967; Wexler and Halwes, 1983).”
Method
Circadian Rhythms and Exercise Metabolism
Wolff, C. A., Hesketh, S. J., & Esser, K. A. (2022) · Physiology in health and disease · doi:10.1007/978-3-030-94305-9_16 · Cited by 1
Daily rhythms of diabetogenic factors in men: role of type 2 diabetes and body weight
Isherwood, C., Robertson, M. D., Skene, D. J., & Johnston, J. D. (2023) · Endocrine Connections · doi:10.1530/ec-23-0064 · Cited by 1
“Genetic lesioning of clocks in transgenic mouse studies has demonstrated the importance of individual peripheral clocks in key metabolic processes such as glucose homeostasis, insulin secretion and body weight regulation (5, 6, 7, 8, 9).”
Background
Circadian Clocks and Metabolism
Challet, É., & Vuillez, P. (2024) · Royal Society of Chemistry eBooks · doi:10.1039/bk9781839167553-00476 · Cited by 2
Nutrition, Epigenetics, and Circadian Rhythms
Cai, D., Liu, H., Li, K., & Zhu, Y. (2024) · Epigenetics and human health · doi:10.1007/978-3-031-54215-2_8 · Cited by 1
Insights into the influence of high‐intensity interval training on skeletal muscle clock gene expression in insulin‐resistant individuals
Desjardins, K., Taherkhani, S., Méthot, L., Castonguay, V., & Leduc‐Gaudet, J. (2024) · The Journal of Physiology · doi:10.1113/jp286939 · Cited by 1
“Consistent with this, Dr Stefano Schiaffino’s lab showed that muscle-specific inactivation of Bmal1 in mice triggered muscle insulin resistance and impaired glucose metabolism (Dyar et al., 2014).”
Tic‐tac‐mito: The relationship between the biological clock with mitochondria dynamics and skeletal muscle function in humans
de Jesus, I. C. G., & Araújo, F. M. (2024) · The Journal of Physiology · doi:10.1113/jp287210 · Cited by 1
“Of note, no histological evidence of muscle degeneration was seen in this model (Dyar et al., 2013).”
Developing Circadian Therapeutics Against Age-Related Metabolic Decline
Nohara, K., Yoo, S. H., & Chen, Z. (2017) · Healthy ageing and longevity · doi:10.1007/978-3-319-64543-8_11 · Cited by 1
Melatonin: Manager of psychosomatic and metabolic disorders in polymorbid cardiovascular pathology
Partsernyak, A. S., Polyakova, V. O., Trufanov, A. G., Медведев, Д. С., Витальевна, Т. Д., Markin, K. V., Курасов, Е. С., Kuznetsova, E. V., & Krasichkov, A. S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.989497 · Cited by 1
“The decrease in the glycemic level is compensated due to the circadian nature of glucose excretion from the liver, which depends on the daily rhythm of GLUT 2 expression, reaching its maximum during the resting– fasting phase (Dyar et al., 2014).”
Background
Positive Correlation Between Changes in Serum Albumin Levels and Breakfast Non-Protein Calorie/Nitrogen Ratio in Geriatric Patients
Fukuda, Y., Ochi, M., Kanazawa, R., Nakajima, H., Fukuo, K., & Nakai, M. (2023) · Journal of Clinical Medicine Research · doi:10.14740/jocmr4848 · Cited by 2
Reply from Elizabeth Schroder, Brian Hodge, Lance Riley, Xiping Zhang and Karyn Esser
Schroder, E. A., Hodge, B. A., Riley, L. A., Zhang, X., & Esser, K. A. (2016) · The Journal of Physiology · doi:10.1113/jp272165 · Cited by 1
“…clock genes (e.g. Rev-erb, Rora and Dbp) from muscle of the imKO mice generated by Dyar et al. it is difficult to completely resolve the underlying differences through which the phenotypes of the iMSBmal1 KO mouse we present in our paper compare to the imKO mouse described by Dyar et al. (2014).”
Result
Faculty Opinions recommendation of Acute sleep loss results in tissue-specific alterations in genome-wide DNA methylation state and metabolic fuel utilization in humans.
Kempermann, G. (2018) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733851922.793550051 · Cited by 1
Abstracts of the 2016 Spring Padua Muscle Days: Muscle decline in aging and neuromuscular disorders - Mechanisms and countermeasures | Terme Euganee, Padua, Italy, April 13-16, 2016
Editors, T. (2016) · European Journal of Translational Myology · doi:10.4081/ejtm.2016.5904 · Cited by 1
Impact of Bmal1 rescue and time-restricted feeding on liver and muscle proteomes during the active phase in micePreprint
Smith, J. G., Molendijk, J., Blazev, R., Chen, W. H., Zhang, Q., Litwin, C., Greco, C. M., Sassone‐Corsi, P., Muñoz‐Cánoves, P., Parker, B. L., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.12.544652 · Cited by 1
Synchronization of biological oscillators : modeling, analysis and coupling of the mammalian cell cycle and circadian clock
Almeida, S. J. F. (2018) · theses.fr (ABES) · doi:10.70675/d7f43940zfb09z447az8fcez09de3d68881f · Cited by 1
“of BMAL1 in promoting insulin sensitivity in mouse liver and muscle [97] [98], as well as the fact that CRY1, here presenting a similar trend as BMAL1, also plays a role in improving hepatic insulin sensitivity [99], these results may help to explain the higher incidence of insulin resistance in indiviuals subjected t…”
Background
What are the effects of circadian rhythms on the G-protein coupled receptors involved with glucose metabolism?
Skiffey, M. (2015) · Carroll Collected (John Carroll University)
Circadian Biology: Interaction with Metabolism and Nutrition
Johnston, J. D. (2016) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789813143319_0005
Obesity and Circadian System
Bakır, B. O. (2017) · Advances in Obesity Weight Management & Control · doi:10.15406/aowmc.2017.06.00146
“Besides, skeletal muscle specific BMAL1 knockout mice show impaired muscle glucose metabolism characterized by disrupted glucose stimulated insulin intake and reduced levels of insulin dependent glucose transporters [47].”
Background

Authors: 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., Albiero, M., Moretti, I., Eckel-Mahan, K. L., Baldi, P., Sassone-Corsi, P., Rizzuto, R., Bicciato, S., Pilegaard, H., Blaauw, B., & Schiaffino, S.
Affiliations: Veneto Institute of Molecular Medicine (IT)
University of Padua (IT)
University of Copenhagen (DK)
University of Modena and Reggio Emilia (IT)
University of California, Irvine (US)
Corresponding author: Dyar, Kenneth A.
Schiaffino, Stefano
ORCID: Dyar, Kenneth A.
Ciciliot, Stefano
Tagliazucchi, Guidantonio M.
Patel, Vishal R.
Forcato, Mattia
Paz, Marcia I.P.
Gudiksen, Anders
Solagna, Francesca
Albiero, Mattia
Baldi, Pierre
Rizzuto, Rosario
Bicciato, Silvio
Pilegaard, Henriette
Blaauw, Bert
Schiaffino, Stefano
Venue: Molecular Metabolism
Publisher: Elsevier BV
Published: 2014-02
Volume: 3
Issue: 1
Pages: 29-41
ISSN: 2212-8778 (ISSN-L)
DOI: 10.1016/j.molmet.2013.10.005
PMC: PMC3929910
OpenAlex: W1964634897
Cited by: 454
References: 73
Citations by year: 2026: 34 · 2025: 37 · 2024: 40 · 2023: 46 · 2022: 42 · 2021: 33 · 2020: 53 · 2019: 34 · 2018: 36 · 2017: 28 · 2016: 42 · 2015: 19 · 2014: 9
FWCI: 12.78
Type: journal article
Language: en
Update notices: erratum (2014-12-01)
Open access: gold
doi.org
Licence: cc-by-nc-sa
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-sa/3.0/ (vor)
Locations: Molecular Metabolism (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, other-oa)
eScholarship (California Digital Library) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by-nc-sa)
IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by-nc-sa)
Padua Research Archive (University of Padova) (submittedVersion)
Funders: European Commission (223576, 294777)
Italian Space Agency (ASI, project OSMA)
Italian Ministries of Health (Ricerca Finalizzata) and of Education, University and Research (PRIN, FIRB), NIA (2P01AG025532-06A1)
Cariparo Foundation (Padua)
Italian Association for Cancer Research (AIRC) and Telethon–Italy (GPP1005A, GGP11082)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
Keywords: circadian rhythm, Bmal1, insulin sensitivity, glucose uptake, GLUT4, TBC1D1, pyruvate dehydrogenase, PDK4, PDP1, glucose oxidation, glycolysis, metabolome, conditional knockout mice

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Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock

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