Cited by 145Muscle Physiology and DisordersCircadian rhythm and melatoninGenetics, Aging, and Longevity in Model Organisms

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Intrinsic muscle clock is necessary for musculoskeletal health

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Schroder, Elizabeth A., Harfmann, Brianna D., Zhang, Xiping, Srikuea, Ratchakrit, England, Jonathan H., Hodge, Brian A., Wen, Yuan, Riley, Lance A., Yu, Qi, Christie, Alexander, Smith, Jeffrey D., Seward, Tanya, Wolf Horrell, Erin M., Mula, Jyothi, Peterson, Charlotte A., Butterfield, Timothy A., Esser, Karyn A.·2015·The Journal of Physiology

DOI 10.1113/jp271436PMC PMC4704520

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Abstract

KEY POINTS: The endogenous molecular clock in skeletal muscle is necessary for maintenance of phenotype and function. Loss of Bmal1 solely from adult skeletal muscle (iMSBmal1(-/-) ) results in reductions in specific tension, increased oxidative fibre type and increased muscle fibrosis with no change in feeding or activity. Disruption of the molecular clock in adult skeletal muscle is sufficient to induce changes in skeletal muscle similar to those seen in the Bmal1 knockout mouse (Bmal1(-/-) ), a model of advanced ageing. iMSBmal1(-/-) mice develop increased bone calcification and decreased joint collagen, which in combination with the functional changes in skeletal muscle results in altered gait. This study uncovers a fundamental role for the skeletal muscle clock in musculoskeletal homeostasis with potential implications for ageing. ABSTRACT: Disruption of circadian rhythms in humans and rodents has implicated a fundamental role for circadian rhythms in ageing and the development of many chronic diseases including diabetes, cardiovascular disease, depression and cancer. The molecular clock mechanism underlies circadian rhythms and is defined by a transcription-translation feedback loop with Bmal1 encoding a core molecular clock transcription factor. Germline Bmal1 knockout (Bmal1 KO) mice have a shortened lifespan, show features of advanced ageing and exhibit significant weakness with decreased maximum specific tension at the whole muscle and single fibre levels. We tested the role of the molecular clock in adult skeletal muscle by generating mice that allow for the inducible skeletal muscle-specific deletion of Bmal1 (iMSBmal1). Here we show that disruption of the molecular clock, specifically in adult skeletal muscle, is associated with a muscle phenotype including reductions in specific tension, increased oxidative fibre type, and increased muscle fibrosis similar to that seen in the Bmal1 KO mouse. Remarkably, the phenotype observed in the iMSBmal1(-/-) mice was not limited to changes in muscle. Similar to the germline Bmal1 KO mice, we observed significant bone and cartilage changes throughout the body suggesting a role for the skeletal muscle molecular clock in both the skeletal muscle niche and the systemic milieu. This emerging area of circadian rhythms and the molecular clock in skeletal muscle holds the potential to provide significant insight into intrinsic mechanisms of the maintenance of muscle quality and function as well as identifying a novel crosstalk between skeletal muscle, cartilage and bone.

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PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues
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
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
Transcriptional architecture and chromatin landscape of the core circadian clock in mammals
Koike, N., Yoo, S.-H., Huang, H.-C., Kumar, V., Lee, C., Kim, T.-K., & Takahashi, J. S. (2012) · Science · doi:10.1126/science.1226339 · Cited by 1,464
Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review
Mitchell, W. K., Williams, J., Atherton, P., Larvin, M., Lund, J., & Narici, M. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00260 · Cited by 1,377
Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock
Kondratov, R. V., Kondratova, A. A., Gorbacheva, V. Y., Vykhovanets, O. V., & Antoch, M. P. (2006) · Genes & Development · doi:10.1101/gad.1432206 · Cited by 1,188
JTK_CYCLE: An Efficient Nonparametric Algorithm for Detecting Rhythmic Components in Genome-Scale Data Sets
Hughes, M. E., Hogenesch, J. B., & Kornacker, K. (2010) · Journal of Biological Rhythms · doi:10.1177/0748730410379711 · Cited by 1,087
Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms
Talmadge, R. J., & Roy, R. R. (1993) · Journal of Applied Physiology · doi:10.1152/jappl.1993.75.5.2337 · Cited by 804
Contractile properties of skeletal muscles from young, adult and aged mice.
Brooks, S. V., & Faulkner, J. A. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp017279 · Cited by 777 · cited 1×
“Physiological cross-sectional area was estimated according to Brooks & Faulkner (1988) and used to calculate specific force.”
Method
Health in a 24-h society
Rajaratnam, S. M., & Arendt, J. (2001) · The Lancet · doi:10.1016/s0140-6736(01)06108-6 · Cited by 711
Muscle type and fiber type specificity in muscle wasting
Ciciliot, S., Rossi, C. A., Dyar, K. A., Blaauw, B., & Schiaffino, S. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.05.016 · Cited by 644

Show all 80 references

Research works printed but not linked: 2

10.1111/j.1469-7793.2003.00499.x · DOI
Harrison DE, 2011, Life Span as a Biomarker

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Authors: Schroder, E. A., Harfmann, B. D., Zhang, X., Srikuea, R., England, J. H., Hodge, B. A., Wen, Y., Riley, L. A., Yu, Q., Christie, A., Smith, J. D., Seward, T., Wolf Horrell, E. M., Mula, J., Peterson, C. A., Butterfield, T. A., & Esser, K. A.
Affiliations: University of Kentucky (US)
Center for Muscle Biology University of Kentucky Lexington KY USA
Corresponding author: Esser, Karyn A.
ORCID: Schroder, Elizabeth A.
Harfmann, Brianna D.
Zhang, Xiping
Srikuea, Ratchakrit
Hodge, Brian A.
Wen, Yuan
Riley, Lance A.
Yu, Qi
Christie, Alexander
Smith, Jeffrey D.
Peterson, Charlotte A.
Butterfield, Timothy A.
Esser, Karyn A.
Venue: The Journal of Physiology
Publisher: Wiley
Published: 2015-11-23
Volume: 593
Issue: 24
Pages: 5387-5404
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jp271436
PMC: PMC4704520
OpenAlex: W2100177722
Cited by: 145
References: 80
Citations by year: 2026: 12 · 2025: 17 · 2024: 21 · 2023: 11 · 2022: 13 · 2021: 16 · 2020: 16 · 2019: 9 · 2018: 8 · 2017: 10 · 2016: 12
FWCI: 4.34
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (T32CA165990)
National Institute of Environmental Health Sciences (RC1ES018636)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR066082)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords: circadian clock, Bmal1, skeletal muscle, muscle-specific knockout, muscle fiber type, muscle fibrosis, muscle strength, bone mineralization, aging, gait
MeSH terms: Animals, Biological Clocks, Bone and Bones, Calcinosis, Collagen, Fibrosis, Gait, Joints, Mice, Inbred C57BL, Phenotype, Muscle, Skeletal, Mice, ARNTL Transcription Factors

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Intrinsic muscle clock is necessary for musculoskeletal health

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